Community Dent Oral Epidemiol 2015; 43; 471–478 All rights reserved
Ó 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Association between vitamin D deficiency and periodontal status in current smokers
Hyo-Jin Lee1,2, Dong-Il Je3, Seong-Jae Won3, Dai-Il Paik1,2 and Kwang-Hak Bae1,2 1 Department of Preventive and Public Health Dentistry, School of Dentistry, Seoul National University, Seoul, Korea, 2Dental Research Institute, School of Dentistry, Seoul National University, Seoul, Korea, 3Korean Minjok Leadership Academy, Gangwon-do, Korea
Lee H-J, Je D-I, Won S-J, Paik D-I, Bae K-H. Association between vitamin D deficiency and periodontal status in current smokers. Community Dent Oral Epidemiol 2015; 43: 471–478. © 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Abstract – Objectives: The aim of this study was to examine whether vitamin D level is associated with periodontitis using a representative sample of Korean adults. Methods: A total of 6011 subjects who participated in the fourth Korea National Health and Nutrition Examination Survey (KNHANES) were examined. Vitamin D deficiency was defined as 25-hydroxyvitamin D serum concentrations to be under or equal to 20 ng/ml. We assessed periodontal conditions by Community Periodontal Index (CPI) and defined higher CPI as ≥code 3. Multivariate logistic regression analyses were performed adjusting for sociodemographics, oral and general health behaviors, and systemic health status. All analyses considered a complex sampling design, and a subgroup analysis was performed to determine estimates stratified according to the effect modifier. Results: There was no association between vitamin D deficiency and higher CPI after adjusting for the covariates in the total sample. According to the strata of smoking, the significant association was found in only current smokers after adjusting for the covariates including pack-years (odds ratio: 1.53, 95% confidence interval: 1.07–2.18). Conclusions: A significant association between vitamin D deficiency and periodontal status was found in only current smokers. Smoking could modify the effect of vitamin D on periodontitis.
Periodontitis is a chronic inflammatory disease caused by a bacterial infection of the supporting tissues around the teeth. It can result in the formation of soft tissue pockets, loss of connective tissue and bone support, loosening of teeth, pain, and impaired mastication (1, 2). Periodontal disease is one of the most common chronic diseases in the world, and it is also one of the main causes necessitating an extraction of permanent teeth (3, 4). Vitamin D is a fat-soluble vitamin that can be synthesized within the human skin when exposed to adequate sunlight (5), which makes it unique from other essential vitamins that require outer intake through food or artificial insertion. Vitamin D is essential for regulating the metabolism of calcium and phosphorous and also for regulating the level of parathyroid hormone (6); hence, it doi: 10.1111/cdoe.12173
Key words: epidemiology; nutrition; periodontitis; smoking; vitamin D Kwang-Hak Bae, 28, Yeongun-dong, Jongnogu, Seoul, 110-749, Korea Tel.: +82 2 740 8747 Fax: +82 2 765 1722 e-mail: [email protected] Submitted 27 April 2014; accepted 5 May 2015
maintains bone health (7). Moreover, vitamin D has protective associations with conditions such as osteoporosis, hypertension, cardiovascular disease, diabetes, and cancer (5, 8, 9), because it may act as a modulator of inflammatory responses. Unfortunately, vitamin D deficiency is widely prevalent. It has been estimated in approximately 1 billion people around the world (8). In Korea, the prevalence of vitamin D deficiency (defined as ≤20 ng/ml) for adults aged ≥19 years was 69.0% in 2009 according to the Korea National Health and Nutrition Examination Survey (KNHANES) (10). Recent studies reported that vitamin D deficiency may affect the periodontal health (11–13). Dietrich et al. (14) reported that low vitamin D levels were associated with periodontitis independently of bone mineral density among US adults.
471
Lee et al.
Alshouibi et al. (15) found that the vitamin D intake was associated with periodontal health. Because vitamin D has both immunomodulatory effects and an effect on bone mineral density (14, 16, 17), it may influence the development of periodontal disease. In recent years, several studies have reported the association between the polymorphism of vitamin D receptor (VDR) genes and periodontitis (11) through its effects on bone metabolism and immune functions (18, 19). When investigating the periodontitis-associated factors, effect modification needs to be considered in an appropriate manner in epidemiological studies as multivariate models with a single estimate requiring homogeneity of the effects across the different levels of the extraneous variables such as gender and smoking (20). However, there are few studies on the association between vitamin D deficiency and periodontitis based on a nationally representative sample considering smoking as an effect modifier. Therefore, the purpose of this study was to examine whether vitamin D level is associated with periodontitis considering the effect modifiers among a representative sample of Korean adults adjusted for sociodemographics, oral and general health behaviors, and systemic health status.
Materials and methods Study design and subject selection The study data include a subset of the KNHANES conducted by the Korea Center for Disease Control and Prevention (KCDC) in 2009. The sampling protocol for the KNHANES was designed to involve a complex, stratified, multistage, and probabilitycluster survey of a representative sample of the noninstitutionalized civilian population in Korea. The survey was performed by the Korean Ministry of Health and Welfare. The target population of the survey included all noninstitutionalized civilian Korean individuals aged 1 year or older. The survey used stratified multistage probability sampling units based on geographic area, gender, and age, which were determined based on the household registries of the 2005 National Census Registry, the most recent 5-year national census in Korea. Using the 2005 census data, 200 primary sampling units (PSU) were selected across Korea. The final sample set for KNHANES included 4600 households. A detailed description of the sampling can be found in the KNHANES report (21). A total of 10 533
472
participants aged 19 years and over participated in KNHANES and provided data for one or more of the variables (periodontitis and confounders). Of them, 6011 subjects were measured to evaluate vitamin D in blood and periodontitis. Written informed consent was obtained from all participants.
Clinical variables Periodontal status. We used the World Health Organization (WHO) community periodontal index (CPI) to assess periodontal conditions and defined higher CPI as a CPI greater than or equal to ‘code 3’. A CPI score of code 3 indicates that at least one site had a probing pocket depth (PD) greater than 3.5 mm (code 4 greater 5.5 mm) in the index teeth. The index tooth numbers were 11, 16, 17, 26, 27, 31, 36, 37, 46, and 47 according to the Federation Dentaire Internationale (FDI) system. A specially designed, lightweight CPI probe was used that met WHO guidelines (22). A sextant was examined only if there were at least two teeth present not scheduled for extraction. If no index teeth were present in a sextant qualifying for examination, all remaining teeth were examined and the highest score was recorded as the score for that sextant. An approximately 20 g probing force was used. The probe tip was gently inserted into the gingival sulcus or pocket, and the total extent of the sulcus or pocket was explored. Thirteen trained dentists examined the periodontal status of the subjects in the 2009 KNHANES. The interexaminer mean of Kappa value was 0.75 (0.53–0.94). Vitamin D levels. Vitamin D levels were measured by the whole blood levels (ng/ml), which were analyzed with 1 ml sample of blood from each subject based on radioimmunoassay (23). Vitamin D from the skin and diet is metabolized in the liver to 25-hydroxyvitamin D (25(OH)D) that is used to determine a patient’s vitamin D status (24). Vitamin D deficiency was defined as 25(OH)D serum concentrations to be below or equal to 20 ng/ml. This cut-point follows the suggestions of the Institute of Medicine (IOM) and the Pediatric Endocrine Society and is equivalent to the standards used in many laboratories (25). Covariates. The covariates were categorized into three groups. The first group consisted of sociodemographic variables: age, gender, educational level, and household income. The educational level
Vitamin D deficiency and periodontal status
was assessed by the highest diploma. The household income was the monthly average family income. It was adjusted for the number of family members and was categorized into four quartiles from top to bottom. The second group included variables related to oral and general health behaviors, such as use of floss, use of interproximal tooth brush, alcohol consumption experience in a lifetime, and pack-years. Amount of smoking was defined as the average number of cigarettes per day they have smoked or had smoked prior to quitting. Pack-years were calculated by multiplying the number of packs of cigarettes smoked per day by the number of years the person has smoked or had smoked prior to quitting (pack-years = amount of smoking [cigarettes/ day] 9 period of smoking (y)/20). The third group included variables related to the systemic health status such as vitamin D level, diabetes, obesity, and dietary conditions. Dietary conditions were assessed using a self-administration questionnaire survey to measure food security related to dietary diversity. It was categorized into four groups according to food insufficiency in a recent year (Enough and diverse: enough of the kinds of food we want to eat, Enough but not diverse: enough but not always the kinds of food we want, Sometimes insufficient: sometimes not enough to eat, Insufficient: often not enough to eat). Sociodemographic variables, oral and general health behaviors, and systemic health status were examined using a self-administration questionnaire survey.
Statistical analyses Individual weighted factors were used, and the complex sampling design of the survey was considered to obtain the variances. A multivariate logistic regression analysis was applied to examine the associations between vitamin D level and CPI, adjusted for the effects of the above-mentioned covariates in the logistic model. A subgroup analysis was performed to determine estimates stratified according to the effect modifier as the interaction terms of periodontitis with smoking were significant. The subjects were divided into two groups for the subgroup analysis according to current smoking status (Yes: those who were currently smoking and had smoked 100 cigarettes or more in their whole life, No: those who had never smoked or had smoked fewer than 10 cigarettes in their life or those who had smoked in the past but stopped smoking at that time). The statistical analyses were
performed using SPSS version 21.0 software (SPSS, Chicago, IL, USA).
Results Table 1 lists the characteristics of the study subjects categorized by the periodontal status. The demographic characteristics of the subjects were as follows: the mean age was 40.61 0.41 years in the lower CPI group and 51.82 0.53 years in the higher CPI group. The percentage of higher CPI in males (36.8%) was higher than females (25.3%), and the crude odds ratio (OR) of males for higher CPI was 1.05 [95% confidence interval (CI): 1.04– 1.05]. The percentage of higher CPI was 29.1% in the vitamin D deficiency group and 35.0% in nonvitamin D deficiency group, and the crude OR of vitamin D deficiency for higher CPI was 0.76 (95% CI: 0.64–0.91). Pack-years were 5.12 0.19 per day in lower CPI group and 12.16 0.45 per day in the higher CPI group. Table 2 shows the characteristics of the study subjects categorized by the current smoking status. The mean age was 41.07 0.50 years in current smokers and 46.15 0.43 years in noncurrent smokers. The current smokers were 26.1% in the vitamin D deficiency group and 28.6% in non-vitamin D deficiency group. The percentage of current smokers in the higher CPI groups (32.6%) was higher than the lower CPI group (23.9%). The results of the subgroup analyses are presented as smoking status was a significant effect modifier (Table 3). The association was different according to the strata of current smoking. In current smokers, subjects with vitamin D deficiency were 1.53 (95% CI: 1.07–2.18) times more likely to have a higher CPI than those without vitamin D deficiency. However, the vitamin D levels were not associated with a higher CPI in noncurrent smokers.
Discussion This study was conducted to examine the association between vitamin D deficiency and periodontal status. An association was revealed between vitamin D deficiency and a higher CPI after adjusting for sociodemographics, oral and general health behaviors, and systemic health status. However, this association was significant in only current
473
Lee et al. Table 1. Univariate association with sociodemographic characteristics, oral and general health behaviors, and systemic health status based on periodontal status (CPI) Lower CPI Variables
n
Higher CPI % (SE)a
Age (n = 6245) 40.61 0.41c Gender (n = 6245) Male 1543 63.2 (1.3) Female 2678 74.7 (1.1) Highest diploma (n = 6210) Primary school 966 52.7 (2.0) Middle school 428 59.0 (2.5) High school 1583 73.2 (1.3) ≥University or college 1221 76.2 (1.3) Household incomed (n = 6184) 75% 1294 74.6 (1.3) Use of floss (n = 6234) No 3554 67.4 (1.1) Yes 658 78.1 (1.5) Use of interproximal tooth brush (n = 6234) No 3654 69.3 (1.1) Yes 558 66.5 (2.1) Pack-years (n = 6232) 5.12 0.19c Alcohol consumption experience in a lifetime (n = 5291) No 2519 72.4 (1.2) Yes 1101 65.7 (1.4) Vitamin D deficiency (n = 6011)e Yes (≤20 ng/ml) 2766 70.9 (1.2) No (>20 ng/ml) 1307 65.0 (1.7) Diabetes (n = 5829) Normal 3039 73.8 (1.0) Impaired fasting glucose 619 57.7 (2.0) Diabetes 288 49.6 (2.5) Obesity (n = 6200) Underweight 201 77.9 (2.8) Normal 2705 70.7 (1.1) Obese 1275 63.8 (1.5) Dietary conditions (n = 6245) Enough and diverse 1803 72.1 (1.3) Enough but not diverse 2208 68.2 (1.2) Sometimes insufficient 173 50.0 (3.9) Insufficient 37 54.8 (7.7)
n
% (SE)a 51.82 0.53c
OR (95% CI)b 1.05 (1.04–1.05)
1026 998
36.8 (1.3) 25.3 (1.1)
1.72 (1.53–1.93) Reference
708 295 625 384
47.3 (2.0) 41.0 (2.5) 26.8 (1.3) 23.8 (1.3)
2.87 (2.35–3.50) 2.22 (1.75–2.81) 1.17 (1.00–1.38) Reference
498 513 547 450
38.4 (2.0) 33.6 (1.5) 31.6 (1.7) 25.4 (1.3)
1.83 (1.50–2.25) 1.49 (1.26–1.75) 1.36 (1.15–1.61) Reference
1839 183
32.6 (1.1) 21.9 (1.5)
1.73 (1.45–2.05) Reference
1750 272
30.7 (1.1) 33.5 (2.1) 12.16 0.45c
0.88 (0.72–1.08) Reference 1.03 (1.02–1.03)
1048 623
27.6 (1.2) 34.3 (1.4)
Reference 1.37 (1.19–1.57)
1198 740
29.1 (1.2) 35.0 (1.7)
0.76 (0.64–0.91) Reference
1163 452 268
26.2 (1.0) 42.3 (2.0) 50.4 (2.5)
Reference 2.07 (1.77–2.42) 2.86 (2.34–3.51)
65 1239 715
22.1 (2.8) 29.3 (1.1) 36.2 (1.5)
0.68 (0.49–0.95) Reference 1.36 (1.20–1.56)
743 1088 163 30
27.9 (1.3) 31.8 (1.2) 50.0 (3.9) 45.2 (7.7)
Reference 1.20 (1.05–1.38) 2.58 (1.89–3.54) 2.13 (1.15–3.94)
Weighted percentage standard error. Crude odds ratio and 95% confidence interval for higher CPI. c Weighted mean and standard error. d Household income: monthly average family equivalent income (¼ monthly average household income pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi = ðthe number of household membersÞ. e The vitamin D deficiency was defined as ≤serum 25(OH)D 20 ng/ml based on the suggestion of IOM. a
b
smokers. The results indicate that smoking could modify the effect of vitamin D deficiency on a higher CPI. Several studies have shown associations between vitamin D and periodontal health. Dietrich et al. (14) conducted a study in a large, representative sample of the US population to determine whether serum 25(OH)D3 concentrations were associated with periodontal disease. They found that low
474
serum 25(OH)D3 concentrations may be associated with periodontal disease independently of bone mineral density. Alshouibi et al. (15) performed a survey with 562 older men between 1986 and 1998. They reported that a total intake of at least 800 IU/ day vitamin D was associated with lower odds of periodontal disease than an intake of
Ó 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Association between vitamin D deficiency and periodontal status in current smokers
Hyo-Jin Lee1,2, Dong-Il Je3, Seong-Jae Won3, Dai-Il Paik1,2 and Kwang-Hak Bae1,2 1 Department of Preventive and Public Health Dentistry, School of Dentistry, Seoul National University, Seoul, Korea, 2Dental Research Institute, School of Dentistry, Seoul National University, Seoul, Korea, 3Korean Minjok Leadership Academy, Gangwon-do, Korea
Lee H-J, Je D-I, Won S-J, Paik D-I, Bae K-H. Association between vitamin D deficiency and periodontal status in current smokers. Community Dent Oral Epidemiol 2015; 43: 471–478. © 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Abstract – Objectives: The aim of this study was to examine whether vitamin D level is associated with periodontitis using a representative sample of Korean adults. Methods: A total of 6011 subjects who participated in the fourth Korea National Health and Nutrition Examination Survey (KNHANES) were examined. Vitamin D deficiency was defined as 25-hydroxyvitamin D serum concentrations to be under or equal to 20 ng/ml. We assessed periodontal conditions by Community Periodontal Index (CPI) and defined higher CPI as ≥code 3. Multivariate logistic regression analyses were performed adjusting for sociodemographics, oral and general health behaviors, and systemic health status. All analyses considered a complex sampling design, and a subgroup analysis was performed to determine estimates stratified according to the effect modifier. Results: There was no association between vitamin D deficiency and higher CPI after adjusting for the covariates in the total sample. According to the strata of smoking, the significant association was found in only current smokers after adjusting for the covariates including pack-years (odds ratio: 1.53, 95% confidence interval: 1.07–2.18). Conclusions: A significant association between vitamin D deficiency and periodontal status was found in only current smokers. Smoking could modify the effect of vitamin D on periodontitis.
Periodontitis is a chronic inflammatory disease caused by a bacterial infection of the supporting tissues around the teeth. It can result in the formation of soft tissue pockets, loss of connective tissue and bone support, loosening of teeth, pain, and impaired mastication (1, 2). Periodontal disease is one of the most common chronic diseases in the world, and it is also one of the main causes necessitating an extraction of permanent teeth (3, 4). Vitamin D is a fat-soluble vitamin that can be synthesized within the human skin when exposed to adequate sunlight (5), which makes it unique from other essential vitamins that require outer intake through food or artificial insertion. Vitamin D is essential for regulating the metabolism of calcium and phosphorous and also for regulating the level of parathyroid hormone (6); hence, it doi: 10.1111/cdoe.12173
Key words: epidemiology; nutrition; periodontitis; smoking; vitamin D Kwang-Hak Bae, 28, Yeongun-dong, Jongnogu, Seoul, 110-749, Korea Tel.: +82 2 740 8747 Fax: +82 2 765 1722 e-mail: [email protected] Submitted 27 April 2014; accepted 5 May 2015
maintains bone health (7). Moreover, vitamin D has protective associations with conditions such as osteoporosis, hypertension, cardiovascular disease, diabetes, and cancer (5, 8, 9), because it may act as a modulator of inflammatory responses. Unfortunately, vitamin D deficiency is widely prevalent. It has been estimated in approximately 1 billion people around the world (8). In Korea, the prevalence of vitamin D deficiency (defined as ≤20 ng/ml) for adults aged ≥19 years was 69.0% in 2009 according to the Korea National Health and Nutrition Examination Survey (KNHANES) (10). Recent studies reported that vitamin D deficiency may affect the periodontal health (11–13). Dietrich et al. (14) reported that low vitamin D levels were associated with periodontitis independently of bone mineral density among US adults.
471
Lee et al.
Alshouibi et al. (15) found that the vitamin D intake was associated with periodontal health. Because vitamin D has both immunomodulatory effects and an effect on bone mineral density (14, 16, 17), it may influence the development of periodontal disease. In recent years, several studies have reported the association between the polymorphism of vitamin D receptor (VDR) genes and periodontitis (11) through its effects on bone metabolism and immune functions (18, 19). When investigating the periodontitis-associated factors, effect modification needs to be considered in an appropriate manner in epidemiological studies as multivariate models with a single estimate requiring homogeneity of the effects across the different levels of the extraneous variables such as gender and smoking (20). However, there are few studies on the association between vitamin D deficiency and periodontitis based on a nationally representative sample considering smoking as an effect modifier. Therefore, the purpose of this study was to examine whether vitamin D level is associated with periodontitis considering the effect modifiers among a representative sample of Korean adults adjusted for sociodemographics, oral and general health behaviors, and systemic health status.
Materials and methods Study design and subject selection The study data include a subset of the KNHANES conducted by the Korea Center for Disease Control and Prevention (KCDC) in 2009. The sampling protocol for the KNHANES was designed to involve a complex, stratified, multistage, and probabilitycluster survey of a representative sample of the noninstitutionalized civilian population in Korea. The survey was performed by the Korean Ministry of Health and Welfare. The target population of the survey included all noninstitutionalized civilian Korean individuals aged 1 year or older. The survey used stratified multistage probability sampling units based on geographic area, gender, and age, which were determined based on the household registries of the 2005 National Census Registry, the most recent 5-year national census in Korea. Using the 2005 census data, 200 primary sampling units (PSU) were selected across Korea. The final sample set for KNHANES included 4600 households. A detailed description of the sampling can be found in the KNHANES report (21). A total of 10 533
472
participants aged 19 years and over participated in KNHANES and provided data for one or more of the variables (periodontitis and confounders). Of them, 6011 subjects were measured to evaluate vitamin D in blood and periodontitis. Written informed consent was obtained from all participants.
Clinical variables Periodontal status. We used the World Health Organization (WHO) community periodontal index (CPI) to assess periodontal conditions and defined higher CPI as a CPI greater than or equal to ‘code 3’. A CPI score of code 3 indicates that at least one site had a probing pocket depth (PD) greater than 3.5 mm (code 4 greater 5.5 mm) in the index teeth. The index tooth numbers were 11, 16, 17, 26, 27, 31, 36, 37, 46, and 47 according to the Federation Dentaire Internationale (FDI) system. A specially designed, lightweight CPI probe was used that met WHO guidelines (22). A sextant was examined only if there were at least two teeth present not scheduled for extraction. If no index teeth were present in a sextant qualifying for examination, all remaining teeth were examined and the highest score was recorded as the score for that sextant. An approximately 20 g probing force was used. The probe tip was gently inserted into the gingival sulcus or pocket, and the total extent of the sulcus or pocket was explored. Thirteen trained dentists examined the periodontal status of the subjects in the 2009 KNHANES. The interexaminer mean of Kappa value was 0.75 (0.53–0.94). Vitamin D levels. Vitamin D levels were measured by the whole blood levels (ng/ml), which were analyzed with 1 ml sample of blood from each subject based on radioimmunoassay (23). Vitamin D from the skin and diet is metabolized in the liver to 25-hydroxyvitamin D (25(OH)D) that is used to determine a patient’s vitamin D status (24). Vitamin D deficiency was defined as 25(OH)D serum concentrations to be below or equal to 20 ng/ml. This cut-point follows the suggestions of the Institute of Medicine (IOM) and the Pediatric Endocrine Society and is equivalent to the standards used in many laboratories (25). Covariates. The covariates were categorized into three groups. The first group consisted of sociodemographic variables: age, gender, educational level, and household income. The educational level
Vitamin D deficiency and periodontal status
was assessed by the highest diploma. The household income was the monthly average family income. It was adjusted for the number of family members and was categorized into four quartiles from top to bottom. The second group included variables related to oral and general health behaviors, such as use of floss, use of interproximal tooth brush, alcohol consumption experience in a lifetime, and pack-years. Amount of smoking was defined as the average number of cigarettes per day they have smoked or had smoked prior to quitting. Pack-years were calculated by multiplying the number of packs of cigarettes smoked per day by the number of years the person has smoked or had smoked prior to quitting (pack-years = amount of smoking [cigarettes/ day] 9 period of smoking (y)/20). The third group included variables related to the systemic health status such as vitamin D level, diabetes, obesity, and dietary conditions. Dietary conditions were assessed using a self-administration questionnaire survey to measure food security related to dietary diversity. It was categorized into four groups according to food insufficiency in a recent year (Enough and diverse: enough of the kinds of food we want to eat, Enough but not diverse: enough but not always the kinds of food we want, Sometimes insufficient: sometimes not enough to eat, Insufficient: often not enough to eat). Sociodemographic variables, oral and general health behaviors, and systemic health status were examined using a self-administration questionnaire survey.
Statistical analyses Individual weighted factors were used, and the complex sampling design of the survey was considered to obtain the variances. A multivariate logistic regression analysis was applied to examine the associations between vitamin D level and CPI, adjusted for the effects of the above-mentioned covariates in the logistic model. A subgroup analysis was performed to determine estimates stratified according to the effect modifier as the interaction terms of periodontitis with smoking were significant. The subjects were divided into two groups for the subgroup analysis according to current smoking status (Yes: those who were currently smoking and had smoked 100 cigarettes or more in their whole life, No: those who had never smoked or had smoked fewer than 10 cigarettes in their life or those who had smoked in the past but stopped smoking at that time). The statistical analyses were
performed using SPSS version 21.0 software (SPSS, Chicago, IL, USA).
Results Table 1 lists the characteristics of the study subjects categorized by the periodontal status. The demographic characteristics of the subjects were as follows: the mean age was 40.61 0.41 years in the lower CPI group and 51.82 0.53 years in the higher CPI group. The percentage of higher CPI in males (36.8%) was higher than females (25.3%), and the crude odds ratio (OR) of males for higher CPI was 1.05 [95% confidence interval (CI): 1.04– 1.05]. The percentage of higher CPI was 29.1% in the vitamin D deficiency group and 35.0% in nonvitamin D deficiency group, and the crude OR of vitamin D deficiency for higher CPI was 0.76 (95% CI: 0.64–0.91). Pack-years were 5.12 0.19 per day in lower CPI group and 12.16 0.45 per day in the higher CPI group. Table 2 shows the characteristics of the study subjects categorized by the current smoking status. The mean age was 41.07 0.50 years in current smokers and 46.15 0.43 years in noncurrent smokers. The current smokers were 26.1% in the vitamin D deficiency group and 28.6% in non-vitamin D deficiency group. The percentage of current smokers in the higher CPI groups (32.6%) was higher than the lower CPI group (23.9%). The results of the subgroup analyses are presented as smoking status was a significant effect modifier (Table 3). The association was different according to the strata of current smoking. In current smokers, subjects with vitamin D deficiency were 1.53 (95% CI: 1.07–2.18) times more likely to have a higher CPI than those without vitamin D deficiency. However, the vitamin D levels were not associated with a higher CPI in noncurrent smokers.
Discussion This study was conducted to examine the association between vitamin D deficiency and periodontal status. An association was revealed between vitamin D deficiency and a higher CPI after adjusting for sociodemographics, oral and general health behaviors, and systemic health status. However, this association was significant in only current
473
Lee et al. Table 1. Univariate association with sociodemographic characteristics, oral and general health behaviors, and systemic health status based on periodontal status (CPI) Lower CPI Variables
n
Higher CPI % (SE)a
Age (n = 6245) 40.61 0.41c Gender (n = 6245) Male 1543 63.2 (1.3) Female 2678 74.7 (1.1) Highest diploma (n = 6210) Primary school 966 52.7 (2.0) Middle school 428 59.0 (2.5) High school 1583 73.2 (1.3) ≥University or college 1221 76.2 (1.3) Household incomed (n = 6184) 75% 1294 74.6 (1.3) Use of floss (n = 6234) No 3554 67.4 (1.1) Yes 658 78.1 (1.5) Use of interproximal tooth brush (n = 6234) No 3654 69.3 (1.1) Yes 558 66.5 (2.1) Pack-years (n = 6232) 5.12 0.19c Alcohol consumption experience in a lifetime (n = 5291) No 2519 72.4 (1.2) Yes 1101 65.7 (1.4) Vitamin D deficiency (n = 6011)e Yes (≤20 ng/ml) 2766 70.9 (1.2) No (>20 ng/ml) 1307 65.0 (1.7) Diabetes (n = 5829) Normal 3039 73.8 (1.0) Impaired fasting glucose 619 57.7 (2.0) Diabetes 288 49.6 (2.5) Obesity (n = 6200) Underweight 201 77.9 (2.8) Normal 2705 70.7 (1.1) Obese 1275 63.8 (1.5) Dietary conditions (n = 6245) Enough and diverse 1803 72.1 (1.3) Enough but not diverse 2208 68.2 (1.2) Sometimes insufficient 173 50.0 (3.9) Insufficient 37 54.8 (7.7)
n
% (SE)a 51.82 0.53c
OR (95% CI)b 1.05 (1.04–1.05)
1026 998
36.8 (1.3) 25.3 (1.1)
1.72 (1.53–1.93) Reference
708 295 625 384
47.3 (2.0) 41.0 (2.5) 26.8 (1.3) 23.8 (1.3)
2.87 (2.35–3.50) 2.22 (1.75–2.81) 1.17 (1.00–1.38) Reference
498 513 547 450
38.4 (2.0) 33.6 (1.5) 31.6 (1.7) 25.4 (1.3)
1.83 (1.50–2.25) 1.49 (1.26–1.75) 1.36 (1.15–1.61) Reference
1839 183
32.6 (1.1) 21.9 (1.5)
1.73 (1.45–2.05) Reference
1750 272
30.7 (1.1) 33.5 (2.1) 12.16 0.45c
0.88 (0.72–1.08) Reference 1.03 (1.02–1.03)
1048 623
27.6 (1.2) 34.3 (1.4)
Reference 1.37 (1.19–1.57)
1198 740
29.1 (1.2) 35.0 (1.7)
0.76 (0.64–0.91) Reference
1163 452 268
26.2 (1.0) 42.3 (2.0) 50.4 (2.5)
Reference 2.07 (1.77–2.42) 2.86 (2.34–3.51)
65 1239 715
22.1 (2.8) 29.3 (1.1) 36.2 (1.5)
0.68 (0.49–0.95) Reference 1.36 (1.20–1.56)
743 1088 163 30
27.9 (1.3) 31.8 (1.2) 50.0 (3.9) 45.2 (7.7)
Reference 1.20 (1.05–1.38) 2.58 (1.89–3.54) 2.13 (1.15–3.94)
Weighted percentage standard error. Crude odds ratio and 95% confidence interval for higher CPI. c Weighted mean and standard error. d Household income: monthly average family equivalent income (¼ monthly average household income pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi = ðthe number of household membersÞ. e The vitamin D deficiency was defined as ≤serum 25(OH)D 20 ng/ml based on the suggestion of IOM. a
b
smokers. The results indicate that smoking could modify the effect of vitamin D deficiency on a higher CPI. Several studies have shown associations between vitamin D and periodontal health. Dietrich et al. (14) conducted a study in a large, representative sample of the US population to determine whether serum 25(OH)D3 concentrations were associated with periodontal disease. They found that low
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serum 25(OH)D3 concentrations may be associated with periodontal disease independently of bone mineral density. Alshouibi et al. (15) performed a survey with 562 older men between 1986 and 1998. They reported that a total intake of at least 800 IU/ day vitamin D was associated with lower odds of periodontal disease than an intake of
