Clinical implication of fasting glucose and systolic/diastolic blood pressure on the prevalence of periodontitis in non‑diabetic and non‑hypertensive adults using nationally representative data
- Authors:
- Published online on: June 7, 2018 https://doi.org/10.3892/etm.2018.6260
- Pages: 671-678
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Copyright: © Han et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
Introduction
Previous studies have shown that systemic diseases are known to be associated with periodontitis (1). The prevalence of both diabetes mellitus and hypertension is increasing worldwide (2). Diabetes and hypertension are widely studied for possible association with periodontitis (3,4). The rapid increase in the prevalence of diabetes is also seen in Korea (5). The prevalence of diabetes among adults aged ≥30 years in 2001, 2005 and 2007–2009 was 8.9, 9.1 and 9.9%, respectively based on the series of Korea National Health and Nutrition Examination Surveys (5). The report with more current results showed that the prevalence of diabetes increased up to 11.0% in 2013 (6). Complication of diabetes includes diabetic retinopathy, diabetic nephropathy, diabetic neuropathy and macrovascular diseases (7). Previous report showed that the prevalence of hypertension was 28.5% in the Korean National Health and Nutrition Examination Survey in 2011 (8). The report indicated that the awareness, treatment, and control rates of the generation population were generally improved. Researchers have shown that a relationship exists between type 2 diabetes mellitus and periodontal disease (9). Glycemic control has been shown to affect periodontal disease and participants having poorly controlled diabetes were associated with severe periodontitis (10). Similarly, a positive association has been reported between hypertension and periodontitis (4). All periodontal measures had significant associations with hypertension (11).
However, the association between impaired fasting glucose or high blood pressure and periodontitis in individuals without diabetes or hypertension is not yet well understood. Thus, this study was performed to assess the relationship between fasting glucose and systolic/diastolic blood pressure on the prevalence of periodontitis in non-diabetic and non-hypertensive adults using nationally representative data. Subgroup analysis was performed to evaluate the combined effects of obesity/abdominal obesity and impaired fasting glucose.
Materials and methods
Survey and subjects
This survey was reviewed and approved by the Institutional Review Board of the Korean Centers for Disease Control and Prevention, and all participants provided written informed consent. This study is a secondary data analysis of data collected during the Korean National Health and Nutrition Examination Survey (KNHANES) from 2013 to 2015. The Institutional Review Board at the Catholic University of Korea approved of this study (KC16EISI0713). This study is a human observational study and the authors have conformed to the STROBE guidelines.
A total of 22,948 individuals participated in the KNHANES survey. The number of surveys was reduced to 13,401 by excluding participants without periodontal examination, participants with less than 8 h of fasting before examination, and individuals who were younger than 19 years old. The analysis in this study was confined to a total of 8,341 responses that had no missing values for the outcome variables (Fig. 1).
Demographic variables
Sociodemographic and lifestyle variables of participants were evaluated with a self-administered questionnaire regarding education level, household income, smoking, and alcohol intake. Smokers were classified as current smokers or non-smokers. Alcohol consumption was categorized as drinkers [mild to moderate drinkers (1–30 g/day)], and heavy drinkers (>30 g/day), or non-drinkers. Education level was categorized as either entered high school (≥10 years) or not. Number of household members was evaluated. Household income was divided into quartiles by number of included family members. The lowest quartile of household income was less than 1,092.40 USD/month.
Anthropometric measurements
Trained staff members performed the measurements of the participants. Heath status of each participant was evaluated. Body weight and height were measured with the participants in light indoor clothing without shoes (12). Waist circumference was measured at the narrowest point between the lower border of the rib cage and the iliac crest. Body mass index was calculated by the following formula: weight/height2 (kg/m2). Systolic blood pressure and diastolic blood pressure were measured on the right arm using a standard mercury sphygmomanometer (Baumanometer; W.A. Baum Co., Inc., Copiague, NY, USA). Systolic blood pressure and diastolic blood pressure measurements were performed two times with a 5-min interval, and the average of the two measurements was used for the analysis.
After fasting for more than 8 h, blood samples were collected from the antecubital veins. Serum fasting plasma glucose, glycated hemoglobin, the total concentration of cholesterol, low-density lipoprotein, and triglycerides were tested with the Automatic Analyzer 7600 (Hitachi, Tokyo, Japan) using the kits (Daiichi, Tokyo, Japan) (13).
Description of obesity, diabetes mellitus, and hypertension
Body mass index was categorized by ≥25 kg/m2 or lower. Waist circumference was categorized as ≥90 cm in men and ≥80 cm in women. A body mass index (BMI) ≥25 kg/m2 was defined as the presence of obesity (14), and the cutoffs of abdominal obesity were defined as waist circumference (WC) ≥90 cm in men or ≥85 cm in women (15). Diabetes was diagnosed if fasting blood sugar was ≥126 mg/dl, glycated hemoglobin was ≥6.5% or the individual was currently using antidiabetic medications (16). Impaired fasting glucose was defined as a level of blood glucose between 100 and 125 mg/dl with no diabetic medication. Hypertension was defined as systolic blood pressure ≥140 mmHg and diastolic blood pressure was ≥90 mmHg or reported use of regular antihypertensive drugs (17). Metabolic syndrome was diagnosed if three or more of the following criteria were fulfilled: waist circumference ≥90 cm in men and ≥80 cm in women; fasting triglycerides ≥150 mg/dl or use of lipid-lowering medication; high-density lipoprotein cholesterol <40 mg/dl in men and <50 mg/dl in women or use of lipid-lowering medication; blood pressure ≥130/85 mmHg or use of antihypertensive medication; and fasting blood glucose ≥100 mg/dl or current use of antidiabetic medication (18).
Oral health behaviors and periodontitis
Periodontal treatment needs were assessed using the Community Periodontal Index (CPI), which the World Health Organization/Federation Dentaire Internationale has defined as an epidemiological screening procedure for rough depiction of periodontal status and treatment needs by trained dental practitioners (19). All teeth of each subject were divided into sextants. A specially designed periodontal probe (PWHO, Osung MND, Seoul, Republic of Korea) with a ball end 0.5 mm in diameter was used. Ten specific index teeth (17, 16, 11, 26, 27, 36, 37, 31, 46 and 47) were examined to evaluate each sextant's score. A sextant was only scanned if two or more teeth were present. If index teeth were absent from a sextant, then all of the remaining teeth were examined to produce the score, and the highest score was recorded as the score for the sextant. Code 3 was used for a shallow pocket with depth of 3.5–5.5 mm and code 4 for a deep pocket depth ≥5.5 mm. Moderate periodontal disease was defined if CPI was code 3 and severe periodontitis was defined if CPI was code 4. Presence of periodontitis was defined if CPI was 3 or greater.
The frequency of daily tooth brushing and use of secondary oral products were used for the evaluation of oral health behavior. Secondary oral products included dental floss, mouthwash, interdental brushes, electric toothbrushes, irrigation devices, tongue cleaners, end-tufted brushes, and special devices for dentures. The survey also recorded the participants' tooth pain.
Statistical analysis
All analyses were conducted using SAS version 9.3 (SAS Institute Inc., Cary, NC, USA). The SAS survey procedure was applied to reflect the complex sampling design and the sampling weights of KNHANES and to provide nationally representative prevalence estimates. The data are presented as the mean ± standard error of the mean for continuous variables and as proportions (standard errors) for categorical variables. A Chi-square test for categorical variables or an independent t-test for continuous variables was performed to assess the differences in characteristics categorized by presence of periodontitis. Logistic regression analysis was used to evaluate the periodontitis in association with impaired fasting glucose categorized by the presence of obesity or abdominal obesity. The model was adjusted for age, sex, smoking, drinking, education, income, body mass index, number of natural teeth, frequency of tooth brushing per day, and use of secondary oral products.
Results
Table I shows the baseline characteristics of study participants according to the presence of periodontitis. Among the 8,341 participants, 1,968 were diagnosed as having periodontitis. The percentage of males was higher in periodontitis group (P<0.05). The systolic blood pressure, diastolic blood pressure, glucose level, glycated hemoglobin, body mass index, total cholesterol, low-density lipoprotein, and triglycerides were statistically higher in the periodontitis group (P<0.05). The numbers of current smokers and individuals with lower income or tooth pain were higher in the periodontitis group. However, the percentage of individuals with tooth brushing frequency of three or higher per day and the percentage of individuals using secondary oral products were significantly lower in the periodontitis group (P<0.05).
The percentage of moderate and severe periodontitis categorized by blood pressure and glucose level is shown in Fig. 2. The percentage of periodontitis increased with increasing systolic blood pressure. Similar trends were seen with diastolic blood pressure. The percentage of periodontitis increased with higher glucose level, with similar trends in glycated hemoglobin.
The prevalence of periodontitis in the combination of obesity/abdominal obesity and impaired fasting glucose level is shown in Fig. 3. Fig. 3A shows odds ratios (ORs) of periodontitis categorized by the presence of obesity and impaired fasting glucose. Even for participants without obesity, the ORs increased to 1.311. For participants with obesity having impaired fasting glucose, the ORs of periodontitis increased to 1.523. Similar trends were seen with participants with abdominal obesity (Fig. 3B). ORs for participants without abdominal obesity having impaired glucose, participants with abdominal obesity with normal glucose level, and individuals having combination of abdominal obesity and impaired fasting glucose were 1.320, 1.297 and 1.434, respectively, when a non-abdominally obese individual with normal fasting glucose was considered as reference.
Fig. 4 shows ORs and 95% confidence intervals (CIs) of periodontitis after adjustments for age, sex, smoking, drinking, education, income, body mass index, waist circumference, chronic kidney disease, number of natural teeth, frequency of tooth brushing per day, and use of secondary oral products.
Table II shows the ORs and 95% CIs of periodontitis categorized by systolic blood pressure, diastolic blood pressure, glucose, and glycated hemoglobin. The ORs and 95% CIs for systolic blood pressure of 90≤x<100, 100≤x<110, 110≤x<120, 120≤x<130, and 130≤x<140 were 1.116 (0.591, 2.107), 1.165 (0.624, 2.175), 1.238 (0.673, 2.278), 1.008 (0.538, 1.888), and 1.042 (0.545, 1.993), respectively, when systolic blood pressure <90 was considered as reference. The ORs and 95% CIs for diastolic blood pressure of 65≤x<70, 70≤x<75, 75≤x<80, 80≤x<85, and 85≤x<90 were 1.192 (0.94, 1.511), 1.324 (1.049, 1.67), 1.152 (0.905, 1.467), 1.188 (0.931, 1.516), and 1.263 (0.937, 1.702), respectively, when diastolic blood pressure <65 was considered as reference. The ORs and 95% CIs for glucose of 90≤x<100, 100≤x<110, and 110≤x<126 were 1.074 (0.92, 1.253), 1.214 (0.986, 1.494), and 1.358 (1.005, 1.834), respectively, when glucose <90 was considered as reference. The ORs and 95% CIs for glycated hemoglobin 5≤x<5.5, 5.5≤x<6, and 6≤x<6.5 were 0.887 (0.583, 1.348), 0.853 (0.559, 1.301), and 1.021 (0.652, 1.599), respectively, when glycated hemoglobin <5 was considered as reference.
 | Table II.Odds ratios and 95% confidence interval for periodontitis categorized by systolic blood pressure, diastolic blood pressure, glucose and glycated hemoglobin. |
Discussion
This study showed that both impaired fasting glucose and prehypertension were associated with periodontitis by multiple logistic regression analyses after adjusting for confounding factors among Korean adults. Subgroup analysis revealed that ORs of periodontitis increased in impaired fasting glucose in both non-obese and obese participants. Highest ORs were seen with the combination of impaired fasting glucose and obesity/abdominal obesity.
Various parameters can be used to determine impaired fasting glucose and prehypertension (17,20–24). Impaired fasting glucose was defined as a level of blood glucose between 100 and 125 mg/dl with no diabetic medication (17). The criteria for the World Health Organization is 110≤x<125 mg/dl (20). Regarding hypertension, if the participants were ≥60 years old, then average blood pressure of 150/90 mmHg or lower was considered as controlled, and the criteria of blood pressure <140/90 mmHg was considered controlled for individuals younger than 60 (21). A previous report recommended lower targets for individuals with diabetes mellitus of 130/80 mmHg (22). In a previous study, prehypertension was defined as systolic blood pressure between 120 and 139 mmHg or diastolic blood pressure between 80 to 89 mmHg (23). In another study, participants with repeated measurements of systolic pressure of 130 to 139 mmHg and diastolic pressure of 89 mmHg or lower, or systolic pressure of 139 mmHg or lower and diastolic pressure of 85 to 89 mmHg, were assigned to the treatment of prehypertension (24). In this study, we classified the glucose level and glycated hemoglobin into four stages according to the severity. Systolic and diastolic blood pressure was categorized into six stages according to the severity.
A previous report recommended initiating treatment in adults aged 60 years or older with systolic blood pressure persistently at or above 150 mmHg to achieve a target systolic blood pressure of less than 150 mmHg to reduce the risk for mortality, stroke, and cardiac events (25). However, it was noted that evidence was low in quality for achieving a target systolic blood pressure of less than 140 mmHg to reduce the risk of stroke or cardiac events. Similarly, another report showed that more intensive blood pressure-lowering treatment of a group with mean blood pressure level of 133/76 mmHg resulted in no clear effects on total mortality, cardiovascular death, heart failure, or end-stage renal disease (26). Fewer studies have been performed regarding prehypertension and it was shown that prehypertension was considered a precursor of stage 1 hypertension and a predictor of excessive cardiovascular risk (24). Prevalence of periodontitis in the prehypertension group increased from 25.8% for systolic blood pressure of 120≤x<130 mmHg and 34.2% for 130≤x<140 mmHg, respectively. Prevalence of periodontitis in the prehypertension group increased from 25.2 to 27.4% for diastolic blood pressure of 80≤x<85 and 85≤x<90 mmHg, respectively.
A previous report showed pre-diabetes related to impaired fasting glucose was positively associated with periodontitis (27). Research has also shown that periodontitis showed an association with decreased β-cell function and increased prevalence of impaired fasting glucose before onset of diabetes (28). It was also shown that chronic periodontitis measured by clinical attachment loss and pocket depth was positively associated in a linear relation with impaired fasting glucose (28). This study also showed that the percentage of periodontitis increased from 22.0% for fasting glucose level of 90≤x<100 mg/dl, 30.7% for fasting glucose level of 100≤x<110 mg/dl, and 37.3% for fasting glucose level of 110≤x<126 mg/dl. ORs of periodontitis increased with impaired fasting glucose and combination of obesity and impaired fasting glucose showed the highest ORs of 1.523. The relative increase of ORs of impaired fasting glucose for periodontitis was 1.311 for no obesity but 1.137 for the obesity group. Similar trends were seen regarding abdominal obesity. The relative increase of ORs of impaired fasting glucose for periodontitis was 1.320 for no abdominal obesity but 1.106 for the abdominal obesity group. It should also be considered that more care may be given to prehypertensive individuals with impaired fasting glucose (23).
This study emphasized the importance of evaluation and treatment of periodontitis in individuals with prediabetes and prehypertension. This study has great strength because the conclusion was derived from nationally representative data (29). The design of this study is based on a stratified, multistage, probability-cluster survey of the population of institutionalized civilians (30). Oral health was evaluated using periodontal index from index teeth using probing depth (31). A multiple regression analysis was used to evaluate periodontitis in relation to impaired fasting glucose and blood pressure after adjustment for various confounding factors including age, sex, smoking, drinking, socioeconomic factors, oral health behavior, and systemic diseases (32). However, it should be noted that the causal direction of the associations between prediabetes/prehypertension and periodontitis cannot be ascertained due to the design of this study being cross-sectional (33).
The association between fasting glucose/blood pressure and periodontitis was proven by multiple logistic regression analyses after adjusting for confounding factors among non-diabetic and non-hypertensive Korean adults. Subgroup analysis showed that higher ORs of periodontitis were noted in participants having both impaired glucose level and obesity when compared with individuals without impaired glucose level or obesity. Further prospective studies with a larger sample size of individuals over a longer period of time are required to evaluate the cause-and-effect association. The results of the present study suggest that detection of fasting glucose and blood pressure may serve as a risk indicator for periodontal disease.
Acknowledgements
The authors thank the Korea Centers for Disease Control and Prevention for providing the necessary data.
Funding
This study was supported by Research Fund of Seoul St. Mary's Hospital, The Catholic University of Korea. This work was partly supported by Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Science, ICT & Future Planning, Daejeon, Republic of Korea (grant no. NRF-2017R1A1A1A05001307).
Availability of data and materials
All data generated or analyzed during this study are included in this published article.
Authors' contributions
KH and JP collaborated to design the study; KH and JP were responsible for data access and analysis; KH and JP wrote the manuscript; both authors reviewed the manuscript.
Ethics approval and consent to participate
The Institutional Review Board at the Catholic University of Korea approved this study (approval no. KC16EISI0713).
Patient consent for publication
Not applicable.
Competing interests
The authors confirm that they have no competing interests.
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