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Relationship of Metabolic Syndrome to Periodontal Disease in Japanese Women: The Hisayama Study

¹ Department of Preventive Dentistry, Kyushu University Faculty of Dental Science, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan;
³ Department of Environmental Medicine, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan; and
⁴ Department of Medicine and Clinical Science, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan

^* corresponding author, shimadha{at}mbox.nc.kyushu-u.ac.jp

	ABSTRACT

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Recent studies have suggested that several systemic conditions—such as obesity, hypertension, hyperlipidemia, and diabetes—are related to periodontitis. The objective of this study was to examine the relationship between periodontitis and 5 components of metabolic syndrome—abdominal obesity, triglyceride level, high-density lipoprotein cholesterol level, blood pressure, and fasting blood sugar level—in 584 Japanese women. In multivariate analyses, persons exhibiting more components of metabolic syndrome had significantly higher odds ratios for a greater pocket depth and clinical attachment loss than did those with no components; the odds ratios for a greater pocket depth and clinical attachment loss of the persons exhibiting 4 or 5 components were 6.6 (95% confidence interval = 2.6–16.4) and 4.2 (95% confidence interval = 1.2–14.8), respectively. These results indicate that metabolic syndrome increases risk of periodontitis, and suggest that people exhibiting several components of metabolic syndrome should be encouraged to undergo a periodontal examination.

KEY WORDS: metabolic syndrome • periodontal disease • risk factor • epidemiology • Japanese women

	INTRODUCTION

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Obesity, hypertension, impaired glucose tolerance, and abnormal lipid metabolism have received a great deal of attention as risk factors for arteriosclerotic diseases, including coronary artery disease. The term ’metabolic syndrome’ is commonly used to refer to a condition in which several such components are present in an individual (Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults, 2001). The prevalence of metabolic syndrome is increasing worldwide (Cameron et al., 2004). Although each component of metabolic syndrome independently increases the risk for cardiovascular disease (McGill et al., 2002; The DECODE Study Group, 2003; Eberly et al., 2003; Masley et al., 2006), many studies have reported that an accumulation of these components significantly enhances the risk of death from all causes and cardiovascular disease (Isomaa et al., 2001; Lakka et al., 2002).

Obesity has emerged as a risk indicator of periodontal disease (Saito et al., 2001, 2005), and some studies have reported that individuals with peridontitis had higher blood pressure than individuals without periodontitis (Joss et al., 1994). Furthermore, many studies have reported that periodontitis is more prevalent in persons with diabetes (Page et al., 1997; Soskolne and Klinger, 2001), and that individuals with periodontitis have abnormal lipid metabolism (Losche et al., 2000; Noack et al., 2000; Katz et al., 2002; Moeintaghavi et al., 2005). However, it is unclear whether the accumulation of the components of metabolic syndrome increases the risk of periodontal disease. In this study, we examined the relationship between periodontal disease and the components of metabolic syndrome, singly and in combination, through a community-based health examination held in the town of Hisayama, Fukuoka, Japan.

	MATERIALS & METHODS

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Study Population
From July to September, 1998, a total of 982 Hisayama residents aged 40–79 yrs (21.6% of the total population in that age group) underwent a comprehensive health examination that included a periodontal examination (Saito et al., 2004). In this study, we analyzed 584 women with at least 10 teeth (Saito et al., 2005). The Ethics Committee of the Kyushu University Faculty of Dental Science and the Department of General Affairs and Health and Welfare of Hisayama approved the study design, data collection methods, and procedure for obtaining informed consent.

Oral Examination
Following the method of the Third National Health and Nutrition Examination Survey (Brown et al., 1996), a periodontal examination was performed on randomly selected quadrants, one maxillary and one mandibular. The periodontal examination was carried out by one of four dentists trained to perform a clinical examination of oral health status. The examiner reliability of the periodontal examination was verified by an inter-examiner calibration of outpatients visiting Kyushu University Dental hospital; the kappa value for the periodontal examination exceeded 0.8, suggesting very good inter-examiner agreement (Shimazaki et al., 2004). The pocket depth and clinical attachment loss were measured as periodontal parameters at mesio-buccal and mid-buccal sites for all of the teeth in 2 quadrants. We divided the participants into two groups, based on mean pocket depth: < 2.0 mm (n = 484, 82.9% of all participants) and 2.0 mm (n = 100, 17.1%). Similarly, we divided the participants into two groups based on mean clinical attachment loss: < 3.0 mm (n = 547, 93.7%) and 3.0 mm (n = 37, 6.3%).

General Examination
Blood pressure was measured 3 consecutive times, after participants rested for at least 5 min, by means of a standard mercury sphygmomanometer, with the participants in the sitting position, and the average value was used for the analysis. A blood sample was collected from the antecubital vein the morning after an overnight fast and analyzed for serum cholesterol, triglycerides, and fasting plasma glucose, according to previously described methods (Kubo et al., 1999). Trained nurses measured the participants’ waist circumference at the level of the umbilicus. The measurement was taken after the participants exhaled. Each participant completed a self-administered questionnaire in advance that included a medical history of diabetes, hypertension, smoking, and medication use; the questionnaire was checked by trained nurses.

The National Cholesterol Education Program (NCEP) definition of metabolic syndrome requires the presence of 3 or more of 5 components: abdominal obesity (waist circumference > 88 cm), triglycerides 150 mg/dL, decreased serum high-density lipoprotein (HDL) cholesterol (< 50 mg/dL), systolic blood pressure 130 mm Hg or diastolic blood pressure 85 mm Hg, and fasting plasma glucose 110 mg/dL (Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults, 2001). The participants receiving antihypertensive medication were counted as positive for hypertension, and those receiving antidiabetic medication or insulin therapy were counted as positive for glucose intolerance.

Statistical Analysis
Differences in mean values and proportions were evaluated by Student’s t test and Pearson’s chi-square test, respectively. We performed logistic regression analyses to determine the effect of the number of positive components of metabolic syndrome on pocket depth and clinical attachment loss, calculating the odds ratio and 95% confidence interval. The statistical analysis was performed with SPSS (version 12.0; SPSS Japan, Tokyo, Japan).

	RESULTS

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The overall mean pocket depth and clinical attachment loss values were 1.5 and 1.9, respectively (Table 1). The mean pocket depth was similar between the participants with a mean pocket depth 2.0 mm and those with a mean clinical attachment loss 3.0. The mean clinical attachment loss in participants with a mean pocket depth 2.0 mm was 2.8, and the mean clinical attachment loss in those with a mean clinical attachment loss 3.0 mm was 3.4 (Table 1). Participants with a mean pocket depth 2.0 mm had a larger waist circumference, lower HDL cholesterol, and higher fasting plasma glucose than those with a mean pocket depth < 2.0 mm (Table 1). The proportion of participants who had a history of hypertension and were taking antihypertensive medication was higher in the group with a mean pocket depth 2.0 mm (Table 1). The participants with a mean clinical attachment loss 3.0 mm were older and more likely to have a history of diabetes than those with a mean clinical attachment loss < 3.0 mm (Table 1).

	DISCUSSION

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A large waist circumference (> 88 cm), suggesting an accumulation of visceral fat, showed an independent, significant association with a greater pocket depth, but not with clinical attachment loss value. The present results agreed with those of our previous study, in which body mass index, body fat, and waist-hip ratio were used as obesity indexes (Saito et al., 2005), although the obesity index was not as closely related to periodontitis in the present study. The difference may be the result of differences in the obesity indices and cut-off points used in the two studies. In the present study, blood pressure did not have a significant relationship to periodontitis in an independent analysis. Given that many of the participants with greater pocket depth values were taking antihypertensive medication, a strong relationship between blood pressure and periodontitis would not have been expected.

In this study, the participants with low HDL cholesterol levels had a higher risk for periodontitis; of the 5 components, HDL cholesterol had the highest odds ratio for a greater pocket depth and clinical attachment loss. Several studies have reported a significant relationship between abnormal lipid metabolism and periodontitis, but the significant indices for lipid metabolism differed from study to study (Losche et al., 2000; Noack et al., 2000; Katz et al., 2002; Moeintaghavi et al., 2005). If the study populations were different, the relationship between periodontal condition and lipid metabolism would differ because of the differences in genetic background, diet, population age and sex structure, and body habitus. Also, fasting plasma glucose was significantly associated with periodontitis. The significant relationship between diabetes and periodontitis is well-known, and some studies have suggested that impaired glucose tolerance is associated with periodontal disease (Saito et al., 2004, 2006), and that periodontal treatment in diabetics has a beneficial effect on the control of blood-sugar level (Grossi et al., 1997; Stewart et al., 2001). From these studies, periodontitis would have a close relationship with abnormal lipid metabolism and impaired glucose tolerance.

In this study, female participants exhibiting several components of metabolic syndrome had higher risk for periodontal disease. Although periodontitis is a chronic inflammatory disease caused by Gram-negative anaerobic bacteria, such as Porphyromonas gingivalis and Tannerella forsythia, periodontal conditions are significantly associated with the frequency of toothbrushing, regular dental visits, and smoking and drinking habits (Sakki et al., 1995; Albandar et al., 2000; Shimazaki et al., 2005; Krustrup and Petersen, 2006). Thus, negative lifestyle habits may aggravate periodontal disease as well as health conditions such as obesity, hypertension, impaired glucose tolerance, and abnormal lipid metabolism. We propose that there is a bidirectional association between the components of metabolic syndrome and periodontal disease. However, we could not confirm a causal link between metabolic syndrome and periodontal disease, because this was a cross-sectional study; longitudinal cohort studies are required for confirmation.

Although an annual general health examination is common in Japan, a yearly dental examination is not. Without a dental check-up, many would be unaware of the presence of periodontal disease, because the subjective symptoms are weak. The results of this study suggest that people with several components of metabolic syndrome may be at higher risk for periodontal disease. We recommend that anyone exhibiting several components of metabolic syndrome receive a dental and periodontal check-up, along with a general health examination.

This study had a few limitations. Although some components of metabolic syndrome did not have a significant, independent relationship with periodontal disease, our results cannot assert an insignificant bilateral relationship between periodontal disease and these components, because the sample size was not large enough to verify the insignificance. This study showed the relationship between components of metabolic syndrome and periodontal condition only in female participants; we do not know the relationship in males. Our periodontal examination at the mesio-buccal and mid-buccal sites of each tooth in 2 quadrants may have led to bias, because we did not examine the periodontal condition at 6 sites per tooth in all of the teeth present. Further investigations are required to clarify the relationship between metabolic syndrome and periodontal disease in men, and to determine whether oral health care in individuals exhibiting metabolic syndrome has the potential to reduce the incidence of various systemic diseases.

	ACKNOWLEDGMENTS

 
We are grateful to Dr. Daisuke Ikeda and Dr. Atsusi Hideshima (Kyushu University, Fukuoka, Japan) for participating in the oral examination. This work was supported by Grants-in-Aid of Scientific Research (Nos. 15390652 and 17209066) from the Ministry of Education, Science, Sports and Culture of Japan, and by the departmental budget.

	FOOTNOTES

 
² present address, Department of Oral Health, Nagasaki University Graduate School of Biomedical Sciences;

Received May 15, 2006; Last revision October 17, 2006; Accepted November 7, 2006

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