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Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2007-2522
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The Journal of Clinical Endocrinology & Metabolism Vol. 93, No. 10 3989-3994
Copyright © 2008 by The Endocrine Society

BRIEF REPORT

Association of the Metabolic Syndrome with Severe Periodontitis in a Large U.S. Population-Based Survey

Francesco D'Aiuto, Wael Sabbah, Gopalakrishnan Netuveli, Nikos Donos, Aroon D. Hingorani, John Deanfield and Georgios Tsakos

Periodontology Unit, UCL Eastman Dental Institute (F.D., N.D.), London WC1X 8LD, United Kingdom; Center for Clinical Pharmacology (A.D.H.), University College London, London WC1E 6JF, United Kingdom; Department of Epidemiology and Public Health (W.S., G.T.), University College London, London WC1E 6BT, United Kingdom; Department of Primary Care and Social Medicine (G.N.), Imperial College London, London SW7 2AZ, United Kingdom; and Vascular Physiology Unit (J.D.), Institute of Child Health and Great Ormond Street Hospital for Sick Children, London WC1N 1LE, United Kingdom

Address all correspondence and requests for reprints to: Dr. Francesco D'Aiuto, Periodontology Unit, UCL Eastman Dental Institute and Hospital, 256 Gray’s Inn Road, London WC1X 8LD, United Kingdom. E-mail: f.daiuto{at}eastman.ucl.ac.uk.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: Metabolic syndrome and periodontitis both have an increasing prevalence worldwide; however, limited information is available on their association.

Objective: The objective of the study was to assess the association between periodontitis and the metabolic syndrome in a cross-sectional survey of a nationally representative sample of the noninstitutionalized civilians in the United States.

Design, Setting, and Participants: Data analysis from the Third National Health and Nutrition Examination Survey on 13,994 men and women aged 17 yr or older who received periodontal examination were studied.

Main Outcome Measures: Association of diagnosis and extent of periodontitis (gingival bleeding, probing pocket depths) with the metabolic syndrome and its individual component conditions (central obesity, hypertriglyceridemia, low high-density lipoprotein-cholesterol, hypertension, and insulin resistance) were measured. Adjustment for age, sex, years of education, poverty to income ratio, ethnicity, general conditions, and smoking were considered.

Results: The prevalence of the metabolic syndrome was 18% [95% confidence interval (CI) 16–19], 34% (95% CI 29–38), and 37% (95% CI 28–48) among individuals with no-mild, moderate, and severe periodontitis, respectively. After adjusting for confounders, participants aged older than 45 yr suffering from severe periodontitis were 2.31 times (95% CI 1.13–4.73) more likely to have the metabolic syndrome than unaffected individuals. Diagnosis of metabolic syndrome increased by 1.12 times (95% CI 1.07–1.18) per 10% increase in gingival bleeding and 1.13 times (95% CI 1.03–1.24) per 10% increase in the proportion of periodontal pockets.

Conclusions: Severe periodontitis is associated with metabolic syndrome in middle-aged individuals. Further studies are required to test whether improvements in oral health lead to reductions in cardiometabolic traits and the risk of metabolic syndrome or vice versa.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
The metabolic syndrome, a clustering within individuals of several cardiovascular risk factors, is becoming a common disorder among U.S. citizens and worldwide (1, 2, 3). A diagnosis of metabolic syndrome is associated with doubling in risk for future cardiovascular diseases and type 2 diabetes mellitus (4, 5). According to Adult Treatment Panel III and recent consensus workshops, the metabolic syndrome is defined as the concurrence of hypertension and atherogenic lipid profiles [hypertriglyceridemia and low high-density lipoprotein (HDL)-cholesterol] but also obesity and insulin resistance (6, 7). A proinflammatory and procoagulant state may also coexist in this syndrome, with elevation of C-reactive protein and fibrinogen (8, 9). The exact mechanisms behind this systemic response remain uncertain. There is evidence to also suggest that this chronic inflammatory state is associated with endothelial dysfunction, which might contribute to the increased cardiovascular risk of people affected by this disorder and with the increased risk of type 2 diabetes (10, 11, 12, 13).

Periodontitis is a common chronic infection of the adult population characterized by an exaggerated gingival inflammatory response against a pathogenic bacterial microflora, resulting in alveolar bone and eventually tooth loss (14). Periodontitis has also been associated with systemic alterations such as low-grade inflammation (15, 16), dyslipidemia (17), glucose intolerance (18, 19), a procoagulant state (20), and endothelial dysfunction (21). A growing body of evidence also indicates that periodontitis is associated with measures of body weight in youth (22) as well as insulin resistance (23). Because both periodontitis and the metabolic syndrome are associated with systemic inflammation and insulin resistance, these two diseases may be linked through a common pathophysiological pathway. This could explain the almost 20% increased risk of cardiovascular diseases reported in patients with periodontitis (24). Little information, however, is available on the possible association between periodontitis and the metabolic syndrome as sole clinical entity (25). Our aim was therefore to ascertain the association between the metabolic syndrome and periodontal diseases in a cross-sectional survey of a nationally representative sample of the noninstitutionalized civilians in the United States.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Data were derived from the third National Health and Nutrition Examination Survey (NHANES III) conducted in 1988–1994 on a national probability sample of noninstitutionalized, nonmilitary American population (26). We used data pertaining to the population aged 17 yr and older, excluding pregnant women and those individuals reporting cardiac condition or any medical condition requiring antibiotic coverage before the dental examination. From a total of 13,994 subjects who had periodontal assessment, our final study sample was of 13,677 individuals.

Assessment of metabolic syndrome was based on the following five components: central obesity (waist circumference >102 cm for males and >88 cm for females); hypertriglyceridemia (triglycerides >150 mg/dl); low HDL-cholesterol (<40 mg/dl for men and <50 for women); high blood pressure (systolic: >130 mm Hg or diastolic: >85 mm Hg or on blood pressure medication); and high plasma glucose (>110 g/dl) (7). Metabolic syndrome was considered present in participants exceeding the threshold limits for at least three of these components (7).

Reproducible periodontal measures were done on dentate participants on randomly assigned half-mouths by calibrated examiners as previously described in the NHANES procedures manuals (26). Among a plethora of case definitions of periodontitis (27, 28), we used a recently reported definition of periodontitis suited for epidemiologic surveys (28) as follows: moderate periodontitis = two sites not on the same tooth with loss of periodontal attachment 4 mm or greater or one site with gingival probing depth 4 mm or greater and severe periodontitis = two sites not on the same tooth with loss of periodontal attachment 6 mm or greater and at least one site with gingival probing depth 4 mm or greater (28). We also used continuous measures of periodontal health/disease as proxy for systemic exposure of periodontitis (29). Proportion of periodontal sites with periodontal pockets 4 mm or greater per number of examined sites and proportion of gingival bleeding sites per number of examined sites were included in the analyses.

The STATA 8.0 (StataCorp, College Station, TX) statistical program was used for all analyses (estimated prevalence, logistic regression), taking into account population weights and adjustment for the complex sampling design. Logistic regression analyses were used to assess the associations between the presence of metabolic syndrome and its components (dependent variables) with the different measures of periodontal disease adjusted for the effect of other variables (age, sex, years of education, poverty to income ratio, ethnicity, general conditions, and smoking) were used as covariates in all multivariate models. General conditions were assessed by aggregate binary variables to note the presence of chronic heart diseases, cancer, diabetes, stroke, emphysema, asthma, arthritis, lupus, thyroid disease, and goiter (30). Participants were grouped into three groups according to cigarette smoking: current smokers, nonsmokers, and no respondents. Analyses were performed in the all study sample and the subgroup of middle-aged individuals (presenting with the highest prevalence of periodontitis and the metabolic syndrome; see Table 1Go) and never-smokers (defined as persons who reported having smoked <100 cigarettes during their lifetime). For each outcome variable (metabolic syndrome and each of the individual components), analyses were conducted for the whole available sample, and the different regression models were based on the same number of subjects to ensure comparability.


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  		TABLE 1. Frequency distribution of periodontitis (no-mild, moderate, and severe) and the metabolic syndrome in different age groups

 

   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Baseline characteristics of subjects among subgroups of periodontitis are reported in Table 2Go. Substantial differences in most the variables examined were observed, and therefore, only adjusted multivariate estimates are reported. Diagnosis of no-mild, moderate, or severe periodontitis was associated with a linear increase in the prevalence of the metabolic syndrome; 18% [95% confidence interval (CI) 16–19] among participants with no or mild periodontitis, 34% (95% CI 29–38) and 37% (95% CI 28–48) among those with moderate and severe periodontitis had metabolic syndrome, respectively (P < 0.01 for linear trend). Similarly, among individuals with moderate and severe periodontitis, there was a higher prevalence of obesity (48–54%, 95% CI 44–63 vs. 31%, 95% CI 30–33), hypertension (51–56%, 95% CI 47–64 vs. 27%, 95% CI 25–29), and high glucose levels (18–24%, 95% CI 15–30 vs. 8%, 95% CI 8–9) (all P < 0.001), compared with those with no or mild periodontitis.


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  		TABLE 2. Baseline characteristics of subjects by diagnosis of periodontitis (n = 13,677) (pregnant women are excluded from all analyses

 
After adjusting for the effect of age, sex, years of education, poverty to income ratio, ethnicity, general conditions, and smoking in multiple logistic regression, among participants with severe periodontitis, the odds for the metabolic syndrome was 1.45 (95% CI 0.91–2.33), compared with those with no or mild periodontitis (Table 3Go). In the middle aged group (45 yr or older), severe periodontitis was mildly associated with the metabolic syndrome [odds ratio (OR) 1.74, 95% CI 1.10–2.76, P < 0.05, n = 263], and the magnitude of this association increased in the subgroup of never-smokers (OR 2.31, 95% CI 1.13–4.73, P < 0.05, n = 61). A consistent positive association between severe periodontitis diagnosis and insulin resistance was observed. Indeed adjusted ORs of 1.71 (95% CI 1.16–2.54, P < 0.01, n = 337), 1.74 (95% CI 1.10–2.78, P < 0.05, n = 263), and 4.74 (95% CI 2.05–10.97, P < 0.01, n = 61) for hyperglycemia were found in all the sample, the middle-aged group, and the subgroup of nonsmokers with severe periodontitis respectively.


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  		TABLE 3. Adjusted associations between diagnosis of periodontitis (no-mild, moderate, and severe) and the metabolic syndrome and its individual components

 
Both continuous measures of periodontal disease examined (bleeding and pocket scores) were associated with higher odds of components of the metabolic syndrome (Fig. 1Go). A 10% increase in gingival bleeding extent was associated with an OR for metabolic syndrome of 1.12 (95% CI 1.07–1.18, P < 0.001) and a 10% increase in the periodontal pocket extent with and OR of 1.13 (95% CI 1.03–1.24, P < 0.05). Moreover, there was evidence to suggest a positive association of each periodontal marker with each individual component of the metabolic syndrome, with all associations with the exception of hypertriglyceridemia remaining significant, even after adjusting for confounders (Fig. 1Go).


Figure 1
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  		FIG. 1. Odds ratios (95% CIs) of metabolic syndrome and individual components calculated for clinical measures of periodontal disease (A and B). For gingival bleeding and pocket depth scores, OR is for 10% increase. ORs are presented as adjusted values ({square}) for age, sex, years of education, poverty ratio, ethnicity, general conditions, and smoking.

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
This analysis provides evidence of a positive association between continuous measures of gingival health and the metabolic syndrome and its components in all age groups of this study sample. We also confirmed an association between diagnosis of severe periodontitis with the metabolic syndrome and in particular with the insulin resistance component in middle-aged never-smoker individuals.

Over the past decade, accumulating evidence suggests that periodontitis may be associated with an increased risk of future cardiovascular events and type 2 diabetes in otherwise healthy individuals (24, 31). The magnitude of this association, however, seems to be strongly affected by the inadequacy of current definitions of periodontitis and the use of multiple clinical criteria to ascertain its grade of severity. The strength of our findings lies in having found an association between periodontitis and the metabolic syndrome and its components using both a very conservative case definition of periodontitis and continuous measures of gingival health. However, these data raise the hypothesis of a possible nonlinear relationship between different measures of gingival health and components of the metabolic syndrome. Indeed, a linear association between gingival bleeding/pockets and most metabolic factors in particular obesity was observed at all age groups, whereas when a case definition of periodontitis was used, only measures of insulin resistance were associated with severe periodontitis in middle-aged individuals. Nevertheless, these finding are not surprising because of the bulk of experimental and clinical evidence in support of an association between periodontitis and most of the individual components of the metabolic syndrome. A recent analysis of the same data set both in young individuals and all of the population showed that periodontitis and measures of adiposity are closely linked (22, 32). Furthermore, data from experimental models suggests that adiposity could influence the host response to periodontal bacteria, and it has been proposed as a potential mechanisms explaining this association (33).

Clinical evidence has been produced on the association between periodontitis and measures of insulin resistance (18), lipid alterations (17), and vascular dysfunction (21). Few studies have also reported on a possible positive association between periodontitis, arterial blood pressure, endothelial dysfunction (34, 35), and a dyslipidemic state (36). A bulk of experimental data derived from animal models and epidemiological and intervention trials support the hypothesis that periodontitis triggers a state of low-grade systemic inflammation (37). A complex interplay of the host inflammatory response to periodontal infections, adiposity, and alterations of lipid levels might be responsible for the state of insulin resistance reported in individuals with periodontitis (23) as we also observed in this analysis. We hypothesize that this finding could also explain the reported association among periodontal diseases, the metabolic syndrome, and future increased risk of vascular diseases (38) and diabetes (31). Our group recently showed that 6 months after treatment of severe forms of periodontitis, a substantial improvement in measures of endothelial function was observed (21). Limited and inconclusive evidence, however, has been reported on the potential impact of treatment of periodontitis on other components of the metabolic syndrome in particular blood pressure (39).

Our analysis, however, has several limitations. The cross-sectional nature of the NHANES study does not allow for causal interpretations because the data indicate a strong association without inferring any information as to the direction of a potential causal pathway. It should also be noted that the diagnostic criteria used to define periodontitis as well as definitions of each component of the metabolic syndrome including use of different medications are intentionally conservative. Periodontitis prevalence, therefore, may have been underestimated. The partial (half mouth) recordings available in this data set might also play a role in this. In addition, many other factors (e.g. genetics, oral health behavior) that could be associated with both conditions have not been assessed. We cannot therefore exclude the possibility of a spurious association between periodontitis and metabolic syndrome due to other unmeasured confounding factors (residual confounding). A word of caution in interpreting our results is due in particular with regard to the role of cigarette smoking as a major confounder of this association and due to the limited number of individuals included in the analysis. Nonetheless, it should be noted that despite its limitations, this report emphasizes the possible impact that poor oral health might have on systemic parameters, and this might have important implications for the health of the public. Further intervention studies aimed at controlling periodontal infections are required to test whether improvements in oral health lead to reductions in cardiometabolic traits and the risk of metabolic syndrome.


   Acknowledgments
 
We acknowledge Professor Aubrey Sheiham and Professor Maurizio Tonetti for their help.


   Footnotes
 
Disclosure Statement: The authors have nothing to disclose.

First Published Online August 5, 2008

Abbreviations: CI, Confidence interval; HDL, high-density lipoprotein; NHANES III, third National Health and Nutrition Examination Survey; OR, odds ratio.

Received November 13, 2007.

Accepted July 24, 2008.


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 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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