DOI: 10.2337/diacare.29.02.06.dc05-1355 © 2006 by the American Diabetes Association
Periodontal Changes in Children and Adolescents With DiabetesA case-control study
1 School of Dental and Oral Surgery, Columbia University Medical Center, New York, New York Address correspondence and reprint requests to Evanthia Lalla, DDS, MS, Associate Professor of Dentistry, Division of Periodontics, Columbia University School of DentalOral Surgery, 630 W. 168th St., PH7E-110, New York, NY 10032. E-mail: el94{at}columbia.edu
OBJECTIVETo evaluate the level of oral disease in children and adolescents with diabetes. RESEARCH DESIGN AND METHODSDental caries and periodontal disease were clinically assessed in 182 children and adolescents (618 years of age) with diabetes and 160 nondiabetic control subjects. RESULTSThere were no differences between case and control subjects with respect to dental caries. Children with diabetes had significantly higher plaque and gingival inflammation levels compared with control subjects. The number of teeth with evidence of attachment loss (the hallmark of periodontal disease) was significantly greater in children with diabetes (5.79 ± 5.34 vs. 1.53 ± 3.05 in control subjects, unadjusted P < 0.001). When controlling for age, sex, ethnicity, gingival bleeding, and frequency of dental visits, diabetes remained a highly significant correlate of periodontitis, especially in the 12- to 18-year-old subgroup. In the case group, BMI was significantly correlated with destruction of connective tissue attachment and bone, but duration of diabetes and mean HbA1c were not. CONCLUSIONSOur findings suggest that periodontal destruction can start very early in life in diabetes and becomes more prominent as children become adolescents. Programs designed to promote periodontal disease prevention and treatment should be provided to young patients with diabetes.
Periodontal diseases are bacterial infections of the tissues surrounding and supporting the teeth. Gingivitis, an inflammation of the soft tissues only, can progress to periodontitis, where destruction of connective tissue attachment and alveolar bone can eventually lead to tooth loss. The prevalence of severe periodontitis is 1015% in most populations (1). In 1993, periodontal disease was identified as the sixth complication of diabetes (2), and in the 1997 report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus, periodontal disease was referred to as one of the pathologic conditions often found in adults with diabetes (3). The association between diabetes and periodontal diseases has been recognized in the dental literature for many decades. Indeed, multiple studies have demonstrated that the prevalence, severity, and progression of periodontal disease are significantly increased in patients with diabetes (4). Furthermore, longitudinal studies have shown that severe periodontal disease in diabetic patients at baseline is associated with poor metabolic control and other diabetes complications at follow-up (5,6). A number of reports on the relationship between diabetes and periodontal disease have included children and adolescents; however, these studies are limited with respect to the depth of data collected and analyses presented. Manouchehr-Pour and Bissada (7) reviewed periodontal conditions in individuals with diabetes and reported that in patients with childhood-onset diabetes, periodontitis seems to ensue around puberty and to progress with age. The goal of the present study was to define the oral disease burden in young children and adolescents with diabetes.
The study protocol was approved by the Columbia University Medical Center Institutional Review Board. Parents/legal guardians of participants signed a consent form. One hundred eighty-two patients with diabetes, 618 years of age, were recruited from among the patients followed at the Naomi Berrie Diabetes Center at the Columbia University Medical Center. One hundred and sixty 618 year old subjects seen at the pediatric dental clinic at the Columbia University School of Dental and Oral Surgery who denied history of diabetes served as control subjects. Children in both groups were excluded if they were undergoing active orthodontic therapy.
Oral examination protocol
Diabetes-related variables
Data and statistical analysis We did not include plaque index as one of the adjusting variables, as it is highly correlated with the proportion of sites with bleeding. To avoid multicollinearity, of the two we chose the latter because it is not only a measure of gingival inflammation and a precursor of periodontal destruction but also an index of oral hygiene (affected by the level of plaque control over a longer period of time rather than just the examination day). The case-only analysis investigated the association between periodontitis and certain diabetes-related variables, using an adjusted linear regression model. The dependent variable was number of affected teeth (those having at least one site with >2 mm of attachment loss). Independent variables included: A1C (mean value of all tests performed in the 2 years before the dental examination, excluding any tests that were within 3 months of diagnosis of diabetes), BMI, duration of diabetes, age-subgroup, proportion of sites with gingival bleeding, and adjusting variables: sex, ethnicity, frequency of dental visits, and dental examiner. P < 0.05 (two sided) was considered statistically significant for all analyses.
Case-control analysis Demographic, dental, and periodontal characteristics of the study population are presented in Table 1.
For each subject, we computed the number of carious (decayed) and restored (treated for decay) surfaces and teeth based on the full mouth examination. There were no significant differences between case and control subjects in regard to caries experience.
Children with diabetes had significantly more dental plaque than nondiabetic control children (plaque index 1.2 vs. 1.1, respectively; unadjusted P < 0.001). Similarly, when we calculated the percentage of sites that had visible plaque (plaque index Attachment loss, the hallmark of periodontitis, calculated as either a subject-based mean or as the number of affected teeth (having at least one site with >2 mm of attachment loss) was also significantly higher in diabetic children compared with nondiabetic control subjects (1.8 vs. 0.8 and 5.8 vs. 1.5, respectively).
As shown in Fig. 1, the number of affected teeth was significantly higher in diabetic children versus control children in both age-subgroups, <12 years of age or
Examination of the distribution of subjects with attachment loss in our study population revealed differences depending on the age-subgroup. This was supported by the logistic regression analysis (with presence of periodontitis as the dependent variable) adjusting for several relevant variables, which revealed diabetes and age as the two statistically significant correlates of periodontitis. Results for the whole population and by age-subgroup are summarized in Table 2. When we used different definitions of periodontal disease to allow for even more extensive periodontal destruction, the effect of diabetes remained significant for the older but not for the younger group of patients (data not shown).
Case-only analysis Diabetes-related variables in our cases (for all subjects and by age-subgroup) are presented in Table 3. Ninety-four percent of all children had type 1 diabetes; 11% in the older subgroup had type 2 diabetes. Mean A1C over the 2 years before the examination was 8.4 ± 1.7% and similar in the two subgroups (P = 0.09). However, the percentage of children with poor metabolic control was significantly higher in the older group (P = 0.01). BMI-for-age percentiles were similar in the two groups, but actual BMI was significantly higher in the older group (25.0 ± 7.5 kg/m2) compared with 19.2 ± 4.4 kg/m2 in the younger group (P < 0.001). Further, a higher percentage of the older children had a poor nutritional status indicator, based on their BMI for age (P = 0.04).
Table 4 summarizes results from the linear regression analysis. The focus here was to investigate the relationship between periodontal destruction and diabetes-related variables. The association between number of affected teeth and mean A1C or duration of diabetes was not statistically significant. However, there was a positive and statistically significant association between the number of affected teeth and BMI (regression coefficient 0.12, P = 0.03). One of the adjusting variables, frequency of dental visits, also reached significance in this model (regression coefficient 1.01, P = 0.046).
Previous studies in children with diabetes have indicated that gingival inflammation is significantly increased compared with nondiabetic control subjects, even after adjusting for oral hygiene levels (1315). Findings from the present study indicate that periodontal destruction is increased in children and adolescents with diabetes and, importantly, that this starts earlier in life than formerly recognized (7). Our nondiabetic control subjects represent an underserved, mostly Hispanic population, and recent studies in this population have reported that the oral disease burden is high compared with national standards (16,17). In this study, evidence of periodontal destruction was indeed present in the control group. However, presence of diabetes clearly conferred a significant risk. Regression analysis revealed that diabetes was a statistically significant correlate of periodontitis, even in the 6- to 11-year-old group. This relationship became more pronounced after the age of 12. The etiopathogenesis of both diabetes and periodontitis is complex, and identifying the mechanisms underlying this association was beyond the scope of this study. However, evidence suggests that mechanisms that account for the development of other diabetes complications might be operating in the pathogenesis of accelerated periodontitis in diabetes as well (18). Our finding in this study, that duration of diabetes, and especially mean A1C, were not significantly correlated with the number of affected teeth was intriguing. It appears to be in contrast to previous evidence suggesting that individuals with diabetes and poor metabolic control are at a higher risk for suffering from more severe periodontitis (4). However, not all studies have reported such an association, and there are conflicting data between prospective follow-up studies that have in their majority suggested the former and many cross-sectional studies like ours that have shown no correlation. Interestingly, in the case group, BMI displayed a modest but statistically significant correlation with the number of affected teeth. This finding, although preliminary, is consistent with the current understanding that obesity is associated with the development of a systemic inflammatory state and the recent reports on a significant correlation between periodontitis and BMI in adults (19,20). Further studies including larger numbers of children and adolescents are under way; these will shed more light into these associations, other factors involved, as well as the natural history of the development of periodontal changes in diabetes. Dental caries, xerostomia, and mucosal lesions have been reported in patients with diabetes, but the data are conflicting (21,22). Most recent studies suggest that young people with diabetes exhibit similar levels of caries to systemically healthy individuals (23,24). In this study we found no differences in clinical caries experience between children with diabetes and nondiabetic control children, and the presence of other mucosal lesions was very rare in both groups. It has been reported that patients with diabetes are significantly less likely than those without diabetes to have seen a dentist within the past year, even after adjusting for age, race/ethnicity, education, income, and dental insurance coverage (25). Interestingly, the primary reason for not seeing a dentist given in that study was lack of a perceived need. As periodontal diseases are largely preventable and progression of destruction can be best arrested when identified in early stages, screening for periodontal changes and implementing prevention and treatment programs should be considered as a standard of care for young patients with diabetes. This becomes even more important in the light of the emerging view that control of periodontal infections in adults with diabetes can further have a positive effect on the level of metabolic control in these individuals (26,27).
This study was supported by National Institutes of Health Grant DE14898. We thank Richard Buchsbaum, Johanne Reynoso, and Drs. Melissa Begg and Barney Softness for their valuable assistance.
A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances. Received for publication July 21, 2005. Accepted for publication November 4, 2005.
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