Periodontal disease and type I diabetes mellitus: Associations with glycemic control and complications.

OBJECTIVE: The aim of the study was to evaluate periodontal health status in patients diagnosed with type 1 diabetes mellitus (DM1) and to establish a correlation between metabolic control and periodontal health status.
MATERIALS AND METHODS: Periodontal health parameters namely plaque index (PI), gingival index (GI), probing pocket depth (PPD) and clinical attachment loss (CAL) were recorded in 28 patients diagnosed with type 1 diabetes mellitus (DM1) and 20 healthy controls. Diabetes history was recorded based on the information provided by the physician and it included date of diagnosis, duration, age of diagnosis, latest values of glycosylated haemoglobin and existing diabetic complications. Statistical analysis was performed to evaluate the relationship between periodontal parameters and degree of metabolic control, the duration of the disease and the appearance of complications.
RESULTS: The periodontal health in the diabetic group was compromised and they had greater bleeding index (P < 0.001), probing pocket depth (P < 0.001) and clinical attachment level (P = 0.001). Patients diagnosed for diabetes for shorter duration of time (4-7 years) showed bleeding index-disease severity correlation to be 1.760 ± 0.434.
CONCLUSION: Periodontal disease was more evident in type 1 diabetes mellitus patients and periodontal inflammation is greatly increased in subjects with longer disease course, poor metabolic control and diabetic complications.

INTRODUCTION

Diabetes mellitus is a disease of metabolic dysregulation, primarily of carbohydrate metabolism, characterized by hyperglycemia that results from a defect in insulin secretion, impaired insulin action or both. The chronic hyperglycemia of diabetes is associated with long-term damage, dysfunction, and failure of different organs, especially eyes, kidneys, nerves, heart, and blood vessels. Type I diabetes mellitus, which accounts for 5-10% of those with diabetes, is caused by cell-mediated autoimmune destruction of the insulin-producing β cells in the pancreas. The rate of β-cell destruction is variable. Little or no insulin secretion is manifested by low or undetectable levels of plasma C-peptide. Long-term complications of diabetes include retinopathy and nephropathy, with risk of foot ulcers, amputations, and Charcot's joints. Treatment of this disease is based on subcutaneous administration of insulin, regular exercise, diet, and weight control.[1]

A link between diabetes and periodontitis in adults has been confirmed.[2] In fact periodontitis has been considered as the sixth complication of diabetes.[3] It is well-established that diabetes increases the prevalence, severity, and progression of periodontal disease,[456] although, vice versa, the fact that periodontal disease may complicate the severity of diabetes by worsening the degree of glycemic control has also been proven.[78]

Periodontitis is a chronic low-grade infection induced by multiple pathogens and can result in alteration of insulin action.[9] Chronic gram-negative periodontal infection is currently thought to increase insulin resistance, contributing to the development of metabolic imbalance.[10] Also, the interaction of periodontal bacterial by-products with mononuclear phagocytic cells and fibroblasts is known to induce the chronic release of cytokines (IL-1β, IL-6, TNF-α), PGE2, and CRP.[11]

Several recent studies have suggested that periodontal disease is a crucial aggravating factor in the health of patients with diabetes, mainly because it maintains a chronic systemic inflammatory process, thereby, contributing to diabetic complications.[12] Thus, it has been suggested that adequate periodontal treatment in diabetic patients may be beneficial in reducing diabetic complications.[13]

The present study aims at assessing the prevalence of periodontal disease in type 1 diabetes mellitus patients and its association with glycemic control and diabetic complications.

MATERIALS AND METHODS

A case-controlled clinical study was performed to assess the periodontal health status of type 1 diabetes mellitus (DM 1) patients. Twenty-eight patients diagnosed with DM1 visiting the Outpatient Department of the Satyam Hospital and Research Center for their treatment, were recruited in the study. The patients were diagnosed according to the criteria published by the American Diabetes Association 2011,[14] and they were treated with insulin, antidiabetic drugs, diet, and physical exercise recommendation, under the physician's supervision.

Inclusion criteria

The subjects were aged between 18 and 50 years

Patients with type I diabetes mellitus

Diabetes for more than three years

Patients who did not have any active infection

Patients with >14 natural teeth present and at least five teeth with a probing pocket depth (PPD) of >5 mm and a clinical attachment level (CAL) of >3 mm2

Patients who had not had any periodontal treatment in the last six months.

Exclusion criteria

Patients were excluded if they had non type I diabetes

Pregnancy and lactation

Any inflammatory disease, chronic liver disease or patients receiving any treatment that could modify the study parameters, such as, antibiotics, immunosuppressants, antiepileptics, and so on.

As the control group, 20 healthy individuals, who had come for a routine dental check-up were included. Both the groups were age- and gender-matched.

Diabetes-related parameters

A detailed medical history was provided by the consulting physician and information like date of diagnosis, age at diagnosis, latest reading for HbA1c, and existing diabetic complications were recorded. The diagnosis of type I diabetes was assessed by the C-peptide concentration, and metabolic control was determined on the basis of the glycosylated hemoglobin value (HbA1c), determined by using the Micromat II HbA1c assay (Biorad®), by the affinity chromatography method. Good metabolic control was assumed to be represented by HbA1c <7%, while poor control was defined as HbA1c >7%. Normality for controls was assumed to be <5.5%.[1415]

Diabetic complications such as retinopathy, neuropathy, and nephropathy were examined.

Oral examination

Periodontal examination was performed using the UNC-15 (University of North Carolina) probe (HuFriedy®), calibrated at every millimeter, to determine the parameters. The plaque index[16] was recorded and given a score from 0 to 3. The probing pocket depth was defined as the distance between the gingival margin and the bottom of the probeable pocket to the nearest whole millimeter. The gingival bleeding index[17] was recorded and given a score from 0 to 3. The CAL was computed by subtracting the distance from the visible cemento-enamel junction to the gingival margin from the whole probing depth. The measurements were performed on four surfaces of each tooth (mesiobuccal, midbuccal, distobuccal, and midpalatal/lingual) and the extent of periodontal disease was expressed as a mean of the affected sites out of the total number of sites measured. The total number of teeth were also noted.

At the end of the clinical examination each patient was informed of the clinical findings, given oral hygiene instructions, and advised periodontal treatment, as needed.

Statistical analysis

The data was analysed using the Statistical Package for Social Science (SPSS Chicago USA) version 18. Descriptive statistics were generated for all the study variables. The qualitative variables were described as frequencies and proportions, and the quantitative variables as the mean and standard deviation (SD). The Student t-test was used in the bivariate analysis to compare the means. A P < 0.05 was considered statistically significant. A statistical analysis of the clinical findings was performed to detect the differences between diabetic subjects and controls, to detect the differences between diabetic subjects with different diabetes durations, and the HbA1c%. Logistic regression analysis was done using the forward stepwise method for selecting variables according to the statistic likelihood ratio, in order to assess the association of the independent variables with the probability of being a diabetic patient.

RESULTS

The study consisted of 28 (17 male and 11 female) patients diagnosed with type I diabetes mellitus. The mean age was 32.9 ± 10.71 years, with a range of 18-50 years. On grouping the patients by decades of age, most belonged to the 21-30 and 31-40 year intervals (45 and 30% of the total, respectively). The time elapsed from the diagnosis was 4 - 15 years and they were diagnosed around the mean age of 11 years [Table 1].

Table 1

Variables associated with the two study groups

The control group represented the mean age of 31 ± 7.4 years with an age range of 18-50 years. Most subjects belonged to the 21-30 and 31-40 age group (55 and 35%, respectively). The two groups were matched for age, physical build, and oral hygiene.

There was no significant difference in the plaque index, as the oral hygiene was similar in the two groups.

Significant differences were recorded in the bleeding index, pocket depth, and attachment loss [Table 2]. The diabetic group presented with a mean pocket depth of 6.337 ± 0.650, whereas, it was 5.181 ± 0.705 for the non-diabetics. The gingival bleeding index was 2.708 ± 0.390 and 1.760 ± 0.434 in the study and control group, respectively. The CAL was greater in the diabetics 4.337 ± 0.648, as compared to 2.300 ± 0.557 in the non-diabetics.

Table 2

Comparison of mean values of the periodontal parameters

The mean glycosylated hemoglobin (HbA1c) value among the diabetic patients was 8.84 + 1.34 Table 1. Four patients presented HbA1c values <7%, while the remaining had values >7%. On comparing the diabetics with poor metabolic control of the disease versus those with moderate or good control, significant differences were recorded in the probing pocket depth (P < 0.001), bleeding index (P < 0.001), and clinical attachment level (P = 0.001).

Patients diagnosed with diabetes for shorter duration of time (4 - 7 years) showed the bleeding index–disease severity correlation to be 1.760 ± 0.434 as compared to those diagnosed for a greater period of time 2.728 ± 0.384 [Table 3].

Table 3

Relationship between the periodontal parameters and different aspects of diabetes

Eleven (55%) patients suffered from one or more chronic complications of the disease, while nine (45%) experienced no complications. The severity, duration, and complications significantly affected the periodontal health status [Table 3].

DISCUSSION

In recent decades, many studies have reported that the presence of diabetes mellitus (DM) increases the prevalence, severity, and progression of periodontal disease. There is a bidirectional relationship between the two processes, where diabetes serves as a modifier of the expression of periodontal disease.[18] Most of these studies have emphasized on type 2 diabetes mellitus, with very few studies on the correlation and clinical features of type 1 diabetes mellitus.

Thus, the present study has emphasized on the prevalence of periodontitis in type 1 diabetes mellitus (DM1) and a possible association between glycemic control and the complications. There were 28 DM1-diagnosed patients in the study and 20 healthy controls, who were demographically matched. Individuals younger than 18 years were excluded, to avoid uncertainty in the periodontal status, which could be influenced due to puberty. The patients over 50 years were excluded to avoid the appearance of other systemic complications.

No difference was found in the two groups regarding the plaque index as they had a similar level of oral hygiene. However, it has been shown that diabetic patients harbor more gram negative bacteria and thereby have higher plaque levels. However, bleeding index showed significantly higher values, suggesting greater susceptibility for periodontal disease. These observations were in concordance with most of the studies on diabetes showing that diabetics show greater periodontal inflammation in response to irritation caused by plaque bacteria.[1]

Deeper pathological pockets were observed in the diabetics. This was consensus with the observations by Oliver et al. 1993[19] poorer controlled diabetics showed deeper pockets, as seen by other authors.[1]

Glycosylated hemoglobin (HbA1c) was considered the indicator of metabolic control. Mean HbA1c was 8.84%. We also assessed the levels of C-peptide which ranged from 0.39-1.2 for the severity of type I diabetes and fasting blood glucose for the diabetic status. In the study DM1 patients with better glycemic control (HbA1c < 7.5%) showed significantly lower mean GI and PI and less CAL compared to diabetics with poor glycemic control (HbA1c > 8). However, the regression analysis could not confirm a very strong correlation between metabolic control and periodontitis. The probable reason could be that fact that only HbA1c was alone used for the purpose. It may be possible that poor glycemic control over the last 3 months was more closely correlated with gingival inflammation than connective tissue attachment loss. Measurement of glycemic control and periodontal disease represent different time frames in the patient's life; HbA1c represents glycemic status over 3 months while periodontal parameters represent the cumulative impact of periodontal destruction over an individual's lifetime. Therefore, HbA1c measurement over 24-36 months and then correlation with periodontal health will give better assessment.[20]

The duration of diabetes ranged from 4-15 years. A correlation between the duration of diabetes and the severity of periodontal disease has been reported.[21] A similar correlation was also observed in our study, where longer duration of the disease affected the probing pocket depth, bleeding on probing and clinical attachment level.

In the present study we observed a positive relationship between the bleeding index and the presence of periodontal pockets with complications of diabetes, as related by other authors.[6] The immune alterations in these patients, with subsequent increase in immune inflammatory mediator production, could be responsible for the damage observed in the periodontium, as also systemically.

The pathogenic mechanisms in type I and type II diabetes are quite different, which may have an effect on the risk of periodontal disease as well as on other comorbidities in the two groups of patients. Persistent hyperglycemia over many years, with inherent derangement in the immune mechanism, is the inherent feature of type 1 diabetes mellitus.

CONCLUSION

Periodontal disease is more prevalent and severe in type 1 diabetes mellitus patients. A greater periodontal inflammatory tendency corresponded to those individuals with poorer metabolic control, with or without complications, while longer durations of DM were associated with greater periodontal attachment loss. In the presence of similar plaque scores, type I diabetics are more vulnerable to periodontal disease.