Abstract
Background:
The World Health Organization (WHO) has recommended the age group of 35–44 years for surveillance of oral health conditions in adults. There is a growing incidence of early onset of Type 2 diabetes mellitus (T2DM) worldwide.
Objective:
This study was conducted to find the strength of association between dental caries and periodontitis in patients with T2DM.
Materials and Methods:
This was a case–control study conducted among 35–44-year-old patients with T2DM (n = 185) reporting to various hospitals of Belagavi city and controls (n = 185), who met the inclusion criteria. Group matching was done for age and gender. The study participants were interviewed for their sociodemographic details, relevant medical history, oral health behaviors, and dietary behaviors using a self-designed questionnaire. Dental caries and periodontal status were recorded using the WHO criteria, 2013.
Results:
The mean decayed missing filled teeth was significantly higher among controls than cases (P = 0.006). A significantly higher number of cases had periodontal pockets (crude odds ratio: 6.6) as compared to controls. Regression analysis showed that loss of attachment was significantly associated with T2DM (adjusted odds ratio: 5.9, 95% confidence interval: 2.81–6.89).
Conclusion:
Periodontitis was found to be associated with T2DM. However, no such association was found between dental caries and T2DM.
Keywords: Diabetes mellitus, early onset, oral health, periodontal disease
INTRODUCTION
The worldwide prevalence of diabetes is increasing by the day. The current estimate of diabetes in India is 77 million and is expected to rise up to 134 million by 2045. The Indian state of Karnataka is eighth in line to report maximum diabetes cases.[1] As projected by recent statistics, the prevalence of diabetes in rural and urban parts of India is 15% and 19%, respectively.[2] Most of these cases are of type 2 diabetes mellitus (T2DM).[1] A study conducted in Asian population reported an increase in early onset of T2DM in younger adults. About 25% of the individuals were <49 years of age.[3] Various familial and lifestyle factors are attributed to this. The bidirectional relation between periodontitis and T2DM is well documented in the literature.[4] Diabetic individuals are also known to have more carious lesions due to reduced salivary flow rate.[5] The World Health Organization (WHO) has recommended the age group of 35–44 years for surveillance of oral health conditions in adults.[6] However, the risk of periodontal disease and dental caries remains unknown for individuals in this age range.
Hence, the present study was planned to find an association of dental caries and periodontal disease with T2DM among 35–44-year-old patients in Belagavi city.
MATERIALS AND METHODS
The present study was a hospital-based, matched case–control study conducted from December 2016 to February 2017. The study population comprised 185 patients with T2DM who reported to various hospitals of Belagavi city and 185 controls. Ethical approval was obtained from the ethics committee of the institute before start of the study. Permissions were taken from the respective hospitals, and written informed consent was obtained from the participants of the study.
Inclusion criteria for cases:
Known cases of T2DM in the age range of 35–44 years, who had diabetes since at least 2 years according to their past medical records were considered. As known cases of T2DM were considered, HbA1c was not assessed. Glycemic control was checked using random blood sugar (RBS) exam
Individuals who had any other systemic diseases other than diabetes and who were bed ridden or mentally disoriented were not included
Individuals who had undergone oral prophylaxis in the past 1 year and who gave a history of antibiotic use for more than a week in last 3 months were excluded
Individuals with adverse habits such as alcohol consumption, tobacco smoking, and/or chewing were excluded.
Selection of controls:
Controls were friends and relatives of the patients
They were similar to cases in all aspects expect for presence of diabetes
They were confirmed to be free from diabetes by RBS examination (RBS <140 mg/dl).
Group matching for age and gender was done for cases and controls. The participants were categorized in two age groups, that is, 35–39 years and 40–44 years. Equal number of cases and controls were taken in these age groups. Furthermore, equal number of males and females were present among cases and controls.
Based on the prevalence of periodontitis in diabetics and nondiabetics, that is, 85% and 75%, respectively,[7] considering error 5% and power of the study, 80%, sample size was calculated using the standard formula (n = 2[Zα +Zβ]2 pq/[p1 p2 ]2) . This it was estimated that 185 cases and 185 controls would be required.
A tailor-made questionnaire, face validated by 5 subject experts, was used to interview the participants. Repetitive questions were removed and ambiguous questions were modified. The content validity ratio obtained was 0.99 and was thought to be acceptable. The final questionnaire comprised 11 close-ended and 1 open-ended questions. The participants were examined for dental caries using the WHO Dentition Status 2013.[6] The periodontal status was assessed using community periodontal index (CPI) and loss of attachment[6] and was also categorized as mild, moderate, and sever according to the American Academy of Periodontology.[8] A pilot study was conducted among 30 cases and 30 controls to assess comprehensibility of the questionnaire and feasibility of the study.
Belagavi city was divided into four zones and two hospitals from each zone were randomly selected. Known cases of T2DM were selected from each hospital. RBS estimation of the study participants was done using Accu-Chek Active glucometer kit. RBS levels above 200 mg/dl were considered as poor glycemic control.[9] The interview of study participants included their sociodemographic details, relevant medical history, family history, duration of T2DM, oral hygiene, and dietary behaviors followed by oral examination. Sterilization of the instruments for oral examination was done by autoclave using standard procedure.
Interview and oral examination was done by a single investigator, trained in the Department of Public Health Dentistry of the Institute under the guidance of a professor. It was done for recording RBS levels using the glucometer kit, WHO dentition status 2013, and CPI and loss of attachment. A recording clerk was trained to assist for recording the findings throughout the study. The glucometer was calibrated after every 10 patients using glucose control solution Level 1 (concentration: 50 mg/dl). The intra-examiner reliability resulted in a weighted kappa of 0.85 for WHO dentition status (2013) and 0.80 for CPI.
The data obtained were entered into Microsoft Excel sheet, and the statistical analysis of the same was done using SPSS software version 20.0 (IBM, Chicago, IL, USA). The data were summarized using descriptive statistics. Appropriate parametric and nonparametric tests were applied. Univariate analysis was carried out and the variables which were found to be significantly associated with T2DM were subjected to multiple logistic regression. In all the statistical tests, P < 0.05 was considered statistically significant.
RESULTS
Among 185 T2DM cases, 88 (47.6%) were female and 97 were male (52.4%) and a similar gender-wise distribution was there among the controls. Equal number of T2DM cases and controls belonged to 40–44 years’ age group and 35–39 years’ age group. Cases and controls belonged to similar socioeconomic strata. A significantly higher number of T2DM cases, 44 (23.8%) as compared to controls, had a positive family history of diabetes (P = 0.001). Dietary sugar exposure was significantly less in T2DM cases (sugar score <5) as compared to controls (P = 0.001) [Table 1]. Table 1 shows the details of oral hygiene practices and dental visits among study participants.
Table 1.
Family history for diabetes, dietary sugar exposure and oral heath behaviours among study participants
| Variables | Cases, n (%) | Controls, n (%) | Total, n (%) | P |
|---|---|---|---|---|
| Family history for diabetesa | ||||
| None | 100 (54.1) | 143 (77.3) | 243 (65.7) | 0.001* |
| Father | 48 (26.0) | 29 (15.7) | 73 (19.7) | |
| Mother | 34 (18.4) | 13 (7) | 47 (12.7) | |
| Both parents | 3 (1.6) | 0 | 3 (0.8) | |
| Dietary sugar exposurea | ||||
| Excellent | 103 (55.7) | 26 (14.1) | 129 (34.9) | 0.001* |
| Good | 63 (34) | 87 (47) | 150 (40.5) | |
| Watch out zone | 19 (10.3) | 72 (38.9) | 91 (24.6) | |
| Frequency of toothbrushinga | ||||
| Never | 1 (0.5) | 0 | 1 (0.3) | 0.316 |
| Once a day | 140 (75.7) | 148 (80) | 288 (77.8) | |
| Twice a day | 42 (22.7) | 37 (20) | 79 (21.4) | |
| More than twice a day | 2 (1.1) | 0 | 2 (0.5) | |
| Does your toothpaste contain fluoride?a | ||||
| Yes | 101 (54.6) | 117 (63.2) | 218 (58.9) | 0.027* |
| No | 65 (35.1) | 62 (33.5) | 127 (34.3) | |
| Don’t know | 19 (10.2) | 6 (1.6) | 25 (6.8) | |
| Do you use any interdental AIDS?a | ||||
| Yes | 2 (1.1) | 8 (2.2) | 10 (2.7) | 0.08 |
| No | 183 (98.9) | 177 (95.7) | 360 (97.3) | |
| Duration of brushing | ||||
| <2 min | 132 (32.7) | 174 (47) | 306 (82.7) | 0.000 |
| 2-4 min | 52 (14) | 10 (2.7) | 62 (16.7) | |
| >4 min | 1 (0.3) | 1 (0.3) | 2 (0.6) | |
| Last dental visit | ||||
| 1-2 years back | 64 (34.6) | 41 (22.2) | 105 (28.4) | |
| >2 years | 41 (22.2) | 38 (20.5) | 79 (21.4) | |
| Never visited | 80 (43.2) | 106 (57.3) | 186 (50.2) | |
| Reason for last visit | ||||
| Extraction | 65 (35.1) | 38 (20.54) | 103 (27.9) | |
| Filling | 7 (3.8) | 26 (14.0) | 33 (8.9) | |
| Scaling | 14 (7.5) | 15 (8.1) | 31 (8.4) | |
| Root canal treatment | 1 (0.5) | 0 | 1 (0.5) | |
| Prosthesis | 14 (7.5) | 0 | 14 (3.7) | |
| Regular checkup | 4 (2.2) | 0 | 4 (1.1) | |
| None | 80 (43.2) | 106 (57.3) | 186 (50.3) | |
| Total | 185 | 185 | 370 |
Test applied: aChi-square test; *Statistically significant (P<0.05). P – P-value; n – Frequencies
There was a significant difference in the prevalence of periodontitis among the two groups (P = 0.000). The odds ratio indicated that cases were 6.6 times at a higher risk of developing periodontitis as compared to controls. A significantly lesser number of T2DM had dental caries as compared to controls (P = 0.001) [Table 2].
Table 2.
Crude odds ratio for periodontitis and dental caries among study participants
| Cases, n (%) | Controls, n (%) | Crude OR | Relative risk | Total, n (%) | P | |
|---|---|---|---|---|---|---|
| Periodontitisa | ||||||
| Present | 47 (25.4) | 8 (4.3) | 6.6 | 1.97 | 55 (14.9) | 0.000* |
| Absent | 138 (74.6) | 177 (95.7) | 315 (85.1) | |||
| Dental cariesa | ||||||
| Present | 137 (74.0) | 162 (87.6) | 0.405 | 0.67 | 299 (80.8) | 0.001* |
| Absent | 48 (26.0) | 23 (12.4) | 71 (19.2) | |||
| Total | 185 | 185 | 370 |
Test applied: aChi-square test. *Statistically Significant (P<0.05). OR – Odds ratio; P – P-value; n – Frequencies
The mean decayed missing filled teeth (DMFT) was 2.66 (±2.52) among diabetics and 3.34 (±2.11) among controls. The differences in the mean decayed teeth (P = 0.001) and mean DMFT were statistically significant (P = 0.006) between both the groups. Table 3 shows mean DMFT, CPI, and loss of attachment among study participants. Table 4 shows the correlation of RBS levels and duration of diabetes with loss of attachment and probing depth. Furthermore, significant differences (P = 0.001) with respect to periodontitis were observed between the two groups when categorized according to AAP classification [Figure 1].
Table 3.
Comparative assessment of mean Decayed Missing Filled Teeth, Community Periodontal Index and loss of attachment among study participants
| Variable | Mean±SD | P | |
|---|---|---|---|
|
| |||
| Cases | Controls | ||
| DMFTa | |||
| Decayed teeth | 1.84±1.82 | 2.67±1.99 | 0.001* |
| Missing teeth | 0.59±1.32 | 0.62±1.62 | 0.88 |
| Filled teeth | 0.31±1.13 | 0.24±0.63 | 0.46 |
| DMFT | 2.66±2.52 | 3.34±2.11 | 0.006* |
| CPIb | |||
| Bleeding on probing | 130 (70.3) | 146 (78.9) | 0.066 |
| Periodontal Pocket | 47 (25.4) | 8 (4.3) | 0.001* |
| LOAb | 0.001* | ||
| 0-3 mm | 104 (56.2) | 169 (91.4) | |
| 4-5 mm | 73 (39.5) | 16 (8.6) | |
| 6-8 mm | 8 (4.3) | 0 (0.5) | |
| 9-11 mm | 0 | 0 | |
| 12 mm or more | 0 | 0 | |
Test applied: aIndependent t test, bChi-square test. *Statistically significant (P<0.05). CPI – Community Periodontal Index; DMFT – Decayed Missing Filled Teeth; LOA – Loss of attachment; SD – Standard deviation; P – P-value
Table 4.
Correlation of random blood sugar levels and duration of diabetes with loss attachment and probing depth
| LOA (mm) | Probing depth (mm) | |||
|---|---|---|---|---|
|
|
|
|||
| Pearson correlation coefficient | P | Pearson correlation coefficient | P | |
| RBS levels (mg/dl) | 0.151 | 0.040* | 0.150# | 0.042* |
| Duration of diabetes (years) | 0.080 | 0.138 | 0.167# | 0.023* |
#Pearson correlation coefficient; *Statistically significant (P<0.05). RBS – Random blood sugar; LOA – Loss of attachment; P – P-value
Figure 1.
Distribution of study participants according to gingival and periodontal disease as per American Academy of Periodontology
In multiple logistic regression analysis, diabetes was the dependent variable and family history, use of toothbrush and toothpaste, periodontitis, loss of attachment, and sugar score as independent variables. The odds of having a positive family history were 2.29 times in T2DM participants (95% confidence interval [CI]: 1.261–4.168, P = 0.007) as compared to controls. The odds of T2DM cases being in the excellent zone were 19 times more (95% CI: 8.243–44.771, P = 0.001) as compared to controls. The odds of diabetic participants having periodontitis were 2.49 times higher (95% CI: 1.214–6.778, P = 0. 0.075) than controls. The odds of T2DM cases having loss of attachment were 5.8 times (95% CI: 2.819–6.889, P = 0.001) more than controls [Table 5]. There was no significant difference between the loss of attachment and periodontal probing depth between T2DM cases having controlled and uncontrolled blood glucose levels. Table 6 shows the association of loss of attachment and periodontal probing depth among cases based on glycemic control.
Table 5.
Odds ratio and 95% confidence interval for diabetes as dependent variable according to multiple logistic regression
| Independent variables | OR | 95% CI | P |
|---|---|---|---|
| Positive family history for diabetes | |||
| Present | 2.292 | 1.261-4.168 | 0.007* |
| Absent | |||
| Use of toothbrush and toothpaste | |||
| Yes | 0.574 | 0.361-1.317 | 0.082 |
| No | |||
| Periodontitis | |||
| Present | 2.493 | 1.214-6.778 | 0.075 |
| Absent | |||
| Sugar score | |||
| Excellent | 19.211 | 8.243-44.771 | 0.001* |
| Good | 2.985 | 1.378-6.466 | 0.006* |
| Watch out zone | |||
| LOA | |||
| esent | 5.88 | 2.819-6.889 | 0.001* |
| Absent |
The adjusted variables include: Duration of brushing, fluoride content of dentifrice, attitude towards dental visit, awareness of diet and exercise; *Statistically significant (P<0.05). OR – Odds ratio; CI – Confidence interval; LOA – Loss of attachment; P – P-value; n – frequency
Table 6.
Association of loss of attachment and periodontal probing depth among type 2 diabetes mellitus cases
| Variable | Controlled Total=85 (45.9), n (%) | Uncontrolled** Total=100 (54.1), n (%) | P |
|---|---|---|---|
| LOA | |||
| No LOA | 53 (28) | 51 (27.6) | 0.298 |
| LOA 4-5 mm | 29 (15.7) | 44 (23.8) | |
| LOA >6 mm | 3 (1.6) | 5 (2.7) | |
| PPD | |||
| Normal sulcular depth | 68 (36.8) | 71 (38.4) | 0.279 |
| 4-5 mm depth | 17 (9.2) | 28 (15.1) | |
| >6 mm depth | 0 (0) | 1 (0.5) |
Test applied: Chi-square test (P<0.05 considered statistically significant). **RBS values above 200 mg/dl considered uncontrolled DM. LOA – Loss of attachment; PPD – Periodontal probing depth; RBS – Random blood sugar; DM – Diabetes mellitus; P – P-value. n – frequency
DISCUSSION
The global prevalence of diabetes mellitus by 2030 is estimated to be 522 million, which will account for 7.7% of the population having the disease.[10] Microvascular changes can result in periodontal destruction, while altered salivary function can lead to increased susceptibility to dental caries in patients suffering from T2DM. This can deteriorate the oral health and can have an impact on the day to day activities of an individual. Most of the studies pertaining to T2DM and dental diseases are in older age groups. The WHO has recommended the age group of 35–44 years for surveillance of oral health conditions in adults.[6]
Oral hygiene habits such as brushing frequency, use of interdental aids, and duration of brushing of all participants were assessed in the present study. These factors indirectly contribute to local irritation of the gingiva. There was no significant difference in oral hygiene practices among cases and controls as both belonged to the same demographic cohort. Study participants in both groups showed poor brushing frequency. Our study reported that only a few number of study participants brushed their teeth for 2–4 min, which is the optimum time for brushing.[11] A considerable number of diabetic participants used finger and toothpowder to clean their teeth. Most of the cases and controls used a fluoridated dentifrice in the present study. Very few study participants used interdental aids when compared to other studies.[12] A study suggests that poor oral hygiene practice was significantly associated with periodontal disease in diabetics.[4] The present study also highlighted the fact that only few participants (1.1%) were interested in getting a regular dental checkup done. Furthermore, most of the study participants in both the groups had visited the dentist for extraction. This indicated poor utilization of dental care and that the dental care was availed only in the advanced stage of dental disease.
The CPI developed by the WHO is commonly used internationally for screening of periodontal disease.[13] The WHO oral health assessment form for adults includes CPI modified and loss of attachment which were used in the present study. The CPI modified helps in assessing bleeding on probing and periodontal pocket depth in all teeth present in the oral cavity. The presence of bleeding on probing is considered a primary parameter for assessing gingivitis.[14] The present study assessed presence or absence of gingival disease and the extent of periodontal destruction. A higher number of controls (78.9%) than T2DM (70.4%) had bleeding on probing, which was indicative of gingivitis. However, previous studies reported more number of diabetics having bleeding on probing as compared to controls.[15] Furthermore, a higher number of T2DM cases (25.4%) had periodontal pockets than controls (4.3%). An Indian study reported of almost 50% prevalence of periodontal pockets in T2DM cases aged 35 years and above.[16]
Loss of attachment of 4–5 mm was found more in T2DM cases (39.5%) than controls (8.6%). Furthermore, a few number of T2DM participants had a loss of attachment of 6–8 mm. This depicted that periodontal disease was more severe in T2DM cases than controls. These findings were in accordance to a study conducted by Soni et al.[16] When classified according to the American Academy of Periodontology,[8] periodontitis prevalence was higher in T2DM cases than controls. Most of the T2DM cases had mild (39.5%) or moderate (4.3%) periodontitis. Findings of the present study revealed that there was almost a 6-fold higher risk among diabetic participants for periodontitis as compared to controls. After adjusting the confounders, T2DM cases were 5.8 times at a risk of having a clinical attachment loss. In a systematic review of 53 observational studies conducted in 2020, the prevalence of periodontitis among T2DM cases was 1.58 times and was statistically significant.[4] In a case–control study conducted in Saudi Arabian adults, multivariate analysis depicted 3 times greater odds of diabetic individuals having periodontitis.[17] The present study showed a significant correlation between increasing blood sugar levels and severity of periodontitis. Singh et al. identified that more than 95% of T2DM cases had some periodontal destruction and severe periodontitis, which was associated with poor glycemic control.[18] Similar findings were reported by Dhir et al. and Romano et al.[19,20]
Previous studies suggest that caries prevalence is higher in diabetic individuals due to higher Streptococcus mutans counts than nondiabetic individuals.[21] In the present study, dental caries prevalence and mean DMFT were higher in was higher than T2DM cases. This could be due to more number of diabetic participants brushing their teeth twice daily. Furthermore, the diabetic patients were known cases and they had restricted sugar intake as compared to controls as depicted by their sugar score. Use of fluoridated tooth paste was also assessed, since a large body of evidence suggests that fluoridated tooth paste contributes to caries prevention.[22] Similar findings are reported by Subramanian et al.[23]
Family history for T2DM was considered positive if either of the parents or both had diabetes. The present case–control study showed that positive family history was found to be a strong predictor for T2DM. These findings were supported by Scott et al.[24] and Sakurai et al.[25] After adjusting for the confounders, a significantly higher number of T2DM cases had loss of attachment associated with periodontitis. A considerable number of controls had a positive family history. A familial history of T2DM is a risk factor for T2DM as well as early onset type 1 diabetes.[26,27] Creating awareness in cases as well as controls is thus important.
The interpretation of the present study findings could be influenced by certain limitations. Numerous factors such as calculus and plaque scores, host immune response, and composition of saliva could affect the incidence of oral diseases, which were not taken into consideration. As HbA1c for such a large sample size was not cost effective, it was not used. In the present study, we have included only confirmed diabetic patients. Prediabetes and body mass index are other strong predictors for T2DM. These predictors could be incorporated in future prospective studies. The study might have been subjected to memory recall bias or social desirability bias. Within the limitations of the study, a more sensitive index as used in clinical studies, which could measure bleeding spontaneity, could be used. Future studies can be done using the new classification of periodontal diseases proposed by Caton et al. which will aid in grading the condition according to the type of management.[14]
CONCLUSION
The dental caries experience among T2DM cases was lower than nondiabetics. In the regression analysis, the odds of T2DM cases having loss of attachment were 5.8 times as compared to nondiabetics. The study helped us seek novel information that there was no positive correlation between T2DM and dental caries in the age range of 35–44 years. The data obtained from the present study could help in allocation of resources for health care and can be of aid for health professionals in creating awareness in this high-risk group.
Financial support and sponsorship
This work was funded by the Indian Council of Medical Research, New Delhi. (No. 3/2/Sept. 2016/PG-Thesis-HRD 21).
Conflicts of interest
There are no conflicts of interest.
Acknowledgment
We acknowledge Dr. Ravi Shirahatti and Dr. Mridula Tak for their contribution in statistics.
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