[Downloaded free from http://www.ijph.in on Friday, February 17, 2023, IP: 187.189.31.

66]

Brief Research Article

Dental Caries and their Relation to HbA1c in Adults with Type 2

Diabetes Mellitus
Deepasri Mohan1, Yogesh Bhuvaneshwar2, Ramakrishnan Manjankarni Jeyaram3, Sukanya Saravanan4, Anandakumar Amutha5, Research Team*
1
Oral and Maxillofacial Pathologist, 2Prosthodontist, 3Oral and Maxillofacial Surgeon, 4Dental Consultant, Dental Department, Dr. Mohan’s Diabetes Specialities Centre,
5
Scientist & Head, Department of Childhood and Youth Onset Diabetes, Chennai, Tamil Nadu, India

Summary
Diabetes mellitus with poor glycemic control is often associated with dental caries. We aim to assess the relationship between dental caries
and HbA1c levels among adults with type 2 diabetes (T2D) in Chennai. A cutoff of HbA1c ≥7.0 to 7.9% (53–63 mmol/mol) was used to
define Group 1 (n = 113) as moderately controlled and HbA1c ≥8.0% (64 mmol/mol) to define Group 2 (n = 228) as poorly controlled T2D.
The absolute numbers of decayed, missing, and filled teeth were examined to calculate the decayed, missing and filled teeth index. Group 2
had a significantly higher percentage (48.2%) of decayed teeth when compared to Group 1 (28.3%). Group 2 had a 2.65 times higher risk of
decayed teeth when adjusted for mean carbohydrate consumption, sweets consumption, oral hygiene, and brushing habit. T2D with higher
HbA1c levels is associated with an increased number of decayed teeth. Hence, there is a need for monitoring dental status in T2D as earlier
treatment may prevent or delay decay teeth.

Key words: Adults, decayed ,missing and filled teeth index, decayed teeth, glycated hemoglobin, India

The prevalence of diabetes is increasing all over the world, adults with no residual teeth, and those who did not do an
particularly in developing countries. China and India alone A1c test (a total of 27 patients) during the visit were excluded
contribute about 40% of all people with diabetes in the from the study. Of the remaining 341, a cutoff of HbA1c ≥ 7.0
world.[1] The human oral cavity and contiguous structures can to 7.9%  (53–63 mmol/mol) was used to define Group  1 as
be affected by diabetes. Both diabetes and dental caries are moderately controlled T2D and HbA1c ≥ 8.0% (64 mmol/mol)
associated with ingestion of carbohydrates and an increase in was considered Group 2 as poorly controlled T2D following
insulin deficiency may lead to hyposalivation and an increase the less stringent goals of the American Diabetes Association
in salivary glucose level, leading to dental caries.[2] The present 2021 standards of medical care in diabetes.[3]
study aimed to assess the relationship between dental caries Basic demographic details, anthropometrics, dietary
and  glycated haemoglobin (HbA1c) levels among adults with history, and lifestyle habits of all the study participants
Type 2 diabetes (T2D) seen at a diabetes center in South India. were recorded. Plasma glucose (hexokinase method)
was measured on Beckman Coulter AU2700 Fullerton,
This study is a retrospective data of 368 consecutive adults with
California, USA) biochemistry analyzer. HbA1c was
T2D who visited the dental department of a tertiary care center
estimated by high‑performance liquid chromatography
for diabetes in Chennai from October 2017 to December 2017.
Of the 368 adults, type 1 diabetes, gestational diabetes women,
Address for correspondence: Dr. Sukanya Saravanan,
impaired glucose tolerance, fibrocalculous pancreatic diabetes,
Dental Consultant, Dr. Mohans Diabetes Specialities Centre, Chennai,
Tamil Nadu, India.
Access this article online
E-mail: [email protected]
Quick Response Code:
Website:
www.ijph.in This is an open access journal, and articles are distributed under the terms of the Creative
Commons Attribution‑NonCommercial‑ShareAlike 4.0 License, which allows others to
remix, tweak, and build upon the work non‑commercially, as long as appropriate credit
DOI: is given and the new creations are licensed under the identical terms.
10.4103/ijph.ijph_1935_21 For reprints contact: [email protected]

Submitted: 16‑Oct‑2021 Revised: 29‑Apr‑2022

*Research team: Accepted: 02‑May‑2022 Published: 12-Jul-2022
Radhakrishnan Subashini6, Ranjit Mohan Anjana7, Viswanathan Mohan8
6
Senior Biostatistician, Department of Biostatistics, Madras Diabetes Research How to cite this article: Mohan D, Bhuvaneshwar Y, Jeyaram RM,
Foundation, 7Managing Director & Diabetologist, 8Chairman & Chief Diabetologist, Saravanan S, Amutha A, Research Team. Dental caries and their relation
Department of Diabetology, Dr. Mohan’s Diabetes Specialities Centre and Madras to HbA1c in adults with type 2 diabetes mellitus. Indian J Public Health
Diabetes Research Foundation, Gopalapuram, Chennai, Tamil Nadu, India 2022;66:206-9.

206 © 2022 Indian Journal of Public Health | Published by Wolters Kluwer - Medknow
[Downloaded free from http://www.ijph.in on Friday, February 17, 2023, IP: 187.189.31.66]

Mohan, et al.: Dental caries and glycated haemoglobin in T2D

using the variant machine (Bio‑Rad, Hercules, California, All statistical analyses were conducted using SPSS
USA). Diabetes was diagnosed if the fasting plasma glucose statistical package version 15.0 (SPSS Inc., Chicago,
level was ≥126 mg/dL (7.0 mmol/L) and/or the 2‑h postload Illinois, USA). Normally distributed continuous variables
glucose level was  ≥200  mg/dL  (11.1 mmol/L) and/or if were summarized as mean ± standard deviation, whereas
the participants had been prescribed pharmacotherapy for categorical variables were presented as proportions.
diabetes by a physician. Univariate logistic regression was performed with
decayed tooth (Y/N) as the dependent variable to identify
Dentists clinically examined adults with T2D following the
independent risk factors for a decayed tooth. Multiple
prestructured case sheet of the dental department. Dental
logistic regression was conducted to identify the association
caries was measured visually and no radiographs were taken.
between the decayed tooth and HbA1c ≥8% while adjusting
The absolute numbers of decayed (DT), missing (MT),
for carbohydrate consumption, adherence to sweets
and filled teeth  (FT) were examined for the participants.
consumption, oral hygiene index, and brushing habit.
DMF‑T index is calculated which is a sum of DT + MT + FT.
Both filled and crowned teeth were taken as FT. Third Clinical characteristics, dental caries, and periodontal status of
molars were included. Met Need Index (MNI) indicates the the moderately controlled T2D (Group 1; n = 113) and poorly
treatment received by an individual and it was calculated as controlled T2D (Group 2; n = 228) are presented in Table 1. The
([MT + FT]/[DT + MT + FT] X100).[4] Bleeding on probing presence of dental caries (48.2% vs 28.3) and the mean number
was considered positive if bleeding occurred within 30 seconds of decayed teeth (1.15±1.7 vs 0.60±1.3) are significantly higher
after probing. Periodontal probing was done on each tooth, and in Group 2 when compared to Group 1. The mean number of
the number of teeth with periodontal probing depth ≥4 mm DMF‑T index was higher among Group 2 than in Group 1,
on at least one tooth surface was shown to be associated with but it does not reach significance. The MNI was lower among
periodontitis.[5] Ethical approval of this study was provided Group 2 (P = 0.023). Although the mean value of percentage
by the Institutional Ethics Committee of Madras Diabetic of teeth with bleeding on probing is higher among Group 2,
Research Foundation  (MDRF/NCT/08‑02/2020). Patient there was no significant difference (P = 0.110) between the
written informed consent to use their anonymized medical two groups but percentage of teeth with periodontal pocket
data was obtained from all study subjects. depth was significant between the two groups (6.55 vs. 9.54;

Table 1: Clinical characteristics, dental caries and periodontal status of adults with type 2 diabetes
Clinical characteristics Group 1 (HbA1c ≥7.0-7.9) (n=113) Group 2 (HbA1c ≥8) (n=228) P
Gender - Male, n (%) [CI] 70 (61.9) [52.8-70.5] 152 (66.7) [60.4-72.5] 0.389
Age (years)† 56.0±9.9 [54.2-57.9] 54.3±10.4 [53.0-55.7] 0.153
Duration of diabetes (years)† 12.5±8.2 [11.0-14.1] 11.7±7.9 [10.7-12.7] 0.367
BMI (kg/m2)† 26.7±4.0 [26.0-27.5] 26.9±3.9 [26.4-27.4] 0.752
FPG (mg/dl)† 139±32 [133.3-145.5] 209±68 [199.9-218.0] <0.001*
HbA1c (%)† 7.2±0.4 [7.1-7.3] 9.8±1.5 [9.6-10.0] <0.001*
Treatment, n (%) [CI]
OHAs 112 (78.3) [66.7-82.5] 107 (46.9) [40.5-53.4] <0.001*
Insulin and OHA 31 (21.7) [17.5-33.3] 121 (53.1) [46.6-59.5
DT - Yes, n (%) [CI] 32 (28.3) [20.6-37.1] 110 (48.2) [41.8-54.7] <0.001*
Brushing habit, n (%) [CI]
Once 92 (81.4) [73.5-87.7] 193 (84.6) [79.5-88.9] 0.448
Twice 21 (18.6) [12.3-26.5] 35 (15.4) [11.1-20.5]
Dental variables
Number of DT† 0.60±1.3 [0.36-0.85] 1.15±1.7 [0.92-1.4] 0.001*
Number of MT† 1.46±2.22 [1.05-1.87] 1.43±2.18 [1.15-1.71] 0.905
Number of FT† 0.64±2.22 [0.22-1.05] 0.59±1.73 [0.37-0.82] 0.850
DMF‑T index† 2.70±3.44 [2.06-3.35] 3.17±3.43 [2.71-3.61] 0.235
MNI† 72.0±39.7 [63.1-80.9] 59.5±39.0 [53.6-65.6] 0.023*
Percentage of BOP† 16.1±13.6 [12.5-19.8] 19.8±15.1 [17.1-22.6] 0.110
Percentage PPD ≥4 mm† 6.55±6.47 [4.80-8.30] 9.54±8.07 [8.09-11.00] 0.010*
OHI‑S, n (%) [CI]
Good 3 (2.7) [0.8-6.9] 6 (2.6) [1.1-5.3] 0.168
Fair 106 (93.8) [88.2-97.2] 203 (89.0) [84.5-92.6]
Poor 4 (3.5) [1.2-8.2] 19 (8.3) [5.3-12.4]
*Significant P<0.05, †Mean±SD, CI. BMI: Body mass index, FPG: Fasting plasma glucose, HbA1c: Glycated hemoglobin, OHAs: Oral hypoglycemic
agents, DT: Decayed teeth, MT: Missing teeth, FT: Filled teeth, MNI: Met need index, BOP: Bleeding on probing, PPD: Periodontal pocket depth, OHI-S:
Oral Hygiene Index- Simplified, SD: Standard deviation, CI: Confidence interval, DMF‑T: Decayed, missing, and filled teeth

Indian Journal of Public Health  ¦  Volume 66  ¦  Issue 2  ¦  April-June 2022 207
[Downloaded free from http://www.ijph.in on Friday, February 17, 2023, IP: 187.189.31.66]

Mohan, et al.: Dental caries and glycated haemoglobin in T2D

P = 0.010). When compared to Group 1, poor oral hygiene value even after adjusting for dental attendance.[6] However, in our
index was higher (3.5% vs. 8.3%) in Group 2. study, an association with uncontrolled diabetes was seen even
after adjusting for carbohydrate consumption along with sweets
Analysis of food items and macronutrient intake showed that
adherence, oral hygiene, and brushing habits.
77.3%, 67.6%, 68.6%, and 45.9% of Group 2 adults consumed
more sweets, beverages, nuts, and oils, respectively, when There are several studies done in India relating diabetes
compared to Group 1 (P = 0.027, P = 0.045, P = 0.018, and mellitus with periodontitis[10] and dental caries[6,8] between
P  =  0.010, respectively). A significant reduction of mean the diabetic and nondiabetic populations. The novelty of the
protein (P = 0.019) and fiber (P = 0.030) intake was seen study lies in the fact that to our knowledge, this is the first
in Group 2. In Table 2, when adjusted for carbohydrate and clinic‑based study done to look at the association between
sweets consumption, oral hygiene, and brushing habit, Group 2 the number of decayed teeth and HbA1c levels in adults with
had (odds ratio: 2.65; confidence interval: 1.50–4.65; P = 0.001) T2D and to link it to the dietary intake and other factors.
a higher risk of having a greater number of decayed teeth. Most dental patients in India turn up to the dentist only when
The study findings indicate that adults with T2D who have they are in pain. Till now, there are no criteria for referring
HbA1c ≥8.0% have a greater number of decayed teeth than a diabetic patient to a dentist by general physicians unless
those who have HbA1c ≥7.0%–7.9%. Consumption of sweets they are symptomatic. Hence, we suggest that HbA1c can
and carbohydrates was an additional risk factor along with be considered as a criteria by the diabetologists and they can
HbA1c for decayed teeth among adults with T2D. enlighten patients with poor glycemic control (HbA1c ≥8.0%)
to have a regular dental checkup. This helps to maintain their
In our study, the percentage of decayed teeth was more oral hygiene and aids the patients financially by treating the
in Group  2  (48.2%), which is similar to a study reported dental problems at an early stage rather than spending more
in Tokyo  (49.7%).[6] Oral cariogenic organisms such as money for complex and costly dental treatment in a later stage
Treponema denticola, Streptococcus sanguis, Prevotella of the oral disease.
nigricans, and Streptococcus intermedius were present in the
supragingival plaque of poorly controlled T2D patients due to One of the limitations of the study is that being a retrospective
hyposalivation, low salivary calcium level, and upregulated study, there is a possibility of selection bias. Second, the site of
salivary alkaline phosphatase activity.[7] Our study results are in the caries was not taken into account namely whether it is coronal
accordance with studies[8,9] that found a significant association or root surface caries. Third, only bleeding on probing and
between decayed teeth and HbA1c in adults with T2D. periodontal pocket depth were assessed for the study participants.
Finally, we selected only those who had HbA1c ≥7.0%–7.9%
The MNI was significantly lower in those with poorly
as moderately controlled and  ≥8.0% as poorly controlled
controlled diabetes, which suggests that their dental treatment
diabetes for the current study outcome and could not assess the
needs were not fulfilled to the same extent as the group with
association of dental caries in participants with good diabetes
better diabetes control, which is similar to a study done by
control (HbA1c <7.0%), as ADA glycemic target is <7.0%.
Yonekura et al.[8] These results concerning MNI suggest that
dental intervention for decayed teeth may be beneficial for Hence, a prospective cohort study with adjustment for
those with poorly controlled T2D. confounders including dental examinations (attachment loss,
A cross‑sectional study on 1897 participants revealed a significant plaque index, gingival index, and alveolar bone resorption) and
association between decayed teeth and HbA1c levels in T2D biological and immunological profile of saliva would throw
adults with an HbA1c of ≥8.0% compared to those with a lower more light on the association of diabetes with dental caries.
This study suggests that T2D with higher HbA1c levels have
an increased number of decayed teeth than those with lower
Table 2: Multiple logistic regression analysis using
decayed teeth as dependent variable HbA1c levels. Hence, there is a need for monitoring dental
status in T2D patients as earlier treatment may prevent or
Risk factor DT (yes) delay decay teeth and also educate them about the association
OR (CI) P between dental decay and control of diabetes. Thereby, this
HbA1c≥8% (Group 2) unadjusted 2.36 (1.45-3.83) 0.001* study calls attention to plan strategies to incorporate dental
Model 1 ‑ Adjusted for CHO 2.68 (1.57-4.56) <0.001* examination within the existing noncommunicable disease
Model 2 Model 1+ adjusted for 2.71 (1.54-4.76) 0.001* control programs.
sweets consumption
Model 3 ‑ Model 2+ oral hygiene 2.68 (1.53-4.72) 0.001* Acknowledgments
Model 4 ‑ Model 3+ brushing habit 2.65 (1.50-4.65) 0.001* The authors thank all the participants in the study and the
*Significant at P<0.05. Values are given as OR (95% CI). Model 1 staff of Dr. Mohans’ Diabetes Specialities Centre and Madras
adjusted for carbohydrates, Model 2, as for Model 1 plus adjusted
for sweets consumption; Model 3, as for Model 2 plus oral hygiene Diabetes Research Foundation.
and Model 4, as for Model 3 plus brushing habit. OR=Odds ratio,
CI=Confidence interval, CHO=Carbohydrates, DT: Decayed teeth, Financial support and sponsorship
HbA1c: Glycated hemoglobin Nil.

208 Indian Journal of Public Health  ¦  Volume 66  ¦  Issue 2  ¦  April-June 2022
[Downloaded free from http://www.ijph.in on Friday, February 17, 2023, IP: 187.189.31.66]

Mohan, et al.: Dental caries and glycated haemoglobin in T2D

Conflicts of interest 6. Suzuki S, Yoshino K, Takayanagi A, Ishizuka Y, Satou R, Nara N, et al.

Relationship between blood HbA1c level and decayed teeth in patients
There are no conflicts of interest. with type  2 diabetes: A  cross-sectional study. Bull Tokyo Dent Coll
2019;60:89-96.
References 7. Hintao J, Teanpaisan R, Chongsuvivatwong V, Ratarasan C, Dahlen G.
The microbiological profiles of saliva, supragingival and subgingival
1. Mohan V. Expanding the concept of “clinical inertia in diabetes. plaque and dental caries in adults with and without type  2 diabetes
J Diabetol 2019;10:1-3. mellitus. Oral Microbiol Immunol 2007;22:175-81.
2. Moin M, Malik A. Frequency of dental caries and level of risk among 8. Yonekura S, Usui M, Murano S. Association between numbers of
type II diabetics. Dentistry 2015;5:334. decayed teeth and HbA1c in Japanese patients with type  2 diabetes
3. American Diabetes Association. 6. Glycemic targets: Standards of mellitus. Ups J Med Sci 2017;122:108-13.
medical care in diabetes-2021. Diabetes Care 2021;44:S73-84. 9. Majbauddin A, Tanimura C, Aoto H, Otani S, Parrenas MC,
4. Al-Maweri SA, Halboub ES, Al-Soneidar WA, Al-Sufyani GA.  Oral Kobayashi N, et al. Association between dental caries indicators and
lesions and dental status of autistic children in Yemen: A case-control serum glycated hemoglobin levels among patients with type 2 diabetes
study. J Int Soc Prev Community Dent 2014;4(Suppl 3):S199-203. mellitus. J Oral Sci 2019;61:335-42.
5. Loesche  WJ, Grossman  NS. Periodontal disease as a specific, albeit 10. Sundar  C, Ramalingam  S, Mohan  V, Pradeepa  R, Ramakrishnan  MJ.
chronic, infection: Diagnosis and treatment. Clin Microbiol Rev Periodontal therapy as an adjunctive modality for HbA1c reduction in
2001;14:727-52. type-2 diabetic patients. J Educ Health Promot 2018;7:152.

Indian Journal of Public Health  ¦  Volume 66  ¦  Issue 2  ¦  April-June 2022 209