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An analytical approach to explore clinico-biochemical relationship between type 2 diabetes mellitus (T2DM) and oro-dental diseases including chronic periodontitis.

INTRODUCTION

Type 2 Diabetes Mellitus (T2DM) is a significant public health concern. International Diabetes Federation projects that 642 million individuals will have diabetes by the year 2040. (1) T2DM is associated with concomitant oral and dental manifestations. A two-way relationship between diabetes mellitus and chronic periodontitis has been proposed that not only patients with T2DM are more susceptible to chronic periodontitis, but the presence of chronic periodontitis also affects glycaemic control. (2) Interactions between these two diseases that have important clinical implications for dental professionals, physicians, and most importantly patients. There is scarcity of data on oral complications in patients with T2DM from India particularly the Eastern part till date. This study has been taken up to study various oro-dental conditions particularly chronic periodontitis and their correlation with glycaemic status and with other complications in patients with T2DM. The main objectives were to study oro-dental manifestations in patients with T2DM with particular emphasis on chronic periodontitis.

We also evaluated the association between chronic periodontitis and glycaemic status, microvascular, and macrovascular complications among individuals having T2DM with and without chronic periodontitis.

MATERIAL AND METHODS

This was a hospital-based cross-sectional study. The study was approved by the Institutional Ethical Committee and informed consent was obtained from study subjects.

INCLUSION AND EXCLUSION CRITERIA WERE GIVEN BELOW

Inclusion Criteria

T2DM patients with age between 18 years and 65 years. Exclusion Criteria

1. Smokers and those consuming chewable tobacco.

2. Subjects with less than 20 teeth were excluded. This was to ensure that patients had sufficient teeth on which to assess periodontal health.

3. Systemic conditions affecting periodontal tissues other than T2DM like haemolytic anaemia, HIV infection, etc.

4. Medications with side effects shown to affect periodontal tissues like anticonvulsants (Phenytoin, phenobarbitone, valproate), calcium channel blockers (amlodipine, verapamil), and immunosuppressants (Cyclosporine).

5. Pregnant subjects.

All study subjects underwent meticulous clinical and laboratory evaluation as per standard practice of T2DM. HbA1c assay was done using Bio-Rad laboratory analyser by High Performance Liquid Chromatography method.

Hyposalivation was assessed by doing saliva collection. On day of saliva collection, patient was instructed to refrain from intake of any food or beverage (water exempted) one hour before the collection period. Saliva collection done by the patient was asked to void the mouth of saliva by swallowing. Patient was instructed to keep his/her mouth slightly open and to allow saliva to drain into Falcon 15 mL calibrated conical tube. Patient was classified as having hyposalivation if the saliva quantity was below 5 mL at end of 20-minute period. (3) Periodontal examination was done by a single examiner expert in periodontia to eliminate inter-examiner variability. Periodontal examination was conducted with all aseptic measures. Oral and dental examination was done according to WHO Oral Health Assessment Form. (4) Oral hygiene was assessed by OHI-S (Oral Hygiene Index-Simplified) were also assessed. Average individual debris and calculus scores were combined to obtain the OHI-S. (5,6) Measurements of probing pocket depth were performed at six sites per tooth: mesiobuccal, mid buccal, distobuccal, mesiolingual, mid lingual, and distolingual. Clinical Attachment Level (CAL) to the nearest millimeter was measured with calibrated University of North Carolina-15 probe (UNC-15) as the distance between the Cementoenamel Junction (CEJ) and the base of the pocket. Chronic periodontitis defined by presence of [greater than or equal to] 2 Interproximal sites with CAL [greater than or equal to] 4 mm or [greater than or equal to] 2 interproximal sites with Probing Depth [greater than or equal to] 5 mm developed by the Centres for Disease Control and Prevention (CDC) and the American Academy of Periodontology (AAP) Working Group. This was confirmed by radiological evidence of horizontal bone loss. (7)

STATISTICAL ANALYSIS

Data was collected and processed using SAS (Statistical Analysis System) version 9.1 for Windows, SAS Institute Inc. Cary, NC, USA. The results were presented as mean [+ or -] SD for normally distributed data and median (min-max) for nonparametric data. Normality of data was determined using Anderson-Darling test, Shapiro-Wilk test, and QQ plot. For significant difference of continuous variables between two groups, p values were calculated using unpaired t-test with equality of variance tested using Levene's test and for nonparametric data. P-values were calculated using Wilcoxon Mann-Whitney test. To test significant difference of continuous variables between more than two groups, ANOVA with post hoc Bonferroni tests was used for normally distributed data and Kruskal-Wallis test with multiple comparisons Bonferroni method was used for non-normally distributed data. Correlation coefficient was determined using Pearson or Spearman partial correlation test depending on the distribution of data. P<0.05 was considered to be statistically significant.

RESULTS

A total of 100 subjects with T2DM were studied for oro-dental manifestations. Hyposalivation was the most common oral symptom (58%) followed by halitosis (45%), burning mouth sensation (25%), stomatitis (18%), and taste impairment (23%) in subjects with T2DM. Periodontitis, tooth loss, dental caries were dental manifestations observed in 50%, 36%, and 24% respectively (Table 1).

Prevalence of oro-dental complications was studied among subjects well-controlled glycaemic status (HbA1C<7%) and uncontrolled glycaemic status (HbA1C>7%). Oral manifestations were significantly higher among T2DM subjects with uncontrolled glycaemic status except stomatitis and burning mouth sensation (Figure 1).

Patients with T2DM were analysed into two groups those with chronic periodontitis and those without chronic periodontitis. On comparison of glycaemic indices, it was observed that the FPG, PPG, HbA1c levels were higher in T2DM subjects with chronic periodontitis compared to those without a significant difference was observed between FPG, PPPG, and HbA1C values (p<0.05) among these groups. Duration of T2DM was more among T2DM with chronic periodontitis compared to those without (p<0.05). There was no significant difference between lipid parameters between two groups (Table 2).

FPG: fasting plasma glucose, PPPG: postprandial plasma glucose, HbA1C: haemoglobin A1C, GFR: estimated glomerular filtration rate, CVD: cardiovascular disease, DKD: diabetic kidney disease, OHI-S: oral hygiene index-simplified, CAL: clinical attachment loss, BOP: bleeding on probing, PPD: pocket probing depth.

Microvascular complications including diabetic kidney disease, retinopathy, neuropathy as well macrovascular complications were significantly higher among subjects with T2DM having chronic periodontitis as compared to those without (p<0.05) (Table 2). In the present study, most of the patients brushed only once a day in both groups. All of the patients in both groups used toothbrush and toothpaste (Table 2). Plaque Index (PI) and OHI-S, which are the markers of oral hygiene suggested similar oral hygiene status in both the groups (Table 2). There was statistically significant direct correlation between HbA1c and clinical attachment level unadjusted as well after adjustment done for serum creatinine, body mass index, plaque index, and OHI-S. (r=0.29 p=0.048). (Figure 2).

[FIGURE 2 OMITTED]

DISCUSSION

In the present study, hyposalivation (58%) was the most common oral manifestation. Hyposalivation being more common in present study was might be due to presence of neuropathy. Prevalence of hyposalivation varies among different studies. Similarly, Shrimali et al (8) reported significantly higher prevalence of hyposalivation among poorly-controlled patients with DM. Saliva possess lubricating and antimicrobial properties. Reduction in salivary quality and quantity results in increased susceptibility to dental caries, mucosal ulcers, and fungal infections. (9) In the present study, halitosis was observed among 45% subjects with T2DM. Halitosis is primarily caused by bacterial putrefaction and the generation of volatile sulfur compounds. Halitosis in individuals with DM is due to poor oral hygiene, periodontal disease. (10) Periodontitis, tooth loss, dental caries were observed in 50%, 36%, and 24% respectively (Table 2). Factors favouring an increased risk for dental caries among subjects with DM include increased glucose concentration in saliva and GCF, a reduced salivary flow rate. (11) The observations in present study were in accordance with studies conducted by Gibson. (12) and Sreebny. (13) Sreebny et al. (13) reported hyposalivation in 43% among 40 subjects with DM. Other oral complications included burning mouth sensation in 25%, stomatitis in 18%, taste impairment in 20%, and oral candidiasis in 8%. Oro-dental manifestations were significantly higher among T2DM subjects. Uncontrolled glycaemic status compared to well-controlled glycaemic status in the present study. Bajaj et al (14) reported periodontal disease in 34% followed by oral candidiasis in 24%, tooth loss in 24%, and dental caries in 24%, oral mucosal ulcers in 22%, taste impairment in 20%, halitosis in 16%, xerostomia and salivary gland hypofunction in 14%, and burning mouth sensation in 10% among 50 patients with DM.

In present study, glycaemic indices FPG, PPPG, HbA1c were higher in subjects with T2DM with chronic periodontitis than those without. In 4343 NHANES III (1988-1994) participants aged 45 years and older of whom 502 had diabetes, severe periodontitis was found in 14.3% of those with poorly-controlled diabetes (HbA1c >9%) and in 8.8% of those with "better" controlled (HbA1c [less than or equal to] 9%) diabetes compared to 4.1% among people without diabetes. After controlling for potential confounders, individuals with diabetes who had poor glycaemic control had 2.90 times and those with better control 1.56 times higher risk for periodontitis than individuals without diabetes. (15) In the present study, direct linear relationship between HbA1C and severity indicators of periodontitis, CAL, and number of sites with bleeding on probing was observed. Similarly, Anoop Kumar et al (16) observed positive correlation between worsening of glycaemic level and increase in severity of periodontitis. In this study, clinical attachment loss was found to be significantly associated with glycaemic control. Similarly, Collin et al (17) reported an association between advanced periodontal disease and impaired glycaemic control among 25 adults with DM. Apoorva et al (18) reported direct association between rising HbA1c levels and severity of periodontitis.

In the present study, microvascular complications as well as macrovascular complications were higher among the subjects with T2DM with chronic periodontitis compared to those without (Table 2). Diaz R et al (19) observed 41% prevalence of neuropathy among T2DM subjects with periodontitis. They observed significant association between severe periodontitis and edentulism with neuropathy among 436 patients with T2DM (Adjusted OR: 1.7; IC 95%: 1.1-2.6). In a longitudinal study of 529, Gila River Indian adults with type 2 diabetes, Shultis et al (20) observed that incidence of end-stage renal disease in individuals with moderate or severe periodontitis or in those who were edentulous were 2.3, 3.5, and 4.9 times as high respectively compared with those with none/mild periodontitis.

Thorstensson et al (21) more likely to have prevalent proteinuria and cardiovascular complications including stroke, transient ischaemic attacks, angina, myocardial infarction, and intermittent claudication compared to controls at followup. Noma H et al (22) from Japan observed that severity of periodontal disease was significantly correlated with the severity of diabetic retinopathy (p=0.0012). Moreover, the risk of proliferative diabetic retinopathy was significantly higher (2.8 times; p=0.036) in the presence of periodontal disease. Various mechanisms that explain the increased susceptibility to periodontitis in diabetes mellitus are increased MMP, adhesion molecules synthesis, impaired chemotaxis, prolonged inflammation, increased oxidative stress, increased GCF and salivary glucose levels, cytokine dysregulation, impaired bone formation and repair. (23)

To conclude, oro-dental manifestations are common in patients with T2DM, hyposalivation, periodontitis, halitosis, tooth loss, dental caries, burning mouth sensation, taste impairment are common oro-dental manifestations among patients with T2DM. Oro-dental manifestations are more common among T2DM patients with poor glycaemic status. Chronic periodontitis is associated with poor glycaemic control in patients with T2DM.

Chronic periodontitis is associated with diabetic microvascular and macrovascular complications. Further rigorous, systematic studies with larger sample size are required to establish relationship between chronic periodontitis and glycaemic status diabetic complications.

REFERENCES

(1.) http://www.diabetesatlas.org/ Last accessed on 01/01/2016.

(2.) Preshaw PM, Alba AL, Herrera D, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia 2012;55(1):21-31.

(3.) Tabari ZA, Azadmehr A, Nohekhan A, et al. Salivary Visfatin concentrations in patients with chronic periodontitis. Journal of Periodontology 2014;85(8):1081-5.

(4.) World Health Organisation. WHO oral health assessment form for adults (tooth). In: Oral health surveys: basic methods. 2013.

(5.) Silness J, Loe H. Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964;22(1):121-35.

(6.) Greene JC, Vermillion JR. The simplified oral hygiene index. J Am Dent Assoc 1964;68(1):7-13.

(7.) Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol 2007;78(7 Suppl):1387-99.

(8.) Shrimali L, Astekar M, Sowmya GV. Correlation of oral manifestations in controlled and uncontrolled diabetes mellitus. Int J Oral Max Pathol 2011;2(4):24-7.

(9.) Chavez EM, Borrell LN, Taylor GW, et al. A longitudinal analysis of salivary flow in control subjects and older adults with type 2 diabetes. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;91(2):166-73.

(10.) Spielman AI, Bivona P, Rifkin BR. Halitosis. A common oral problem. N Y State Dent J 1996;62(10):36-42.

(11.) Albrecht M, Banoczy J, Tamas G. Dental and oral symptoms of diabetes mellitus. Community Dent Oral Epidemiol 1988;16(6):378-80.

(12.) Gibson J, Lamey PJ, Lewis M, et al. Oral manifestations of previously undiagnosed non-insulin-dependent diabetes mellitus. J Oral Pathol Med 1990;19(6):284-7.

(13.) Sreebny LM, Yu A, Green A, et al. Xerostomia in diabetes mellitus. Diabetes Care 1992;15(7):900-4.

(14.) Bajaj S, Prasad S, Gupta A, et al. Oral manifestations in type 2 diabetes and related complications. Ind J Endo Metab 2012;16(5):777-9.

(15.) Tsai C, Hayes C, Taylor GW Glycaemic control of type 2 diabetes and severe periodontal disease in the US adult population. Community Dent Oral Epidemiol 2002;30(3):182-92.

(16.) Kumar A, Pandey MK, Singh A, et al. Prevalence and severity of periodontal diseases in type 2 diabetes mellitus of Bareilly Region (India). Int J Med Sci Public Health 2013;2(1):77-83.

(17.) Collin HL, Uusitupa M, Niskanen L, et al. Periodontal findings in elderly patients with non-insulin-dependent diabetes mellitus. J Periodontol 1998;69(9):962-6.

(18.) Apoorva SM, Sridhar N, Suchetha A. Prevalence and severity of periodontal disease in type 2 diabetes mellitus (non-insulin-dependent diabetes mellitus) patients in Bangalore City: an epidemiological study. J Indian Soc Periodontol 2013;17(1):25-9.

(19.) Menchaca-Diaz R, Bogarin-Lopez B, Zamudio-Gomez MA, et al. Severe periodontitis, edentulism, and neuropathy in patients with type 2 diabetes mellitus. Gac Med Mex 2012;148(1):34-41.

(20.) Shultis WA, Weil EJ, Looker HC, et al. Effect of periodontitis on overt nephropathy and end-stage renal disease in type 2 diabetes. Diabetes Care 2007;30(2):306-11.

(21.) Thorstensson H, Kuylenstierna J, Hugoson A. Medical status and complications in relation to periodontal disease experience in insulin-dependent diabetics. J Clin Periodontol 1996;23(3 pt 1):194-202.

(22.) Noma H, Sakamoto I, Mochizuki H, et al. Relationship between periodontal disease and diabetic retinopathy. Diabetes Care 2004;27(2):615.

(23.) Andersen PCC, Flyvbjerg A, Buschard K, et al. Relationship between periodontitis and diabetes: lessons from rodent studies. J Periodontol 2007;78(7):1264-75.

Ashish Deshmukh [1], Nilanjan Sengupta [2], Soumik Goswami [3], Prasanta Bandyopadhyay [4], Sananda Saha [5]

[1] Senior Resident, Department of Endocrinology, Nil Ratan Sircar Medical College, Kolkata.

[2] Professor, Department of Endocrinology, Nil Ratan Sircar Medical College, Kolkata.

[3] RMO cum Clinical Tutor, Department of Endocrinology, Nil Ratan Sircar Medical College, Kolkata.

[4] Professor, Department of Periodontics, Dr. R. Ahmed Dental College and Hospital, Kolkata.

[5] Postgraduate Trainee, Department of Periodontics, Dr. R. Ahmed Dental College and Hospital, Kolkata.

Financial or Other, Competing Interest: None.

Submission 25-05-2016, Peer Review 29-07-2016, Acceptance 04-08-2016, Published 01-09-2016.

Corresponding Author:

Dr. Ashish Deshmukh, Senior Resident, Department of Endocrinology, Nil Ratan Sircar Medical College, 138, A.J.C Bose Road Kolkata-700014.

E-mail: drasd2001@gmail.com

DOI: 10.14260/jemds/2016/1161
Table 1: Shows Distribution of Various Clinical Parameters of Oral
Health in Subjects with T2DM (n=100)

Oro-Dental Manifestation    Percentage

Hyposalivation                  58%
Halitosis                       45%
Tooth loss                      36%
Chronic periodontitis           50%
Burning mouth sensation         25%
Dental caries                   24%
Taste impairment                23%
Stomatitis                      18%
Oral candidiasis                8%

Table 2: Showing Relationship Between Anthropometric Parameters,
Metabolic Parameters, in Patients with T2DM with Chronic Periodontitis
and Without Chronic Periodontitis

                          T2DM with CP           T2DM without CP
Parameter                    (n=50)                   (n=50)

Age                   47.27 [+ or -] 9.19      47.22 [+ or -] 7.44
Sex (Female)%                  60                       58
Toothbrush use                 44                       46
  (Once daily)
Duration of T2DM       5.53 [+ or -] 2.93       4.36 [+ or -] 2.58
BMI                   25.92 [+ or -] 2.97      25.58 [+ or -] 3.04
FPG                  133.39 [+ or -] 26.46      119 [+ or -] 22.55
PPPG                  212.18 [+ or -] 56.5    182.60 [+ or -] 35.13
HbA1C                  7.98 [+ or -] 0.96       7.16 [+ or -] 0.53
Total cholesterol    186.24 [+ or -] 33.53    184.84 [+ or -] 36.56
Triglycerides        159.27 [+ or -] 60.09    151.46 [+ or -] 62.85
HDL cholesterol       43.69 [+ or -] 8.39      43.78 [+ or -] 7.73
LDL cholesterol      108.31 [+ or -] 27.87     109.12 [+ or -] 31.1
eGFR                  81.43 [+ or -] 28.48     89.50 [+ or -] 21.69
Neuropathy %                   52                       30
DKD %                          36                       16
Retinopathy %                  38                       20
CVD %                          32                       10
Number of teeth       29.48 [+ or -] 2.88      31.56 [+ or -] 1.16
Plaque Index           2.47 [+ or -] 0.61       2.40 [+ or -] 0.70
OHI-S                  4.76 [+ or -] 1.06       4.58 [+ or -] 0.99
CAL                    4.92 [+ or -] 1.13       1.22 [+ or -] 0.60
PPD                    4.20 [+ or -] 1.55       0.32 [+ or -] 0.47
Sites with BOP        40.51 [+ or -] 19.40              0

Parameter            P value

Age                    0.89
Sex (Female)%          0.77
Toothbrush use         0.74
  (Once daily)
Duration of T2DM       0.03
BMI                    0.57
FPG                   0.004
PPPG                  0.002
HbA1C                 0.001
Total cholesterol      0.84
Triglycerides          0.52
HDL cholesterol        0.76
LDL cholesterol        0.89
eGFR                   0.11
Neuropathy %           0.04
DKD %                  0.03
Retinopathy %          0.04
CVD %                 0.012
Number of teeth       0.004
Plaque Index           0.59
OHI-S                  0.40
CAL                   <0.001
PPD                   <0.001
Sites with BOP        <0.001

Fig. 1: Distribution of Various Clinical Parameters of Oral
Health in Subjects with T2DM (percentage) in Uncontrolled
and Well-Controlled Glycaemic Status

                              Uncontrolled     Well controlled
                              Glycemic state   glycemic state
                              (HbA1C >7%)       (MbA1C <7%)
Hyposalivation                     70               10
Burning mouth sensations #         28               15
Halitosis                          52               15
Stomatitis #                       19               15
Chronic periodontitis              57               20
Tooth loss                         43               10
Dental caries                      29                5
Oral candidiasis                   10                0
Taste impairment                   28                5

Note: Table made from bar graph.
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Title Annotation:Original Research Article
Author:Deshmukh, Ashish; Sengupta, Nilanjan; Goswami, Soumik; Bandyopadhyay, Prasanta; Saha, Sananda
Publication:Journal of Evolution of Medical and Dental Sciences
Article Type:Report
Date:Sep 1, 2016
Words:3063
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