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Table of Contents   
ORIGINAL RESEARCH  
Year : 2012  |  Volume : 23  |  Issue : 3  |  Page : 368-372
Comparison of glycosylated hemoglobin levels in periodontitis patients and healthy controls: A pilot study in Indian population


Department of Periodontics, JSS Dental College and Hospital, A Constituent College of JSS University, Mysore, India

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Date of Submission18-Nov-2011
Date of Decision28-Aug-2011
Date of Acceptance14-Nov-2011
Date of Web Publication11-Oct-2012
 

   Abstract 

Background: Periodontitis is associated with glycemic control in patients with diabetes. The purpose of this study was to determine if glycosylated hemoglobin is elevated in patients with periodontitis who are non-diabetic adults.
Materials and Methods: A total of 36 patients were selected and were divided into test and control groups. Test group included 18 adults without diabetes, but with periodontitis (having at least five teeth with probing depth (PD) ≥5 mm, bleeding on probing (BOP), and clinical attachment loss (>1 mm) on >5 teeth or radiographic bone loss), and the control group included 18 healthy adults (PDs ≤4 mm and BOP ≤15% and no clinical attachment loss). Glycosylated hemoglobin (HbA1c) was assessed in laboratory for these patients. Groups were compared using the t test,kruskal-wallis test, pearsson correlation.
Results: Both the groups showed similar HbA1c levels, but there was a marginal increase in levels in the test group (cases), which was not statistically significant (cases- 6.06%, controls-5.8%; P=0.101).There was no significant difference found in the mean HbA1c levels among males and females and among various age groups. Mean BMI among the cases and controls was found to be similar. When inter and intra group comparisons were done according to BMI categories among the cases and controls, we found similar mean HbA1c values.
Conclusion: Indians are at a high risk of developing periodontitis and diabetes. These data suggest a possible link between periodontitis and glycemic control in non-diabetic individuals. Periodontal disease may be a potential contributor to development of type 2 diabetes.

Keywords: Glycosylated hemoglobin, non-diabetics, periodontitis

How to cite this article:
Saxena RM, Deepika P C. Comparison of glycosylated hemoglobin levels in periodontitis patients and healthy controls: A pilot study in Indian population. Indian J Dent Res 2012;23:368-72

How to cite this URL:
Saxena RM, Deepika P C. Comparison of glycosylated hemoglobin levels in periodontitis patients and healthy controls: A pilot study in Indian population. Indian J Dent Res [serial online] 2012 [cited 2020 Jul 3];23:368-72. Available from: http://www.ijdr.in/text.asp?2012/23/3/368/102231
India is home to around 40 million diabetics, and this number is thought to give India the dubious distinction of being home to the largest number of diabetics in any one country. The crude prevalence rate of diabetes in urban areas is about 9% and that the prevalence in rural areas has also increased to around 3% of the total population.Surveys have also shown that the prevalence of Impaired Glucose Tolerance (IGT) is also high. Given the observation that around 35% of those with IGT will develop full blown diabetes within 5 years, the sheer numbers of those with diabetes seems overwhelming. [1]

Periodontal disease has been called diabetes' sixth complication, along with retinopathy, nephropathy, neuropathy, macrovascular disease, and an altered wound healing. Periodontitis also seems to be a risk factor for incident diabetes. [2]

A popular theory is that, inflammatory mediators (particularly interleukin-6 and tumor necrosis factor-alpha) generated within the inflamed periodontal tissues or in response to oral bacteria that translocate into the systemic circulation, interfere with the actions of insulin receptors, thereby decreasing insulin sensitivity. [3]

Glucose can bind irreversibly to hemoglobin through a non-enzymatic reaction to form glycosylated hemoglobin (HbA). HemoglobinA1c, or HbA1c, is the major subfraction of HbA. Because it is based on the average life span of an erythrocyte, HbA1c levels reflect glycemic control over the previous 1 to 3 months. [3]

Although many studies reported more severe periodontal disease in subjects with diabetes than those without diabetes, few examined the association between periodontitis and glycemia or the level of glycosylated hemoglobin in adults without diabetes. The purpose of the current study was to examine the association between the periodontitis and glycosylated hemoglobin in non-diabetic adults. This study may provide additional rationale for screening the patients with periodontitis for signs and symptoms of abnormal glucose metabolism.


   Materials and Methods Top


Periodontitis cases and healthy controls were selected over a period of 2 months from the Department of Periodontology of our institution.36 patients selected were aged between ≥35 and ≤65 years, had not been diagnosed with diabetes, had more than 10 natural teeth and had no history of long-term antibiotic use (>14 days) in the past 6 months. Patients who were smokers, pregnant, had recent significant blood loss, or had hemolyticanemia, were excluded. Further selection was based on the clinical examinations and radiographs. The test group included 18 patients with periodontitis, and were defined as those having ≥5 Teeth with probing depth (PD) ≥5 mm, and clinical attachment loss (>1 mm) on > 5teeth or radiographic bone loss and bleeding on probing. Control group included 18 healthy adults with probing depth of ≤4 mm, BOP at ≤15% of tooth sites, no clinical attachment loss, and no periodontal treatment (scaling and root planing or surgery) undertaken within the previous 6 months.

Ethics approval was gained from the ethical committee of our institution before implementation of the study, while written informed consent was obtained from all the participants at the beginning of this study.

Brief medical history was taken for these patients. The body mass index (BMI) was determined by Queletexformula, which was estimated by dividing the body weight (in kilograms) by the square of the height (in meters). Clinical parameters were assessed in each patient, which included bleeding on probing (BOP) measured at 4 sites (mesiofacial, midfacial, distofacial, lingual/palatal) per tooth, pocket probing depth, clinical attachment loss. Clinical assessment was done by using William's periodontal probe. After the clinical assessment, patients were sent to laboratory for getting their glycosylated hemoglobin levels tested, where 2 ml of blood was withdrawn for the same.

Statistical analysis was done using t test, kruskal-wallis test, pearsson correlation. Participant ages, gender, body mass index (BMI, kg/m 2 ) were included in analysis. All analysiswere performed using a statistical software program SPSS (version 16).


   Results Top


Both the groups showed similar HbA1c levels, but there was a marginal increase in levels in the test group, which was not statistically significant (test group- 6.06%, controls-5.8%; P=0.101) [Figure 1]. On comparing HbA1c levels among males and females in cases (6.28% v/s 5.83%) and controls (5.83% v/s 5.75%) separately, levels were almost similar, and the results were not significant. There was no significant difference found in the mean HbA1c levels among the various age groups (35-39, 40-45, 46-50, 51-55, 55+ yrs).
Figure 1: Graph comparing mean glycosylated haemoglobin levels among cases and controls

Click here to view


In this study, patients fell under the following BMI categories (according to WHO classification):

  1. Normal-18.5-24.99 kg/m 2
  2. Overweight-
    1. Pre-obese- 25-29.99 kg/m 2
    2. Obese->30 kg/m 2
When intra and intergroup comparisons were done among the various BMI categories, following results were obtained:

  1. On comparing mean BMI among test group and controls (22.7 kg/m 2 v/s 23.57 kg/m 2 ), t- test showed no significant difference. [Figure 2]
    Figure 2: Graph comparing mean BMI among cases and controls

    Click here to view
  2. When mean BMI was compared among males and females (22.7 kg/m 2 v/s 23.58 kg/m 2 ), t- test showed,there was no significant difference.
  3. HbA1c levels in cases, which had normal BMI and overweight persons, were found to be similar (6.08% v/s 5.7%). [Figure 3]
    Figure 3: BMI- Intragroup comparison-Graph showing mean glycosylated haemoglobin (HbA1c) levels among cases with normal BMI and overweight persons

    Click here to view
  4. HbA1c levels in controls, who had normal BMI and overweight persons (pre- obese, obese class I), calculated by kruskal-wallis test, were found to be similar (normal-5.76% v/s pre-obese- 5.9%, obese- 5.8%). [Figure 4]
    Figure 4: BMI- Intragroup comparison-Graph showing mean glycosylated haemoglobin (HbA1c) levels among controls with normal BMI and overweight persons

    Click here to view
  5. HbA1c levels in persons with normal BMI showed similar results among cases and controls when calculated by t-test (6.08% v/s 5.78%). [Figure 5]
    Figure 5: BMI- Intergroup comparison- Graph showing mean glycosylated haemoglobin (HbA1c) levels in persons with normal BMI among cases and controls

    Click here to view
  6. HbA1c levels in persons who were overweight, showed similar results among cases and controls (5.7% v/s 5.87%). [Figure 6]
    Figure 6: BMI- Intergroup comparison-Graph showing mean glycosylated haemoglobin (HbA1c) levels in overweight persons among cases and controls

    Click here to view
  7. There was a significant correlation reported between HbA1c levels and number of sites with clinical attachment loss >3mm (P= 0.036).

   Discussion Top


Diabetes mellitus is one of the highly prevalent disorders, constituting a huge global public health burden. It is predicted that approximately 300 million people will have diabetes by 2025 worldwide. [4] Most of this growth, driven principally by increasing prevalence of type 2 diabetes mellitus, is occurring in developing countries. Periodontitis is the most common chronic oral infection and major cause of tooth loss in adults, and has been considered as the sixth complication of diabetes mellitus. Conversely, periodontitis is also shown to be a risk factor for poor glycemic control in patients with diabetes due to bacteria and their by-products in the inflamed periodontal tissue, constituting a chronic source of systemic challenge to the host. [5]

In this study, HbA1c levels were slightly higher in periodontitis casesv/shealthy controls, though it was not statistically significant (cases- 6.0611 ± 0.0645, controls- 5.7944 ± 0.1830; P=0.101). Glycosylated hemoglobinlevels according to American Diabetes:

Association guidelines [6] indicate the following:

4%- 6% Normalbr><7% Good diabetes control
7%- 8% Moderate diabetes control
>8% Action suggested to improve diabetes control

In the German study, by Demmer et al, [7] HbA1c values were compared between participants in the upper and lower quintiles in terms of the extent of advanced attachment loss. They studied >7,000 adults without diabetes in the National Health and Nutrition Examination Survey I (1971 to 1976), who were re-examined at least once 6 to 21 years later. Individuals in the upper quintile, in terms of periodontitis, developed diabetes at about twice the rate as the periodontally healthy controls. Our results also are consistent with other reports, which collectively suggest that the periodontitis is associated with the elevated blood glucose levels in adults who have not been diagnosed with diabetes. For example, Nibali et al[8] , compared non-fasting blood glucose levels between periodontally healthy patients and those with advanced disease. Glucose, as well as high-density and low-density lipid cholesterol levels, was significantly higher in periodontitis cases than the controls. Saito et al[9] found that, alveolar bone loss was associated with an impaired glucose tolerance in Japanese men without diabetes.In a study done by Ryan et al[3] , adjusted HbA1c levels were slightly, but statistically significantly higher in periodontitis cases v/s healthy controls.Ryan et al[3] did not find an evidence of a dose-dependent relationship between the disease extent and HbA1c elevations. They suggest that, there may be a threshold, above which the periodontitis affects the HbA1c values in the general population, and this finding needs to be confirmed in larger studies.

We found a positive correlation between HbA1c and number of sites with clinical attachment loss >3 mm, though the association between HbA1c with extent of periodontal pocketing was not significant. In contrast, Ryan et al[3] found a small, but negative correlation between HbA1c and the number of sites with pocket depth ≥5mm.

The present case control study shows a positive correlation between the periodontitis and HbA1c values. In this study, all cases fell under the moderate periodontitis group.If we had taken only severe periodontitis cases, we would have probably found a higher level of HbA1c in test group.

Two patients in the test group had HbA1c levels >7%, but they fulfilled all the inclusion criteria and had no previous diabetes diagnosis or cardinal symptoms of the disease, hence were included in the study.

In this study, participants were matched according to age, and all subjects were from middle or lower socioeconomic strata. Patients in present study fell under the following BMI categories: normal, pre-obese, obese. When inter and intra group comparisonswere done according to BMI categories among the cases and controls, we found similar HbA1c values.

The worsening of glycemic control associated with severe periodontitis is because of persistent systemic challenge with periodontopathic bacteria and their products. This increases the tissue resistance to insulin, preventing glucose from entering target cells and causes elevated blood glucose levels. [10]

In the present study, HbA1c was measured using a laboratory test (Bio Red D-10 analyzer). All samples were sent to the same laboratory.

Even though diabetes diagnosis is based on repeated casual, fasting and postprandial blood glucose assessments, HbA1c is a commonly used treatment endpoint in clinical trials in diabetology, and evidence suggests that, it may be used as a stand-alone diagnostic measure for diabetes in the future. [3]


   Conclusion Top


The current study was inconclusive probably because of smaller sample size, and patients falling only under the moderate periodontitis category. A larger sample with severe periodontitis cases may show a positive result. A contributory role of periodontal disease in the development of type 2 diabetes is potentially of public health importance because of the prevalence of treatable periodontal disease in the population and the pervasiveness of diabetes-associated morbidity and mortality.

 
   References Top

1.The Indian Task Force On Diabetes Care In India:available from: http://www.diabetesindia.com/diabetes/itfdci.htm [Last accessed on 2010 Nov 03].  Back to cited text no. 1
    
2.Loe H. Periodontal Disease. The sixth complication of diabetes mellitus. Diabetes care 1993;16:329-34.  Back to cited text no. 2
    
3.Wolff RE, Wolff LF, Michalowicz BS.A Pilot Study of Glycosylated Hemoglobin Levels in Periodontitis Cases and Healthy Controls. J Periodontol 2009;80:1057-61.  Back to cited text no. 3
[PUBMED]    
4.Green A, Christian Hirsch N, Pramming SK. The changing world demography of type 2 diabetes. Diabetes Metab Res Rev 2003;19:3-7.  Back to cited text no. 4
[PUBMED]    
5.Chen L, Wei B, Li J. Association of periodontal parameters with metabolic level, systemic inflammatory markers in type 2 diabetes patients. J Periodontol 2010;81:364-71.  Back to cited text no. 5
    
6.Nathan DM, Buse JB, Davidson MB, Ferrannini E, Holman RR, Sherwin R,et al. Medical management of hyperglycaemia in type 2 diabetes mellitus: A consensus algorithm for the initiation and adjustment of therapy: A consensus statement from the American Diabetes Association and the European Association for the Study of Diabetes. Diabetologia 2009;52:17-30.  Back to cited text no. 6
[PUBMED]    
7.Demmer RT, Jacobs DR Jr, Desvarieux M. Periodontal disease and incident type 2 diabetes: Results from the First National Health and Nutrition Examination Survey and its epidemiologic follow-up study. Diabetes Care 2008;31:1373-79.  Back to cited text no. 7
[PUBMED]    
8.Nibali L, D'Aiuto F, Griffiths G, Patel K. Severe periodontitis is associated with systemic inflammation and a dysmetabolic status: A case- control study. J ClinPeriodontol 2007;34:931-7.  Back to cited text no. 8
    
9.Saito T, Murakami M, Shimazaki Y,Matsumoto S, Yamashita Y. The extent of alveolar bone loss is associated with impaired glucose tolerance in Japanese men. J Periodontol 2006;77:392-7.  Back to cited text no. 9
[PUBMED]    
10.Mealey BL, Klokkevold PR. Periodontal Medicine: Impact of Periodontal Infection on Systemic Health In: Newman MG, Takei HH, Klokkevold PR, Carranza FA, editors: Clinical Periodontology, 10 th ed. St Louis, Elsevier;2006. p.322.  Back to cited text no. 10
    

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Correspondence Address:
Ruchika M Saxena
Department of Periodontics, JSS Dental College and Hospital, A Constituent College of JSS University, Mysore
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0970-9290.102231

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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]

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