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ORIGINAL ARTICLE
Year : 2010  |  Volume : 14  |  Issue : 4  |  Page : 217-221  

Evaluation of tumor necrosis factor-α (TNF-α) levels in plasma and their correlation with periodontal status in obese and non-obese subjects


Department of Periodontology, Bharati Vidyapeeth Dental College and Hospital, Pune, India

Date of Submission15-Sep-2009
Date of Acceptance09-Aug-2010
Date of Web Publication19-Feb-2011

Correspondence Address:
Suruchi Khanna
28, Florida Estate, Keshavnagar, Mundhawa, Pune - 411 036
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-124X.76920

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   Abstract 

Background: Obesity is emerging as a significant health problem worldwide and is a risk factor for various systemic diseases. Periodontal disease is a multifactorial inflammatory disease. Recent evidence points to a link between obesity and periodontal disease, and a role for tumor necrosis factor-a (TNF-a) has been suggested. Materials and Method: Forty nondiabetic subjects were divided into two groups: group A (non-obese) included subjects with body mass index (BMI) of 18.5 to 27 kg/m2, and group B (obese) included subjects with BMI>27 kg/m2. The BMI, TNF-α levels in plasma and Periodontal Disease Index (PDI) scores were assessed, compared and correlated. Results: Significantly higher PDI scores and TNF-α levels were found in the obese group as compared to those in the non-obese group. Also, a significant and positive correlation was seen between BMI and TNF-α, TNF-α and PDI as well as BMI and PDI. Conclusion: Increase in the levels of tumor necrosis factor-a in plasma and an increase in the severity of periodontal disease may be seen in subjects with a higher body mass index (BMI). This indicates that obesity may be detrimental to the periodontal health of individuals.

Keywords: Obesity, tumor necrosis factor, TNF-α


How to cite this article:
Khanna S, Mali AM. Evaluation of tumor necrosis factor-α (TNF-α) levels in plasma and their correlation with periodontal status in obese and non-obese subjects. J Indian Soc Periodontol 2010;14:217-21

How to cite this URL:
Khanna S, Mali AM. Evaluation of tumor necrosis factor-α (TNF-α) levels in plasma and their correlation with periodontal status in obese and non-obese subjects. J Indian Soc Periodontol [serial online] 2010 [cited 2019 Jul 21];14:217-21. Available from: http://www.jisponline.com/text.asp?2010/14/4/217/76920


   Introduction Top


Periodontitis is a multifactorial disease with microbial dental plaque as the initiator of periodontal disease. However, the manifestation and progression of periodontal disease are influenced by a wide variety of determinants and factors.

Obesity is rapidly becoming a serious problem in both developed and developing countries. Overweight and obesity are risk factors for various diseases, including type 2 diabetes, hyperlipidemia, hypertension, cholelithiasis, arteriosclerosis, and cardiovascular and cerebrovascular diseases.

It is now clear that adipose tissue is complex and metabolically active. It secretes numerous immunomodulatory factors and plays a major role in regulating metabolic and vascular biology. Adipose cells secrete more than 50 bioactive molecules, known collectively as adipokines - which include tumor necrosis factor-a, which may enhance periodontal degradation. [1]

Obesity was noted to contribute to the severity of periodontal disease in rats a few decades ago. Several recent studies have now suggested a relationship between periodontal disease and obesity. [2] It is possible that increase in body fat increases the likelihood of an active host inflammatory response in periodontal disease.

The link between obesity and periodontal disease may not be completely understood, but it is clear that once established, this relationship will prove to be of extreme public health relevance. It may go a long way in planning and modifying preventive and treatment modalities for periodontal disease. Hence this study was planned to evaluate the relationship between obesity, tumor necrosis factor-a and periodontal disease.


   Materials and Methods Top


A total of 40 subjects were selected after calculation of their body mass index and assessment of their fasting blood glucose levels, from the outpatient department in the postgraduate clinic of Department of Periodontology, Bharati Vidyapeeth University Dental College and Hospital, Pune.

Inclusion criteria were age ranging from 20 to 55 years, random selection of male and female subjects, 20 subjects with BMI> 27 kg/m 2 , 20 subjects with BMI ranging from 18.5 to 27 kg/m 2 and at least 6 natural teeth present.

Exclusion criteria included subjects on medication known to affect periodontal conditions or anti-inflammatory drugs; those with history of systemic disease, e.g., hypertension, cardiovascular disease, arthritis etc.; pregnant, lactating females; those with overt hormonal disturbances; smokers; and diagnosed diabetics or subjects with fasting glucose levels exceeding 126 mg/dL as assessed by glucose oxidase-peroxidase method.

All potential participants were explained the need and design of the study. Only subjects who consented for the study were included.

As part of the clinical examination, height was recorded in centimeters up to the nearest 0.00 cm on a stadiometer, and weight was recorded in kilograms up to the nearest 0.00 kg using electronic scales. [3] The body mass index (BMI) of the subjects was calculated as weight in kilograms divided by the height in meters squared. Based on the BMI, the subjects were divided into two groups: group A (non-obese) with subjects with BMI ranging from 18.5 to 27 kg/m 2 and group B (obese) with subjects with BMIth > 27 kg/m 2 . Scores on Simplified Oral Hygiene Index (Greene and Vermillion, 1964) [4] and Periodontal Disease Index (Ramfjord, 1959) [5] were recorded as part of clinical examination.

A venous blood sample was collected from the subjects by venepuncture from the anterior cubital vein using a sterile syringe and needle, at the Pathology Laboratory at Bharati Hospital. The blood sample was collected after overnight fasting. Two milliliters of the blood sample was used to estimate the blood glucose level at the laboratory, and 5 mL of the blood sample was transferred to vials containing anticoagulant and then transferred immediately to the laboratory at Interactive Research School of Health Affairs (IRSHA). Three milliliters of Histopaque-1077 (SIGMA Diagnostics) at room temperature was pipetted into glass centrifuge tubes, and 5 mL of the blood sample was then added by 'layering.' The sample was centrifuged at 3000 rpm using Remi R8C laboratory centrifuge to separate plasma. The top plasma layer was then pipetted into storage vials and stored at a temperature of −80ºC. The stored plasma was used for estimation of tumor necrosis factor-a levels at a later date using an enzyme immunoassay for the in vitro determination of tumor necrosis factor-α in plasma, serum or culture supernatant. The assay was carried out as per manufacturer's directions for use (Immunotech IM1121 kit). Statistical analysis of results was carried out. Descriptive statistics included mean and standard deviation, which were calculated for each of the test groups . The inter-group comparison of BMI, TNF-α levels and PDI scores between obese and non-obese groups was done using unpaired t test. P value<.05 was considered statistically significant. The correlation between BMI and TNF-α levels; TNF-α levels and PDI scores; and BMI and PDI scores was analyzed using Pearson's correlation coefficient. This was done separately for all cases together, as well as for obese and non-obese groups. Partial correlation coefficients were calculated, keeping the Simplified Oral Hygiene Index (OHI-S) scores controlled in obese and non-obese groups.


   Results Top


The mean body mass index (BMI) in the obese group was 35.20±5.10 kg/m 2 , while the mean BMI in the non-obese group was 22.91±1.74 kg/m 2 . The estimated levels of tumor necrosis factor-a (TNF-α) in plasma of obese subjects was 4.94±0.56 pg/mL, and the estimated levels of (TNF-α) in plasma of non-obese subjects was 4.27±0.41 pg/ml [Figure 1]. A statistically significant difference between the two groups was observed using the t test, with higher BMI and higher (TNF-α) levels in the obese group (P=.000) [Figure 1].
Figure 1: Comparison between mean TNF-á levels

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The periodontal status was assessed using the Periodontal Disease Index (PDI). The mean PDI score in the obese group was 4.64±1.13, whereas the mean PDI score in the non-obese group was 1.32±0.75. The t test showed that there was a statistically significant difference in the PDI score between the obese and non-obese groups (P=.000). The results indicated that periodontal disease was more severe in the obese subjects as compared to the non-obese subjects [Figure 2].
Figure 2: Comparison between mean PDI scores

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Body mass index was correlated to (TNF-α) levels in plasma using Pearson's correlation coefficient. When all the subjects (obese and non-obese) were considered together, the Pearson's correlation coefficient was 0.830 (P=.000). When only the obese group was considered, the Pearson's correlation coefficient was 0.902 (P=.000); and when only the non-obese group was considered, the Pearson's correlation coefficient was 0.573 (P=.008). Coefficients of correlation between BMI and TNF-α levels were statistically highly significant and also high, consistent and positive [Figure 3] and [Figure 4].
Figure 3: Correlation between BMI and TNF-α among the subjects of the obese group

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Figure 4: Correlation between BMI and TNF-α among subjects of thenon-obese group

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The TNF-α levels in plasma were also correlated with the PDI scores. When all the subjects (obese and non-obese) were considered together, the Pearson's correlation coefficient was 0.733 (P=.000). When only the obese group was considered, the Pearson's correlation coefficient was 0.609 (P=.004); and when only the non-obese group was considered, the Pearson's correlation coefficient was (P=.019). Coefficients of correlation between TNF-α levels and PDI scores were statistically highly significant and also high, consistent and positive [Figure 5] and [Figure 6].
Figure 5: Correlation between TNF-α and PDI among the subjects of the obese group

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Figure 6: Correlation between TNF-α and PDI among the subjects of the non-obese group

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Analysis of the relationship between BMI and PDI scores revealed that when all the subjects (obese and non-obese) were considered together, the Pearson's correlation coefficient was 0.887 (P=.000). When only the obese group was considered, the Pearson's correlation coefficient was 0.632 (P=.003); and when only the non-obese group was considered, the Pearson's correlation coefficient was 0.322 (P=.166). Coefficients of correlation between BMI and PDI scores were statistically highly significant and also high, consistent and positive when all subjects were considered together and also when only obese group was considered. This may suggest that PDI score increases with the increase in BMI in obese individuals. However, when only non-obese group was considered, a weak positive correlation was seen, but it was not statistically significant [Figure 7] and [Figure 8].
Figure 7: Correlation between BMI and PDI among the subjects of the obese group

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Figure 8: Correlation between BMI and PDI among the subjects of the non-obese group

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In order to eliminate the effects of oral hygiene on the periodontal status in the studied subjects, the oral hygiene status was evaluated in each group and partial correlation coefficients were calculated keeping the oral hygiene status controlled. The results showed that the oral hygiene status of subjects in both groups (obese and non-obese) was similar. The mean OHI-S score of subjects in the obese group was 1.68±0.71, and the mean OHI-S score of subjects in the non-obese group was 1.64±0.63.

The t test showed a P value of .872, indicating that there was no statistically significant difference in the OHI-S score between the obese and non-obese groups [Figure 9].
Figure 9: Comparison between mean OHI-S scores

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Partial correlation coefficients were calculated keeping OHI-S controlled. The correlations between BMI and TNF-α; TNF-α and PDI; as well as BMI and PDI were found to be significant and positive in the obese group. However, in the non-obese group, a weak positive correlation was seen between BMI and PDI, but this was not statistically significant. These are summarized in [Table 1].
Table 1: Correlation between BMI and TNF-á; TNF-á and PDI; BMI and PDI; with OHI-S controlled


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   Discussion Top


Obesity is well known to be a risk factor for various diseases. It is also known to increase mortality from various health disorders. Adipose tissue has also been shown to secrete TNF-α, which causes liver injury in obese rodents. Moreover, TNF-α from adipose tissue has been reported to be directly associated with insulin resistance. [6] Elevated levels of serum TNF-α have been reported in obese nondiabetic individuals, which declined following weight loss. [3]

Increasingly, evidence of a relationship of newly identified risk factors for systemic diseases to periodontal disease is starting to emerge. [2] In this light, recent studies indicate that obesity is emerging as a risk indicator for periodontal disease. [3],[6],[7],[8] In a recent study, the relationship between obesity, TNF-α and periodontal disease has been evaluated, and a model linking inflammation to obesity, diabetes and periodontal infections has been proposed. [3]

In view of the above, the present study was planned to estimate the levels of tumor necrosis factor-a in serum of obese and non-obese subjects and correlate these to the periodontal status of the subjects.

The results of our study show significantly higher BMI and TNF-α levels in obese subjects. This is in agreement with the study by Genco et al. (2005). [3] They found a highly significant elevation of TNF-α as well as soluble TNF receptor levels in plasma of subjects with BMI>30.8 kg/m 2 as compared to those with BMI<24.6 kg/m 2 .

We found significantly higher scores of PDI in obese subjects. The results of our study are similar to those of a cross-sectional study by Saito, Shimazaki, Kogo, Tsuzuki and Ohshima (2001). [6] Similar results were obtained by Mohammad Al Zahrani, Nabeel Bissada and Elaine Borawaski (2003), [9] who examined the relationship between body weight and periodontal disease. In this study, however, obese group was defined by BMI≥30 kg/m 2 ; while in our study, the obese group was defined by BMI≥27 kg/m 2 . When they stratified the data by age, the estimate of the association between prevalence of periodontal disease in young adults and obesity was slightly attenuated (from 1.85 to 1.76) by adjusting for all the covariates but remained significant (P<.01). In our study, no such stratification of data was done.

The results of our study were contrary to those of the study by Torrungruang et al. (2005), [10] in which they studied risk indicators for periodontal disease in older Thai adults. The degree of association between severity of periodontitis and various independent variables was investigated using multinomial logistic regression analysis. They found that body mass index and waist circumference had no significant effect on periodontal disease severity in the multivariate model. The differences in results may be due to the fact that in our study the subjects belonged to a younger age group (20-55 years), while their study involved older subjects (60-73 years). In the study by Mohammad Al Zahrani, Nabeel Bissada and Elaine Borawaski (2003) [9] also, a significant association between the measures of body fat and periodontal disease was found among the younger adults but not among the middle-aged or older adults.

We found the coefficients of correlation between BMI and TNF-α were statistically highly significant and also high, consistent and positive. This suggests that higher concentrations of TNF-α were seen in plasma of subjects with higher BMI. Although correlation between BMI and TNF-α levels in plasma was not reported in the study by Genco et al. (2005), [3] they did find a highly significant elevation of TNF-α in plasma of subjects with BMI>30.8 kg/m 2 as compared to those with BMI<24.6 kg/m 2 . This is similar to our study.

Genco et al. found a modest but statistically significant positive correlation of sTNF-α RI and sTNF-α RII levels with severity of periodontal disease among those in the quartile with the lowest BMI. This was explained by the authors by a possible masking effect. They suggested that the effect of periodontal infection in increasing soluble receptors of TNF-α is masked by the effect of the elevation of TNF-α and its receptors associated with obesity. Only when the effect of BMI is minimal, does one see increased soluble receptor levels in plasma associated with periodontal disease. In our study, however, not only was an increase in TNF-α levels seen with increase in Periodontal Disease Index, it was also highly significant.

The correlation between BMI and PDI seen in our study suggests that more severe periodontal disease is seen with higher BMI. Saito et al. (1998) also showed dose response between obesity and periodontitis. [7] Wood, Johnson, Streckfus (2003) [11] also found statistically significant correlations between periodontitis and waist-hip ratio (WHR), body mass index (BMI), fat-free mass (FFM) and, in some instances, skin-fold thickness (S), respectively.

In order to eliminate the effects of oral hygiene on the periodontal status in the studied subjects, the oral hygiene status was evaluated in each group and partial correlation coefficients were calculated keeping the oral hygiene status controlled. This indicates that there was an increase in TNF-α levels in plasma, and in periodontal disease severity in the obese subjects as compared to non-obese subjects. The results also suggest that this increase in severity may be a consequence of their obese status and not due to the effects of microbial plaque alone.

In conclusion, our study indicates that obesity may be detrimental to the periodontal health of individuals. There may be a need to assess obesity as part of the systemic evaluation of individuals seeking periodontal care, and prevention and control of obesity may become instrumental in providing complete periodontal care to individuals.

To elucidate the relationship between obesity and periodontal disease, further studies with a larger sample of subjects, using additional parameters of fat analysis other than BMI alone and adjusting for multiple confounding factors by the use of multiple regression models are needed. The primary constraint on our study was the cost factor, due to which we were unable to include the above-mentioned parameters. There is also scope to assess the role of many other adipokines in an effort to better understand the underlying link between obesity and periodontal disease.

 
   References Top

1.Ritchie CS. Obesity and periodontal disease. Periodontology 2000 2007;44:154-63.  Back to cited text no. 1
    
2.Nunn ME. Understanding the etiology of periodontitis: An overview of periodontal risk factors. Periodontology 2000 2003;32:11-23.  Back to cited text no. 2
    
3.Genco RJ, Grossi SG, Alex Ho, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes and periodontal infections. J periodontol 2005;76:2075-84.  Back to cited text no. 3
    
4.Greene JC, Vermillion JR. The simplified oral hygiene index. J Am Dent Assoc 1964;68:7-10.  Back to cited text no. 4
    
5.Ramjford SP. The periodontal disease index. J Periodontol 1967;38:602-8.  Back to cited text no. 5
    
6.Saito T, Shimazaki Y, Koga T, Tsuzuki M, Ohshima A. Relationship between upper body obesity and periodontitis. J Dent Res 2001;80:1631-6.  Back to cited text no. 6
    
7.Saito T, Shimazaki Y, Sakamoto M. Obesity and periodontitis. N Engl J Med 1998;339:482-3.  Back to cited text no. 7
    
8.Nishida N, Tanaka M, Hayashi N, Nagata H, Takeshita T, Nakayama K, et al. Determination of smoking and obesity as periodontitis risks using the classification and regression tree method. J Periodontol 2005;76:923-8.  Back to cited text no. 8
    
9.Al-Zahrani MS, Bissada NF, Borawskit EA. Obesity and periodontal disease in young, middle-aged, and older adults. J Periodontol 2003;74:610-5.  Back to cited text no. 9
    
10.Torrungruang K, Tamsailom S, Rojanasomsith K, Sutdhibhisal S, Nisapakultorn K, Vanichjakvong O, et al. Risk indicators of periodontal disease in older Thai adults. J Periodontol 2005;76:558-65.  Back to cited text no. 10
    
11.Wood N, Johnson RB, Streckfus CF. Comparison of body composition and periodontal disease using nutritional assessment techniques: Third National Health and Nutrition Examination Survey (NHANES III). J Clin Periodontol 2003;30:321-7.  Back to cited text no. 11
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]
 
 
    Tables

  [Table 1]


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