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Table of Contents   
ORIGINAL RESEARCH  
Year : 2011  |  Volume : 22  |  Issue : 2  |  Page : 260-265
Detection of odoriferous subgingival and tongue microbiota in diabetic and nondiabetic patients with oral malodor using polymerase chain reaction


1 Department of Periodontics, College of Dental Sciences, Davangere, Karnataka, India
2 Department of Periodontics, Pacific Dental College, Udaipur, India

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Date of Submission22-Jun-2009
Date of Decision11-Aug-2010
Date of Acceptance10-Nov-2010
Date of Web Publication27-Aug-2011
 

   Abstract 

Background: Halitosis has been correlated with the concentration of volatile sulfur compounds (VSCs) produced in the oral cavity by metabolic activity of bacteria colonizing the periodontal pockets and the dorsum of the tongue. It has been assumed that there is a relationship between periodontal disease and diabetes mellitus.
Objectives: The aim of the study was to assess the malodor using the organoleptic method and tanita device; to quantify odoriferous microorganisms of subgingival plaque and tongue coating, such as P. gingivalis (Pg), T. forsythia (Tf), and F. nucleatum (Fn) using polymerase chain reaction (PCR) in nondiabetic and diabetic chronic periodontitis patients.
Patients and Methods: Thirty chronic periodontitis patients (with and without diabetes) with 5-7 mm pocket depth, radiographic evidence of bone loss, and presence of oral malodor participated in this study. Subjective assessment of mouth air was done organoleptically and by using a portable sulfide monitor. Tongue coating was also assessed.
Results: The scores of plaque index, gingival index, gingival bleeding index, VSC levels, and tongue coating between the nondiabetic and diabetic patients were not significant (P>0.5). In nondiabetic patients, Fn was found to be significantly (P<0.5) more in tongue samples, whereas Pg and Tf have not shown significant values (P>0.5). In diabetic patients, Fn and Tf have shown significant (P<0.5) an increase in subgingival and tongue samples, respectively, whereas Pg has not shown significant difference between subgingival and tongue samples.
Interpretation and Conclusion: The results confirm that there is no difference in clinical parameters between nondiabetic and diabetic periodontitis patients, but the odoriferous microbial profiles in tongue samples of diabetic patients were found to be high. However, there is a weak positive correlation between VSC levels, clinical parameters, and odoriferous microbial profiles.

Keywords: Chronic periodontitis, diabetes-mellitus, malodor, organoleptic, polymerase chain reaction, tongue coating

How to cite this article:
Kamaraj DR, Bhushan KS, Laxman VK, Mathew J. Detection of odoriferous subgingival and tongue microbiota in diabetic and nondiabetic patients with oral malodor using polymerase chain reaction. Indian J Dent Res 2011;22:260-5

How to cite this URL:
Kamaraj DR, Bhushan KS, Laxman VK, Mathew J. Detection of odoriferous subgingival and tongue microbiota in diabetic and nondiabetic patients with oral malodor using polymerase chain reaction. Indian J Dent Res [serial online] 2011 [cited 2019 Oct 21];22:260-5. Available from: http://www.ijdr.in/text.asp?2011/22/2/260/84301
Oral malodor is a commonly experienced condition among the general population. Although various nonoral causes are attributed to halitosis, the oral cavity is the principle source of physiologic malodor. [1] Oral malodor can be assessed by various methods and the most common is organoleptical (sniff test) method. A simple rapid chair side sulfide monitor, which provides scoring for the volatile sulfur compounds (VSCs) emanating from the oral cavity, (Tanita Corp., Japan), and its use has been reported by Pedrazzi et al. [2]

Various studies have shown positive correlations between the severity of periodontitis and VSC levels in mouth air, which is attributed to the increase in the percentage of VSCs due to an increase in subgingival plaque and gram-negative anaerobic microflora. [3] Tongue dorsum is an important area of microbial metabolism causing putrefaction, which leads to halitosis. The pathogenic microorganisms in subgingival and tongue samples may predict the risk of developing halitosis as well as periodontitis. [4] A recent study by Chang et al. [5] suggested that Pg, T. denticola(Td), E. corrodens(Ec), and C. albicans may play important roles in the periodontitis of both non-insulin-dependent diabetes mellitus (NIDDM) and non-diabetes mellitus (non-DM) individuals, but the etiology of periodontitis might be same in both the groups. [5]

As per MEDLINE search till date, the assessment of oral malodor using clinical methods and microbial parameters, in nondiabetic and diabetic chronic periodontitis patients is not available.

The purpose of the present investigation was to assess the malodor using the organoleptic method and tanita device; to quantify odoriferous microorganisms, such as P. gingivalis (Pg), T. forsythia (Tf), and F. nucleatum (Fn) of subgingival plaque and tongue coating of nondiabetic and diabetic chronic periodontitis patients using polymerase chain reaction (PCR) technique.


   Patients and Methods Top


Thirty patients of both sexes (15 nondiabetic and 15 diabetic) of age group 30-60 years with chronic generalized periodontitis were included. The screening outlined by the American Diabetes Association in 1979 was used to define the diabetic status of the subjects. [6]

Patients suffering from any other systemic diseases, which were known to cause oral malodor, who had received any antibiotic therapy in the last 3 months, who had received any surgical or nonsurgical therapy 6 months prior to the start of the study, pregnant or lactating mothers and smokers, were excluded from the study. An observational cross-sectional double-blinded study was performed. Patients were refrained from mouth rinses for a period of 24 h prior to examination and also from drinking and eating 2 h prior to their appointment. The clinical parameters recorded include: plaque index (PI), [7] gingival index (GI), [8] and gingival bleeding index (GBI). [9] The investigator who recorded oral malodor and the microbiologist who performed the PCR were blinded.

The malodor was recorded by both organoleptic method and by Tantia breath alert [10] to detect the VSC and hydrocarbon gases in the mouth air. Organoleptic method, considered as a reference standard was performed. The patient was asked to pinch the nose with the fingers to stop his or her breathing for a moment with the lips sealed and then exhale gently by opening the mouth and the odor detected this way was from local factors of oropharyngeal cavity [11] Odor levels were measured as 1 - No odor; 2 - Slight odor; 3 - Moderate odor; 4 - Strong odor. After every use the tip was cleaned and dried. [2]

Tongue coating was estimated by visual examination and scored as 0 - Non visible; 1 - Less than 1/3 rd of tongue dorsum surface covered; 2 - Less than 2/3 rd covered; 3 - More than 2/3 rd covered. [12]

Subgingival plaque and tongue samples were collected from 5 to 6 sites with 5-7 mm of pocket depth [13] and from the dorsal surface of the tongue with a wooden spatula, [3] respectively. The samples were dispensed in separate vials containing transport media, namely, TE buffer (10 mM Tris-HCl, 1 mM EDTA pH 8) and thioglycolate broth and sent to the microbiological laboratory within 24 h of collection, where they were subjected to Multiplex PCR analysis for Pg, Tf, and Fn. [14]

Statistical analysis

The results obtained from the various parameters were subjected to statistical analysis and were expressed as mean±SD and proportions as percentages. Nonparametric tests were used since the measurements were in scores and counts. Wilcoxon's signed rank test and Mann-Whitney test were done for intragroup and intergroup, respectively. The relationship between clinical and microbial parameters was assessed by Spearman's correlation coefficient.


   Results Top


The results are shown in Graphs 1-3 and [Table 1], [Table 2], [Table 3] and [Table 4]. The comparison of PI, GI, and GBI scores between the nondiabetic and the diabetic was not significant [Graphs 1 and 2]. The halitosis measurement revealed that tanita score of II was demonstrated by 53.3% and 66.7% of the subjects of the nondiabetic and diabetic groups, respectively, but organoleptic score of 4 was assessed in nondiabetic (53.3%) and diabetic (46.7%) groups, and no significant differences were found between the groups. On halitosis measurement, both the nondiabetic (53.3%) and diabetic (66.7%) groups showed a maximum tongue coating score of 3 [Graph 3].
Table 1: Comparison of microbial profile in nondiabetic and diabetic patients


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Table 2: Comparison between subgingival plaque and tongue sample in nondiabetic and diabetic patients


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Table 3: Spearman's correlation comparing VSC values (Tanita and Organoleptic) to clinical parameters and tongue coating of nondiabetic and diabetic patients


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Table 4: Spearman's correlation comparing VSC values (Tanita and Organoleptic) to microbial profiles in subgingival and tongue samples of nondiabetic and diabetic patients


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The PCR quantification of Pg was significantly higher in the diabetic group (14.7±13.4) than in the nondiabetic group (1.3±3.8). The PCR quantification of Fn was also highly significant for diabetic (66.8±43.7) group than the nondiabetic group, but no significant difference was found for Tf using the Mann-Whitney test [Table 1].

Microbial profile of tongue samples revealed a highly significant number of Pg in the diabetic group (21.6±11.9) than in the nondiabetic group (5.5±9.4). The PCR quantification of Tf was also highly significant for the diabetic group (12.8±9.0) than the nondiabetic group. Fn showed no significant difference using the Mann-Whitney test [Table 1].

In comparison to the subgingival plaque, tongue sample showed a significantly high level of Tf and Fn in the diabetic group, whereas Fn was found to be significantly high in the nondiabetic group using the Wilcoxon's test [Table 2].

Assessment of correlation between the clinical parameters (TC, PI, GI, GBI) and VSC levels (Tanita score TS and Organoleptic score OS) in nondiabetic and diabetic patients revealed a significant correlation between tongue coating, GI, and GBI in the diabetic group. A higher GI and GBI were observed in the diabetics [Table 3].

The Fn count of tongue sample in the diabetic group was significantly correlated with organoleptic and tanita scores and the Tf count was significantly correlated with tanita score in the nondiabetic group. The results reveal that Fn and Tf were chiefly associated with malodor and the Pg levels were not correlated with both methods of malodor assessment [Table 4].


   Discussion Top


The present study revealed no difference in mean plaque score, gingival score, and percentage bleeding score between the nondiabetic and the diabetic, which is similar to the observation made by a few authors. [15],[16] On the contrary, higher plaque score, [15],[16],[17],[18],[19] gingival score, [18],[19],[20],[21],[22] and higher mean percentage bleeding score [23],[24] in diabetic patients than the nondiabetic were reported.

However, no significant difference in malodor levels and tongue coating were observed between the groups. But, the malodor estimation revealed 66.7% of Tanita score II in diabetic patients in contrast to higher percentage of organoleptic score of II in nondiabetic patients. The tongue coating was not significantly different between the groups. According to these authors, the results are presented for the first time in this study.

Gram-negative anaerobes are known to produce volatile sulfur compounds (VSCs) from blood products, Pg, Fn, and Tf (formerly B. forsythus), which are gram-negative anaerobic rods that actively produce VSCs, such as H 2 S and CH 3 SH. [25] It has been hypothesized that the tongue dorsum may be an important area of microbial metabolism causing putrefaction, leading to halitosis, [26] but the role of specific bacteria on the tongue surface in malodor production has not been fully understood in vivo. These bacteria are detectable through their ability to hydrolyze the synthetic trypsin substrate N-benzoyl-dl-arginine-2-naphthylamide.

In the present study, the subgingival plaque sample presented a significantly higher level of Pg (44.7±13.3) in the diabetic group similar to a few reports, [27],[28],[29],[30],[31],[32] and a few studies reported no difference between diabetic and nondiabetic patients. [28],[29] Fn was significantly high in the diabetic, whereas Tf has not shown any significant difference between the diabetic and the nondiabetic, in contrast to reports suggesting Tf was less frequently associated with periodontal disease in NIDDM than in non-DM individuals. [33] Zambon et al. [34] found Pg in 75%, Pi  Prevotella intermedia Scientific Name Search n 88%, and Fn in 50% of NIDDM with periodontitis. Mandell et al. [35] detected Pi, Ec, and Fn in 53%-80% of their patients, whereas the prevalence of Pg (13%) and Aggregatibacter actinomicetecomitants Aa (7%) were lower in insulin-dependent diabetics with periodontitis. In contrast, Wolff et al found Pg and Fn at a comparable prevalence in a larger nondiabetic population with primarily early periodontitis. [36] The above literature reveals an inconsistent microbial profile among diabetic and nondiabetic groups.

Tongue samples revealed highly significant count of all the three organisms in the diabetic than in the nondiabetic group. The microbial comparison revealed higher PCR quantification of Pg (5.5±9.4) and Fn (34.0±41.7) in the tongue samples of the nondiabetic group and a significantly high Fn count in subgingival samples of diabetic patients. Pg and Tf were high in the tongue samples than the subgingival plaque samples in contrast to a report, [37] wherein Pg was found in only one sample. Fn was found to be high in the tongue sample than the subgingival plaque, in contrast to the detection frequency of Fn in tongue coat was found to be lower than in subgingival plaque. [25]

Tf was found to be more in the subgingival plaque, which was not significant, similar to the report by Kato et al. [25] In contrast, a study suggested that the microbes found in the subgingival plaque and tongue coatings were similar. [38] No consistent results are found in the literature regarding comparison of subgingival plaque with tongue microbial flora.

Recent studies have indicated that the dorsal surface of the tongue may be the primary source of microbial putrefaction in the mouth, [26],[37] and tongue coating, an important factor in the formation of oral malodor in both healthy and periodontitis patients. Although studies suggest that the flora on the tongue is similar to odor-producing periodontal bacteria, [37] a large variability is found in the counts of individual species in subgingival and tongue samples. This finding correlates with the previous studies of the tongue flora, which showed similar fluctuations in total count and in the prevalence and proportions of recovered individual bacterial species. [37] The variability could be due to difficulty in obtaining a standardized sample of the tongue flora and the tongue is a soft, highly mobile, and flexible structure, which hampers standardization of sampling techniques, such as pressure used during collection and surface area being scraped. [36] Fluctuations in the tongue flora over time within an individual as observed by a few authors may provide an additional explanation for the variability in bacterial counts. [36]

Various clinical studies have compared oral malodor and periodontal disease. A highly significant association between malodor and periodontitis was reported in a group of approximately 50 Israeli adults. [39] A study by Mathew and Vandana, revealed positive correlation between clinical parameters and VSC levels, [40] and Bosy et al have shown no correlation between the clinical parameters and halitosis grading. [26]

In this study, tongue coating was correlated with organoleptic assessment of malodor in diabetic group. Further analysis is required to rule out the acetone breath measured in organoleptic method. GI and GBI were also significantly correlated with malodor estimation. Here, for the first time an attempt is made to correlate VSC and clinical parameters, which showed a positive correlation between VSC and tongue coating in the nondiabetic group. [12],[36],[41],[42] A positive correlation between VSC levels and PI have been reported. [3],[42],[43] In contrast, Bosy et al [26] reported that the amount of plaque was not associated with VSC levels. Tsai reported significant correlation between organoleptic score and PI, but the concentration of VSC was not significantly correlated with PI. Studies have also shown positive correlation between VSC levels and GI. [3],[43],[44] In contrary, studies have shown a negative correlation between GI and VSC levels. [26],[45] Studies have shown positive correlation between VSC levels and GBI. [11],[45]

Since tanita gives digital reading and measures only VSC, oral malodor was assessed by both the methods. To prevent interexaminer variability, organoleptic assessment was done by a single operator, but the assessment might not discriminate between VSC and VSC combined with acetone breath in diabetic patients.

On comparison of microbial profile with VSC levels, Fn count was significantly correlated with organoleptic and tanita score in diabetic group, but Tf count was significantly correlated with tanita score in nondiabetic groups. Various studies have also reported significant association of BANA positive organisms, that is, Pg and B. forsythus with the oral malodor. [3],[25],[26],[39],[46],[47]

Study by Tanaka et al [46] reported the association of oral malodor and tongue periodontal pathogens (Pg, Tf, Pi, Fn,, Td) with real-time PCR. Among the periodontopathogens, Tf displayed higher proportions in malodor subjects than healthy controls. In contrast, Donaldson et al [4] concluded that there is no correlation between halitosis and any specific bacterial genus in the dorsum of tongue. The increased diversity of species in halitosis samples suggests that halitosis may be the result of complex interactions between several bacterial species.

As no comparative studies exist in periodontal literature, correlating the relationship between subgingival and tongue microbial profile (Pg, Fn, Tf) and VSC levels (TS and OS) in diabetic patients was not possible.

The dental research community has long ignored the subject of oral malodor. It is our hope that future studies will overcome the difficulty of diagnosing this long-standing problem and provide effective treatments to relieve individuals who suffer from oral malodor. The old practice of tongue cleaning should be recommended as a regular oral hygiene measure


   Conclusion Top


The clinical parameters of periodontal inflammation and oral malodor assessment did not differ between diabetic and nondiabetic patients. Pg and Fn count was found to be higher in subgingival plaque of diabetics, but Fn count was higher in tongue scrapings of nondiabetics. The tongue scrapings of diabetics demonstrated increased number of microorganisms. A weak positive correlation between clinical parameters (TC, PI, GI, GBI) and VSC levels (TS and OS) and significant correlation between organoleptic scoring and tongue coating, GI, GBI was obtained in both diabetic and nondiabetic patients.

 
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Correspondence Address:
Vandana K Laxman
Department of Periodontics, College of Dental Sciences, Davangere, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0970-9290.84301

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]

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3 A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes
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4 The role of oral anaerobic bacteria, and influence of social and health factors in halitosis aethiology [Mutes dobuma anaerobo baktēriju loma, kā arī sociālo un veselības faktoru ietekme uz halitozes etiologiju]
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[Pubmed]



 

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