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| Year : 2014 | Volume
: 57
| Issue : 2 | Page : 259-264 |
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| Periodontal pathogens in atheromatous plaque |
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Saroj K. Rath1, Manish Mukherjee2, R Kaushik3, Sourav Sen4, Mukesh Kumar5
1 Department of Periodontology, Army Dental Centre, Research and Referral Hospital, Delhi Cantonment, New Delhi, India
2 Department of Periodontology and Oral Implantology, Armed Forces Medical College, Pune, India
3 CTC, Armed Forces Medical College, Gaya, Bihar, India
4 Department of Microbiology, Armed Forces Medical College, Gaya, Bihar, India
5 Department of Microbiology, Military Hospital, Gaya, Bihar; Department of Microbiology, AFMC, Pune, India
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| Date of Web Publication | 19-Jun-2014 |
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 Abstract | | |
Background: There has been increasing attention paid in recent years to the possibility that oral bacterial infection, particularly periodontal disease may influence the initiation and or progression of systemic diseases. These studies confirm the observation that heart disease is the most commonly found systemic condition in patients with periodontal disease. Moreover, the literature has also highlighted substantial evidence indicating the presence of Gram-negative periodontal pathogens in atheromatous plaques. Aim: This study intends to investigate the possible association between periodontal health and coronary artery disease by evaluating periodontal status, association between the periodontal plaque and coronary atheromatous plaques for presence of micro-organisms such as, Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, and Tannerella forsythia. Materials and methods: A case-control study was designed with seven patients who had undergone coronary endarterectomy for cardiovascular disease and 28 controls. The periodontal examination for cases was performed 1 day before vascular surgery and the controls were clinically examined. The atheromatous plaque sample collected during endarterectomy and the intraoral plaque samples were subjected to polymerase chain reaction for identification of A. actinomycetemcomitans, P. gingivalis, P. intermedia and T. forsythia. Results: The presence of periodontal bacteria DNA in coronary atheromatous plaques and sub-gingival plaque samples of the same patients was confirmed by this study. CONCLUSION A correlation was established between putative bacteria contributing to atheromatous plaques and species associated with periodontal disease. One particularly important study to be carried out is the investigation of a possible clinically meaningful reduction in coronary heart disease resulting from the prevention or treatment of periodontal disease. Keywords: Atheroma, dental plaque, polymerase chain reaction
How to cite this article:
Rath SK, Mukherjee M, Kaushik R, Sen S, Kumar M. Periodontal pathogens in atheromatous plaque. Indian J Pathol Microbiol 2014;57:259-64 |
| Introduction | |  |
Recent studies have proven that periodontal disease can produce numerous changes in systemic health with changes in the blood chemistry with a rise in inflammatory mediators, proteins, and lipids in the serum. [1] There has been increasing attention paid in recent years to the possibility that oral bacterial infection, particularly periodontal disease may influence the initiation and or progression of systemic diseases. Periodontitis has been proposed as having an etiological or modulating role in cardiovascular and cerebrovascular disease, diabetes, respiratory diseases, adverse pregnancy outcome, and rheumatoid arthritis. [2] Several mechanisms have been proposed to explain probable association between periodontitis and systemic diseases, including potential systemic dissemination of locally produced mediators such as C-reactive protein (CRP), interleukin-1 beta (IL-1β), IL-6, and tumor necrosis factor-alpha. [3]
The first indication of association between the dental disease and cardiovascular disease (CVD) or atherosclerosis was given in 1963. [4] Since then, there is growing evidence that poor dental health, especially the presence of periodontal disease, increases the risk of occurrence of coronary heart disease (CHD). [1] Studies conducted on different populations have suggested that atherosclerosis and the occurrence of acute myocardial infarction could be linked with chronic oral infections. [5] These studies confirm the observation that heart disease is the most commonly found systemic condition in patients with periodontal disease. Moreover, the literature has also highlighted substantial evidence indicating the presence of Gram-negative periodontal pathogens in atheromatous plaques. [6] Elevated levels of inflammatory molecules, which is seen as a result of periodontitis in long-term can predict increased risk for CVD. [7] Increased numbers of leukocytes have also been associated with CVD. [8]
However, evidence that periodontal infections contribute to or are decisive factors in the development of atherosclerotic plaques is circumstantial, and an epidemiological association is not proof of a causal link between pathogens and CVD, although bacterial presence at the diseased site is one of the requirements to determine a causal relationship. [9] As a result of the high-sensitivity of polymerase chain reaction (PCR) and other molecular methods, the presence of these pathogens within atheromatous plaques can be identified. In recent years, studies have implicated Aggregatibacter actinomycetemcomitans, Prevotella intermedia, Porphyromonas gingivalis and Tannerella forsythia in connective tissue attachment loss and periodontal inflammation.
This study intends to investigate the possible association between periodontal health and coronary artery disease by evaluating periodontal status, association between the periodontal plaque and coronary atheromatous plaques for presence of micro-organisms such as, A. actinomycetemcomitans, P. gingivalis, P. intermedia, and T. forsythia.
| Materials and methods | | |
A case-control study was designed in the Department of Dental Surgery and conducted in the coronary care unit of the Department of Cardiothoracic Surgery. A total of seven patients who had undergone coronary endarterectomy for CVD in the Department of Cardiothoracic Surgery between August 2009 and March 2012 were selected as cases and a total of 28 controls subjects were randomly selected from the patients attending Dental outpatient Department of Dental Surgery as per the research protocol initially submitted and approved. The necessary permission and ethical clearance was obtained. All subjects were verbally informed and a duly signed written informed consent was obtained from all the patients prior to their enrolment in the study.
Selection criteria
Following inclusion/exclusion criteria were followed for the study:
Inclusion criteria
- Cases were the patients undergoing coronary endarterctomy for CVD between August 2009 and March 2012 at the Department of Cardiothoracic Surgery.
- Controls were subjects with healthy periodontium without CVD randomly selected from patients attending dental OPD.
- Age group between 40 and 60 years.
- Presence of at least 14 natural teeth.
- No history of scaling/root planning or systemic antibiotic therapy in the previous 6 months.
- No history of other systemic diseases.
Exclusion criteria
- Patients who had received periodontal treatment within the past 6 months.
- Patients in whom oral examination was considered unsafe or contraindicated.
- Pregnant women.
- Patients who could not cooperate in oral examination.
After subject enrollment by an examiner, the following groups were assigned.
Group A (cases)
- A total of seven patients who had underwent coronary endarterctomy between August 2009 and March 2012 at the Department of Cardiothoracic Surgery.
- Atheroma sample collected after endarterctomy and plaque sample collected from periodontal pocket of the cases were later subjected to identification of periodontal pathogens by sampling DNA extract and amplification by PCR.
Group B (controls)
- 1:4 cases were selected as controls by randomization.
- These controls were selected randomly from patients attending Dental outpatient Department with healthy periodontium and without CVD.
- The plaque sample from gingival sulcus collected by a sterile paper point in the pocket later subjected to identification of periodontal pathogens by sampling DNA extract and amplification by PCR.
Periodontal examination
The periodontal examination for cases was performed 1 day before vascular surgery in cardiothoracic ward. The controls were clinically examined in Division of Periodontics in Department of Dental surgery. Clinical data were recorded using guidelines as described below. The clinical parameters included pocket depth (PD), clinical attachment level (CAL), plaque index (PI) by Silness and Loe. [10] Periodontal pocket bleeding index [11] and Russell's periodontal index. [12]
Microbiological examination
The atheromatous plaque sample of 2-10 mm long collected during endarterectomy was harvested and specimens obtained were placed in 10 ml of saline solution in sterile vials. The intraoral plaque samples collected from the same patient in Group A and from the control subjects during periodontal examination were also placed in 10 ml saline solution. All samples were immediately frozen in a bath of liquid nitrogen and stored at –80°C until DNA preparation in the laboratory of microbiology and virology.
Step 1
All the samples were subjected to identification for bacteria namely A. actinomycetemcomitans, P. gingivalis, P. intermedia and T. forsythia by sampling DNA extract and amplification by PCR.
Approximately, 100 mg of tissues was harvested from the atherosclerotic plaques and intra oral plaque then homogenized and subjected to DNA extraction. DNA was extracted by the Qiagen Kit method. After this, the eluted DNA was stored at –20°C.
Step 2
The whole genomic DNA extracts were used as templates in a PCR technique using the universal primers that targeted the 16S rRNA gene. The primers used were as under.
In the second round 40 cycles of PCR was run in the thermo cycler.
Step 3
Gel documentation for multiplex polymerase chain reaction
The amplified amplicon of second round PCR was demonstrated by using 2% agarose gel electrophoresis. By using 100 bp molecular weight markers the periodontal pathogens were identified based on the bp molecular weight [Figure 1] and [Figure 2]. | Figure 1: Amplified product of multiplex polymerase chain reaction 197 bps of band in Porphyromonas gingivalis
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 | Figure 2: Amplified product of multiplex polymerase chain reaction band in 3 and 6 wells showing Aa 360 bps and Tf 745 bps
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Statistical analysis
The clinical and microbiological data collected were tabulated and subjected to statistical analysis. The independent variables included age, and gender, education, socioeconomic status, marital status, medical status, smoking status, number of missing teeth, PD, number of teeth with CAL >3 mm, % sites with bleeding on probing and CAL were used to quantify the type of disease.
Means and proportions for personal characters, major risk factors and clinical parameters were calculated for both groups. The significance of any difference in means was tested by using "Student's t-test," and the significance of any difference in proportions was tested by using Dunn-idαk adjusted P value.
| Results | | |
Intra group comparisons of demographic parameters among cases, that is, patients undergoing coronary endarterectomy showed no statistically significant difference with respect to age, and sex, education, socioeconomic, and smoking status with P value of 1.000.
No statistically significant difference was observed in any of the periodontal parameters including PD, CAL,Periodontal Pocket Bleeding Index PPBI, PI, Russel's periodontal index, no. of sites with recession, average of recession in mm and class of recession, when the intra group comparisons were done with Dunn-Sidak adjusted P value of 1.000, 0.861, 1.000, 0.689, 1.000, 1.000, 1.000, and 0.886, respectively [Table 1]. | Table 1: Intra group comparisons of periodontal examination parameters among cases (Group A)
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The result of intra group comparisons of microbiological examination by PCR of sub-gingival plaque samples and coronary endarterectomy atheroma samples for identification of bacteria namely A. actinomycetemcomitans, P. gingivalis, T. forsythia and P. intermedia showed statistically significant difference in presence of T. forsythia (P value of 0.008) [Table 2]. | Table 2: Intra group comparisons of microbiological examination by PCR between sub-gingival plaque samples and coronary endarterectomy (Group A)
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Inter group comparisons between cases and controls (Group A and B)
Inter group comparisons between cases and controls for demographic parameters showed no statistically significant difference between the cases and controls. Comparisons of periodontal examination data between cases and controls reveal statistically significant higher results in cases for Russel's periodontal index, number of sites with recession, average of recession in mm and class of recession.
Inter group comparisons of microbiological examination by PCR between sub-gingival plaque samples of cases and controls for identification of bacteria showed statistically significant difference in presence of P. gingivalis, T. forsythia and P. intermedia (P value of 0.001, 0.008 and 0.004, respectively). Dunn-Sidak adjusted P value for A. actinomycetemcomitans, P. gingivalis, T. forsythia and P. intermedia were 0.172, 0.001, 0.008, and 0.004, respectively [Table 3]. | Table 3: Inter group comparisons of microbiological examination by PCR between sub-gingival plaque samples of cases and controls (Group A and B)
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During the microbial analysis of plaque samples by PCR in Group A it was seen that A. actinomycetemcomitans were seen in 71.43% of the samples, P. gingivalis in 100%, T. forsythia in 100% and P. intermedia in 71.43% of the samples. All four of these periodontal pathogens were present in 42.86% of the samples and A. actinomycetemcomitans, P. gingivalis and T. forsythia were seen in 57.14% of the samples.
Microbial analysis of endarterectomy samples by PCR in Group A shows that A. actinomycetemcomitans were seen in 42.86% of the samples, P. gingivalis in 71.43%, T. forsythia in 100% whereas P. intermedia was not found in the endarterectomy samples. Three of these periodontal pathogens, that is, A. actinomycetemcomitans, P. gingivalis and T. forsythia were seen in 42.86% of the samples. P. gingivalis and T. forsythia were seen in 28.57% of the endarterectomy samples. Only T. forsythia was seen in 28.8% of the samples .
Microbial analysis of plaque samples by PCR in Group B showed that P. gingivalis, T. forsythia and P. intermedia were seen only in 7.14% of the samples each whereas A. actinomycetemcomitans was not found in any of the sample.
The highlights of PCR analysis results are as follows. A. actinomycetemcomitans was detected both from plaque and atheroma samples of the same individuals in case sample no. 1 and 4. P. gingivalis was present in all the plaque samples and five atheroma samples of Group A. Therefore, five of the cases were positive for P. gingivalis in both atheroma and sub-gingival plaque samples; T. forsythia was detected from all plaque and all seven atheroma samples. However, none of the atheroma sample was infected with P. intermedia even if five of plaque samples were positive.
| Discussion | | |
Recent years have brought much research related to the potential connection between periodontitis and coronary disease. Many authors have demonstrated such a relationship; among others in USA, DeStefano et al., basing on 14 years of research on 9760 individuals aged 25-74 years, reported an increased risk of coronary disease in the group with periodontitis (25% higher). [13]
A case-control study was undertaken to determine association between presence of periodontal pathogens and CVD with the objective of comparing of distribution of four periodontal pathogens namely A. actinomycetemcomitans, P. gingivalis, Tanerella forsythus and P. intermedia between cases and controls to ascertain the role of these pathogens in the presence of CVD. The second important objective of the study was to find out the relationship between the above-mentioned four periodontal pathogens in objective one present in the periodontal pockets and in coronary arteries and the relationship to predict periodontal pathogens in CVD.
The first coronary end arterectomy was done by Baily et al. Due to increased morbidity and mortality, the procedure of coronary endarterectomy had lost its importance. [14],[15] Jhonson and Cooley who performed a large series of coronary endarterectomy revealed that there is an increase in surgical risk and good long term effect in selected group of patient. [16] Probably, because of complications associated with the type of surgery as brought out by various workers, we could be able to get a small number of endartectomy samples after surgical procedure from Department of Cardiothoracic Surgery of CTC, Pune.
The presence of periodontal bacteria DNA in coronary atheromatous plaques and sub-gingival plaque samples of the same patients was confirmed by this study and thus a correlation was established between putative bacteria contributing to atheromatous plaques and species associated with periodontal disease. The data of this study were consistent with those reported by Haraszthy et al. [6] (PCR-amplified 16S rDNA and DNA species-specific probes, 30% positive for T. forsythia, 26% for P. gingivalis, 14% for P. intermedia), Ishihara et al. [17] (PCR-amplified 16S RNA, 21.6% positive for P. gingivalis, 5.9% for T. forsythia) and Zhang et al. [18] T. forsythia was detected in all the seven of our atheromatous plaque samples from coronary endarterectomy, the observation of which was similar to the result of study by Haraszthy et al. [6]
A direct causal relationship between periodontitis and atherosclerotic CVD is not established. Multiple studies, however, support two biologically plausible mechanisms:
- Moderate to severe periodontitis increases the level of systemic inflammation, a characteristic of all chronic inflammatory diseases, and periodontitis has been associated with increased systemic inflammation as measured by high-sensitivity-CRP and other biomarkers. Treatment of moderate to severe periodontitis sufficient to reduce clinical signs of the disease also decreases the level of systemic inflammatory mediators. [19],[20]
- In untreated periodontitis, Gram-negative bacteria may be found in periodontal pockets surrounding each diseased tooth and in approximation to ulcerated epithelium, and bacterial species found predominantly in the periodontal pockets also have been found in atheroma. [21]
This study has proved the association of periodontal disease with coronary artery disease on the basis of second mechanism with existing bacteria both in sub-gingival area and atheroma sample from the same patient.
However, the current study has a few limitations. The conflicts of this study include first, the sample sizes were too small taking into account the number of endarterectomy because of mortality and morbidity associated with it. Second, the PCR which was employed here was not able to detect the bacteria quantitatively, rather only type of bacteria present in both sub-gingival sample and atheroma samples. A real-time PCR technique would have been more appropriate for quantitative analysis of bacteria.
| Conclusion | | |
The outcome of this study strengthens the association between poor periodontal health and coronary artery disease. Case-control design although provides a higher strength of evidence when compared to other cross-sectional studies, is still laden with biases such as small sample size and lack of quantitative bacterial analysis. The accumulation of epidemiologic, in vitro, clinical and animal evidence suggests that periodontal infection may be a contributing risk factor for heart disease. However, legitimate concerns have arisen about the nature of this relationship. Since even a moderate risk contributed by periodontal disease to heart disease could lead to significant morbidity and mortality, it is imperative that further studies be conducted to evaluate this relationship. One particularly important study to be carried out is the investigation of a possible clinically meaningful reduction in CHD resulting from the prevention or treatment of periodontal disease.
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Correspondence Address:
Saroj K. Rath
Department of Periodontology, Army Dental Centre, Research and Referral Hospital, Delhi Cantonment, New Delhi
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/0377-4929.134704
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3] |
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