|Year : 2015 | Volume
| Issue : 2 | Page : 63-68
Relationship between periodontal disease and carotid atheromatous plaque: A clinico-ultrasound study
Surekha Ramrao Rathod1, Farooque Khan1, Trupti Satish Sarda1, Anubha Raj2
1 Department of Periodontology, VSPM Dental College and Research Institute, Nagpur, Maharashtra, India
2 Department of Periodontics, VSPM Dental College and Research Institute, Nagpur, Maharashtra, India
|Date of Web Publication||14-Jul-2015|
Surekha Ramrao Rathod
A-20, Mahalgi Nagar, Ring Road, Nagpur, Maharashtra
Source of Support: None, Conflict of Interest: None
Aim: The aim of this study was to determine the relationship between Carotid atheromatous plaque in carotid artery with periodontal health and disease clinically and ultrasonographically and secondarily whether these relations are dependent on the level of serum high-density lipoprotein (HDL) cholesterol.
Materials and Methods : The cross-sectional study was carried out on 60 subjects. Of which 30 subjects with chronic periodontitis and 30 subjects with healthy periodontium were recruited and they underwent ultrasound scanning of common carotid arteries to determine carotid plaque thickness. Clinical parameters measured were probing pocket depth, clinical attachment loss, plaque index, gingival index and biochemical parameters included total cholesterol, triglycerides, and HDL levels.
Results : Periodontal disease is positively associated with carotid atherosclerosis. Plaque thickness and prevalence of carotid atheromatous plaque were significantly higher in the test group as compared to the control group. In the test group the mean carotid atheromatous plaque thickness was found to be 2.18 mm whereas in the control group it was found to be 0.14 mm. In test group, there was a positive and highly significant correlation of probing depth (PD) with triglycerides and total cholesterol levels and carotid atheromatous plaque thickness but a negative correlation between PD and HDL, triglycerides and total serum cholesterol levels in healthy subjects. HDL was significantly less in test group when compared with a control group with a P = 0.004.
Conclusion: An inter-relationship between periodontal disease and the presence of atheromatous plaque exists. The prevalence of both periodontitis and atherosclerosis is very high. Periodontitis should be diagnosed and treated at its earliest and hence that clinician and public health practitioner can control the epidemic of cardiovascular diseases and reduce mortality.
Keywords: Carotid Doppler, carotid atheromatous plaque, cardiovascular diseases, periodontitis
|How to cite this article:|
Rathod SR, Khan F, Sarda TS, Raj A. Relationship between periodontal disease and carotid atheromatous plaque: A clinico-ultrasound study. Saudi J Oral Sci 2015;2:63-8
|How to cite this URL:|
Rathod SR, Khan F, Sarda TS, Raj A. Relationship between periodontal disease and carotid atheromatous plaque: A clinico-ultrasound study. Saudi J Oral Sci [serial online] 2015 [cited 2019 Sep 22];2:63-8. Available from: http://www.saudijos.org/text.asp?2015/2/2/63/160760
| Introduction|| |
Periodontal disease is a multifactorial infectious disease influenced by several risk factors such as genetic, environmental and host immune system. Although microorganisms are implicated as the etiologic agent responsible for the inflammatory lesion, the products of inflammation play an important role in the loss of connective tissue as well as in the loss of supportive alveolar bone. 
Chronic infections have been reported as one of the risk factors for coronary heart disease such as ischemic stroke and the major contributing factor in the majority of cases of cardiovascular disease, and cerebrovascular disease is atherosclerosis. 
One of the outcomes of this disease process is the narrowing of the arteries resulting from the subendothelial deposition of cholesterol, cholesterol esters and calcium within the vessel walls. Rupture of the atherosclerotic plaque yield thrombi that travel distally to occlude arteries, resulting in myocardial infarction and stroke. 
High Density Lipoprotein (HDL) have several antiatherogenic properties, such as an ability to promote the efflux of cholesterol from cells to function as an important antioxidant by inhibiting Low-Density lipoprotein (LDL) oxidation to prevent or interrupt foam cell formation and to retard inflammatory activity, for instance these properties may prevent harmful effects of infections and conversely infections may have a more detrimental effect in the absence of functioning HDL. Therefore considering the possible biologic mechanism by which chronic bacterial infections increase the risk of atherosclerosis, the role of -HDL appears to be particularly interesting. 
The aim of the present study was to determine the relationship between atheromatous plaque in the carotid artery with periodontal health and disease clinically and ultrasonographically and secondarily whether these relations are dependent on the level of HDL cholesterol. The objectives of the study were to evaluate the presence of carotid atheromatous plaque in healthy and periodontally diseased subjects and to correlate and compare carotid atheromatous plaque and HDL, total serum cholesterol and triglycerides levels in periodontal health and disease.
| Materials and Methods|| |
A randomized cross-sectional observational study was carried out consisting of 60 subjects, ≥38 years of age, reporting to the Department of Periodontics and Implantology (from October 2013 to September 2014). The inclusion criterion was chosen to ensure the adult onset of periodontitis in the patient group and along with it the disease may have had time to affect the process of atherosclerosis. The test group included 30 subjects who were referred to the department of Periodontology and were diagnosed with moderate to severe periodontitis. In the control group the 30 subjects were recruited from the patients coming to the hospital for regular dental check-ups or for the restorative dental procedure. Thus, patients in the control group had healthy periodontium. The purpose of this study was explained verbally as well as written information was provided to all the study participants. Written ethical clearance was obtained from institutional ethics committee. On the basis of extensive medical history by interview, the following subjects were considered for exclusion: Individuals with any given disease or chronic medical condition apart from periodontitis, any type of cardiovascular disease, smokers and pregnant women. The study was conducted in a joint collaboration with the Department of Periodontics, Department of General Radiology, and Department of Biochemistry.
Determining the presence and thickness of carotid plaque in common carotid artery: The ultrasonographic assessment of carotid arteries was done according to the method described in Atherosclerosis Risk In Communities study. , A duplex ultrasound system with 7.5 MHz linear array transducer was used to scan the arteries. The machine used to scan the arteries was Mylab 50 Esoate. The carotid arteries were visualized with transverse and longitudinal scans to check the presence of significant focal atheroma which is defined as a localized protrusion within the vascular lumen. The presence or absence of atherosclerotic plaque and the carotid atheromatous plaque thickness was evaluated in the carotid arteries using Carotid Doppler Ultrasound in both the groups [Figure 1]. The investigations were done by a single, trained and experienced investigator who was blinded about the periodontal status.
Analysis of Systemic conditions: Overall adiposity was estimated by a body mass index which was calculated by the formula weight in kilograms divided by height in meters squared. Participants were asked to fast before coming to the clinical visit and fasting venous blood samples were taken by venipunture in the antecubital fossa in a tube. From these tubes, serum was prepared and was stored at −20°C until all samples from all participants were collected.
|Figure 1: Carotid atheromatous plaque thickness calculated using carotid doppler ultrasound scan|
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Measurement of biochemical parameters: Levels of total serum cholesterol, HDL and triglycerides were determined in the aliquots of plasma that were stored at −20°C. Plasma levels of HDL and total cholesterol were measured with standard enzymatic assays. All the above measurements were made blinded with respect to periodontal status.
Measurement of clinical parameters: The clinical parameters that were recorded in subjects of both the groups at the time of study included Plaque index (PI) (Tureskey and Gilmore), (1970)  Gingival index (GI) (Loe and Silness, 1963),  Probing depth (PD) and Clinical attachment level (CAL). Parameters were recorded using Williams Graduated probe.
It was performed using EPI info software version 7. Pearson's correlation coefficient test was performed to find out correlation between parameters and student t-test was used to check the level of significance (α = 0.05)
| Results|| |
The study was carried out on a total of 60 subjects (37 males and 23 females). The test group consisted of 30 systemically healthy individuals showing a mean age of 43.4 years affected by severe periodontitis. The control group consisted of 30 systemically healthy subjects showing a mean age of 44 years. There was no significant difference in mean age of both the groups. Patients in the test group showed a mean probing pocket depth (PPD) of 4.769 mm and those in the control group showed a mean PPD of 1.305 mm. There was a statistically significant difference with respect to PPD when compared between the two groups. The mean CAL for the test group was 5.86 mm and for the control group mean CAL was 0 mm. The mean GI and PI in the test group were 1.86 and 2.77 respectively whereas in the control group, it was 0 and 2.42 respectively.
In the present study, we found that, periodontal disease is positively associated with carotid atherosclerosis. Plaque thickness and prevalence of plaque were significantly higher in the test group as compared to the control group. In the test group, the mean plaque thickness was found to be 2.18 mm, whereas in the control group it was found to be 0.14 mm. Thus in chronic periodontitis subjects, we found a positive correlation between periodontal disease status and carotid artery plaque thickness suggesting that periodontal disease has an association with atheroma formation. In chronic periodontitis subjects (test group) we found a positive and highly significant correlation of PD with triglycerides and total cholesterol levels and plaque thickness but a negative correlation between PD and HDL, triglycerides and total serum cholesterol levels in healthy subjects. The mean levels of HDL, triglycerides and total cholesterol levels in the test group were 30.69, 206.9 and 191.6 respectively whereas in the control group the mean values were 31.47, 139.5 and 171.2 respectively. Body mass index was also calculated in both the groups and the mean values for the test group, and the control group were 25.46 Kg/m 2 and 20.44 Kg/m 2 respectively. HDL, which is protective cholesterol, was significantly less in periodontitis group when compared with healthy subjects (control group) with a P = 0.004 [Table 1].
|Table 1: Descriptive statistics and details of clinical and biochemical parameters for the control group (group I) and the test group (group II)|
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| Discussion|| |
Connective tissue breakdown or degradation is the hallmark of both cardiovascular and periodontal diseases. The primary enzymes leading to collagen breakdown are matrix metalloproteinases. These enzymes degrade the fibrous cap in atherosclerosis, leading to myocardial infarction.  Similarly, in periodontitis, these enzymes degrade the connective tissue which results in tooth loss.  Thus there exists parallelism between periodontal tissue destruction and cardiovascular disease, both mediated and/or regulated by a similar pathway, in this case one associated with MMPs. Matsumura, et al., 2005 had concluded from his study that there is increasing evidence that inhibition of MMPs, already shown to be effective for inhibition of periodontal attachment loss, can also inhibit the development of cardiac failure.  Literature has shown that systemic and/or local infections may lead to the development of atherosclerosis in association with hemodynamic stress, immune reactions at the vascular walls and lipid imbalance.  This study focused to find the relationship between periodontitis and noninvasive measurements of atherosclerosis in individuals free of any cardiovascular disease. Periodontal disease which is an inflammatory condition of the supporting tissues of the teeth has been found to be associated with the severity and progression of atherosclerosis due to the production of inflammatory mediators and because of the microbial burden. ,
The results of this study showed that periodontal disease is positively associated with carotid atherosclerosis. In a study carried out by Mattila et al., he found an association between periodontal infection and atherosclerosis in 100 subjects (12 females and 88 males) who were referred for coronary angiography.  In chronic periodontitis subjects, we found a positive and statistically significant correlation between periodontal disease status and carotid artery plaque thickness. In this study, total serum cholesterol and triglycerides levels were significantly higher in subjects with periodontitis then in control subjects. These findings are in accordance with those obtained from other clinical studies showing higher lipid levels associated with Porphyromonas gingivalis infection in periodontitis patients. 
In chronic periodontitis subjects, we found a positive and significant correlation between PD and triglycerides and total cholesterol levels whereas in healthy subjects (control group) a negative correlation between PD and HDL, triglycerides, total cholesterol levels was observed.
Matthias and et al. in their study to evaluate the periodontal status along with colour-coded duplex sonography of internal carotid artery stenosis, found that oral hygiene indices are associated with mortality in patients with atherosclerosis.  Losche W also reported higher plasma levels of total cholesterol, LDL cholesterol and triglycerides in chronic periodontitis patients when compared with periodontally healthy controls.  Piconi et al. in their study to evaluate the effect of periodontal therapy on changes in carotid intima media thickness (IMT) in systemically healthy subject, found that IMT was significantly decreased at different locations in the carotid artery. In elderly, the increase in IMT might have been caused by periodontitis, but the well-known influence of ageing on both the prevalence of periodontal disease according to Albander et al. in 1999 and thickening of intima-media according to Howard et al. cannot be ruled out. , In our study, there was no significant difference in the mean age of both the groups. The association between periodontitis and increased thickening of the intima-media has been described in middle-aged to elderly subjects with chronic periodontitis as observed by Beck et al. and Soder et al. ,
Few possible explanations can be given for the association between periodontal disease and development and progression of atherosclerosis:
- Dental disease and atherosclerosis may reflect the individuals susceptibility to develop a disease in response to specific exogenous and endogenous stimuli. The individual's propensity to develop an exuberant inflammatory process is given importance.
- It merely reflects confounding by traditional risk factors for example diabetes, smoking, obesity, etc. which are considered as important determinants for vascular as well as dental diseases [Figure 2]. 
- The inflammation of the periodontal tissues may result in the development and progression of an inflammatory vascular disease. In the current study, a significant correlation between periodontal inflammation and progressive vascular disease has been demonstrated. ,
- According to the infectious theory, transient bacteremia from the periodontal foci leads to inoculation of pathogens in atheroma.
However, it is not clear whether pathogen itself or an immune response to pathogens triggers the progression of atherosclerotic plaque [Figure 3] and [Figure 4]. , Herzberg and Meyer gave an idea that Streptococcus sanguinis might directly lead to aggregation of platelets and thrombi formation, thus leading to the formation of an acute myocardial infarct.  Chiu B in the year 1999 also suggested that P. gingivalis and S. sanguis can be isolated from the atherosclerotic plaque during human carotid endarterectomy. 
|Figure 3: Mechanism of infectious agents in atherosclerosis. HDL: high density lipoprotein, LDL: low density lipoprotein|
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|Figure 4: Pathways relating to periodontal disease and chronic vascular disease|
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There are few limitations of the study :
- Blood pressure was not measured and correlated between the 2 groups.
- Microbiological assessment of the carotid plaque was not carried out.
- As it is a cross-sectional study, no intervention was carried out for the test group. Hence further studies should be carried out to check the effect of intervention therapy in chronic periodontitis patients on the carotid plaque.
| Conclusion|| |
There exists an inter-relationship between the presence of atheromatous plaque with periodontal disease. The prevalence of both periodontitis and atherosclerosis is very high. The cost to society is directly attributable to atherosclerotic sequelae. Periodontitis is treatable, moreover is preventable, which is an option available to clinician and public health practitioner for the control of an epidemic of cardiovascular diseases. As the present study suggest that periodontal infection plays an important role in atherosclerosis, prevention and treatment of the periodontal infection may be very important in preventing mortality and morbidity rate associated with cardiovascular disease. Future directions - Further long-term evaluation is needed to be carried out including more subjects and parameters to further validate the results of the present study and confirm that periodontal disease is a true factor for systemic disease and that initiation or progression of these medical conditions can be reduced by periodontal treatment.
| References|| |
Beck JD, Elter JR, Heiss G, Couper D, Mauriello SM, Offenbacher S. Relationship of periodontal disease to carotid artery intima-media wall thickness: The atherosclerosis risk in communities (ARIC) study. Arterioscler Thromb Vasc Biol 2001;21:1816-22.
Scannapieco FA, Bush RB, Paju S. Associations between periodontal disease and risk for atherosclerosis, cardiovascular disease, and stroke. A systematic review. Ann Periodontol 2003;8:38-53.
Mattila KJ, Nieminen MS, Valtonen VV, Rasi VP, Kesäniemi YA, Syrjälä SL, et al.
Association between dental health and acute myocardial infarction. BMJ 1989;298:779-81.
Ansell BJ, Watson KE, Fogelman AM, Navab M, Fonarow GC. High-density lipoprotein function recent advances. J Am Coll Cardiol 2005;46:1792-8.
Burke GL, Evans GW, Riley WA, Sharrett AR, Howard G, Barnes RW, et al.
Arterial wall thickness is associated with prevalent cardiovascular disease in middle-aged adults. The Atherosclerosis Risk in Communities (ARIC) Study. Stroke 1995;26:386-91.
Soben Peter Community and Preventive Dentistry: Tureskey and Gilmore; 1970.
Loe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 1963;21:533.
Tenenbaum HC, Lai JY, Shelemay A, Goldberg MB. is there a link between periodontitis and cardiovascular disease? 2005.
Lee HM, Ciancio SG, Tüter G, Ryan ME, Komaroff E, Golub LM. Subantimicrobial dose doxycycline efficacy as a matrix metalloproteinase inhibitor in chronic periodontitis patients is enhanced when combined with a non-steroidal anti-inflammatory drug. J Periodontol 2004;75:453-63.
Matsumura S, Iwanaga S, Mochizuki S, Okamoto H, Ogawa S, Okada Y. Targeted deletion or pharmacological inhibition of MMP-2 prevents cardiac rupture after myocardial infarction in mice. J Clin Invest 2005;115:599-609.
Ross R. Atherosclerosis - An inflammatory disease. N Engl J Med 1999;340:115-26.
Desvarieux M, Demmer RT, Rundek T, Boden-Albala B, Jacobs DR Jr, Papapanou PN, et al.
Relationship between periodontal disease, tooth loss, and carotid artery plaque: The Oral Infections and Vascular Disease Epidemiology Study (INVEST). Stroke 2003;34:2120-5.
Cairo F, Gaeta C, Dorigo W, Oggioni MR, Pratesi C, Pini Prato GP, et al.
Periodontal pathogens in atheromatous plaques. A controlled clinical and laboratory trial. J Periodontal Res 2004;39:442-6.
Mattila KJ, Valle MS, Nieminen MS, Valtonen VV, Hietaniemi KL. Dental infections and coronary atherosclerosis. Atherosclerosis 1993;103:205-11.
Cutler CW, Machen RL, Jotwani R, Iacopino AM. Heightened gingival inflammation and attachment loss in type 2 diabetics with hyperlipidemia. J Periodontol 1999;70:1313-21.
Hoke M, Schillinger T, Mlekusch W, Wagner O, Minar E, Schillinger M. The impact of dental disease on mortality in patients with asymptomatic carotid atherosclerosis. Swiss Med Wkly 2011;141:w13236.
Loesche WJ, Schork A, Terpenning MS, Chen YM, Dominguez BL, Grossman N. Assessing the relationship between dental disease and coronary heart disease in elderly U.S. veterans. J Am Dent Assoc 1998;129:301-11.
Albandar JM, Brunelle JA, Kingman A. Destructive periodontal disease in adults 30 years of age and older in the United States, 1988-1994. J Periodontol 1999;70:13-29.
Howard G, Sharrett AR, Heiss G, Evans GW, Chambless LE, Riley WA, et al.
Carotid artery intimal-medial thickness distribution in general populations as evaluated by B-mode ultrasound. ARIC Investigators. Stroke 1993;24:1297-304.
Söder PO, Söder B, Nowak J, Jogestrand T. Early carotid atherosclerosis in subjects with periodontal diseases. Stroke 2005;36:1195-200.
Haynes WG, Stanford C. Periodontal disease and atherosclerosis: From dental to arterial plaque. Arterioscler Thromb Vasc Biol 2003;23:1309-11.
Schillinger M, Exner M, Mlekusch W, Sabeti S, Amighi J, Nikowitsch R, et al.
Inflammation and Carotid Artery - Risk for Atherosclerosis Study (ICARAS). Circulation 2005 3;111:2203-9.
Sabeti S, Exner M, Mlekusch W, Amighi J, Quehenberger P, Rumpold H, et al.
Prognostic impact of fibrinogen in carotid atherosclerosis: Nonspecific indicator of inflammation or independent predictor of disease progression? Stroke 2005;36:1400-4.
Beck JD, Eke P, Heiss G, Madianos P, Couper D, Lin D, et al.
Periodontal disease and coronary heart disease: A reappraisal of the exposure. Circulation 2005;112:19-24.
Desvarieux M, Demmer RT, Rundek T, Boden-Albala B, et al
. Relationship between periodontal disease, tooth loss and carotid artery plaque: The Oral Infection and Vascular Disease Epidemiology Study (INVEST). Stroke 2003;34:1220-54.
Herzberg MC, Meyer MW. Effects of oral flora on platelets: Possible consequences in cardiovascular disease. J Periodontol 1996;67 10 Suppl:1138-42.
Chiu B. Multiple infections in carotid atherosclerotic plaques. Am Heart J 1999;138(5 Pt 2):S534-6.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]