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ORIGINAL ARTICLE
Year : 2017  |  Volume : 5  |  Issue : 1  |  Page : 24-30

Evaluation of association between severe periodontitis and carotid intima-media thickness in young adults


Department of Periodontology, Meenakshi Ammal Dental College, Chennai, Tamil Nadu, India

Date of Web Publication8-Mar-2017

Correspondence Address:
Dr. Sowmiya Lingeshwaran
Department of Periodontology, Meenakshi Ammal Dental College, Maduravoyal, Chennai - 600 095, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/heartindia.heartindia_47_16

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  Abstract 

Background and Objective: To evaluate the association between severe generalized periodontitis and carotid intima-media thickness (CIMT) in young, otherwise systemically healthy individuals.
Materials and Methods: A total of 60 systemically healthy individuals of age between 20 and 40 years were included in the study. Group I consisted of 30 individuals with healthy periodontal tissue and Group II with 30 individuals with severe generalized periodontitis. Ultrasonographic evaluation of bilateral CIMT at the level of common carotid artery was done.
Results: The overall mean intima-media thickness (IMT) in Group I was 0.52 ± 0.07 mm and in Group II was 0.61 ± 0.07 mm. Bivariate analysis considering the binomial IMT (≥0.6) as outcome variable showed odd's ratio = 16 for probing depth and clinical attachment loss. The final model of stepwise logistic regression using binomial IMT (>0.6) as outcome variable showed statistical significance with clinical attachment loss suggesting that as the clinical attachment loss increases the IMT also increases.
Conclusion: Severe generalized periodontitis is associated with subclinical atherosclerosis in young systemically healthy patients.

Keywords: Atherosclerosis, carotid intima-media thickness, periodontitis


How to cite this article:
Lingeshwaran S, Ramakrishnan T, Ari G, Nagarajan A, Ambalavanan N, Kanakamedala AK. Evaluation of association between severe periodontitis and carotid intima-media thickness in young adults. Heart India 2017;5:24-30

How to cite this URL:
Lingeshwaran S, Ramakrishnan T, Ari G, Nagarajan A, Ambalavanan N, Kanakamedala AK. Evaluation of association between severe periodontitis and carotid intima-media thickness in young adults. Heart India [serial online] 2017 [cited 2021 Dec 2];5:24-30. Available from: https://www.heartindia.net/text.asp?2017/5/1/24/201746


  Introduction Top


Periodontitis is a chronic “infectious/inflammatory” disease of multifactorial etiology.[1] Although it is initiated by dental plaque associated microorganisms, the inflammatory process is sustained by the host. Inflammation referring to a protective tissue response to injury has been implicated in the pathogenesis of many human diseases. It plays a central role in complex multifactorial chronic inflammatory diseases including periodontitis and cardiovascular disease (CVD).

The periodontium thus serves as a renewing reservoir for inflammatory mediators that is spilled over into systemic circulation thereby inducing and perpetuating the systemic effects.[2] Interleukin-1α (IL-1α) favors coagulation, thrombosis, and retards fibrinolysis. Chemical mediators IL-1, tumor necrosis factor-α, and thromboxane can cause platelet aggregation and adhesion, formation of lipid-laden foam cells, and deposition of cholesterol in the arteries.

B-mode ultrasonography is a noninvasive and highly reliable tool for assessing the early stages of atherosclerosis by measuring the thickness of the inner layer of the vessel walls.[3] This procedure is been used widely for monitoring the carotid artery and to identify the subclinical atherosclerosis condition.

The present study was performed to assess the link between severe generalized periodontitis and carotid intima-media thickness (CIMT) in young otherwise systemically healthy individuals. The intima-media thickness (IMT) of the carotid artery indicates the subclinical atherosclerosis status of an individual. There are numerous studies which points out this link in older individuals but not in younger adults. Hence, this current study was conducted to determine this association in younger individuals.


  Materials and Methods Top


The current study was undertaken to evaluate the association between severe generalized periodontitis and CIMT in young otherwise systemically healthy individuals.

About 85 outpatients who were referred to the Department of Periodontology, Meenakshi Ammal Dental College, were assessed for eligibility, out of which 21 patients did not meet the inclusion criteria, 4 patients refused to participate, and therefore, the study was commenced with 60 individuals. The statistical power was calculated, and it was found to be 94% with 60 samples. Informed consent was obtained from all the patients. Ethical approval was obtained from the Ethical Committee, MAHER University, Chennai, and the study was conducted according to the principles outlined in the Declaration of Helsinki of 1975.

Inclusion criteria

  • Individuals within the age range of 20–40 years,
  • Individuals with healthy periodontal tissue (Group I)
  • The individuals diagnosed with severe generalized periodontitis (Group II, with clinical attachment loss ≥5 mm in more than 30% of the sites)
  • Smokers who have the habit for >5 years.


Exclusion criteria

  • Individuals who had systemic antibiotic treatment within 3 months or any other regular medication
  • Pregnant mothers
  • Individuals involved in intense sporting activity
  • Smokers who have the habit for <5 years.


Sixty systemically healthy individuals were divided into Group I (control group) consisting of thirty individuals with healthy periodontal tissues and Group II (test group) contained of thirty individuals with severe generalized periodontitis.

All sixty individuals underwent a physical examination. Medical history was determined from each patient by the interview method. The information included as follows:

  • Presence of any systemic disease
  • Weight and height to calculate body mass index (BMI)
  • Smoking status, categorized as former, current or never smoker
  • Family history of CVD
  • Physical activity
  • Education level (high school, graduates).


On the basis of the medical history and smoking habit, the control group and the test group were segregated into homogeneous subgroups based on

  • Gender
  • Age (using a 5-year threshold of tolerance)
  • BMI (using 1-value as the threshold of tolerance)
  • Smoking habits: Exposure to smoking in years (using 5 years threshold of tolerance) were segregated into homogeneous subgroups.


Periodontal disease assessment

A single trained examiner assessed the full mouth plaque score, bleeding score, probing depth, and clinical attachment level in the study participants.

Complete periodontal examination included as follows.

Full mouth plaque score

The measurement of the state of oral hygiene by Silness–Löe plaque index which was based on the recording of the soft debris on all the teeth. Missing teeth are not substituted.

Full mouth bleeding score

Full mouth bleeding score was assessed by the papillary bleeding index (PBI). A blunt periodontal probe is carefully inserted into the gingival sulcus on the mesial aspect of the base of the papilla, then moved coronally to the papilla tip. This is repeated on the distal aspect of same papilla. The intensity of any bleeding thus provoked was recorded on a 0–4 scale.

Probing pocket depth

Probing depth was measured from the gingival margin to the base of the sulcus or pocket with a calibrated periodontal probe (William's periodontal probe) at six sites (mesiobuccal, midbuccal, distobuccal, mesiolingual, midlingual, and distolingual).

Clinical attachment level

It is calculated from measurements made from a fixed point that does not change such as the cementoenamel junction to the base of the sulcus or pocket with calibrated periodontal probe (William's periodontal probe) at six sites (mesiobuccal, midbuccal, distobuccal, mesiolingual, midlingual, and distolingual).

Blood collection and laboratory analysis

Venous blood samples were taken from each subject at least 2 weeks after periodontal examination by a single venipuncture in the antecubital fossa. Tubes containing blood without an anticoagulant were centrifuged at room temperature (2000 ×g) for 15 min. Within 1 h of collection, aliquots of serum samples were stored at −80°C until samples from all participants were collected.

The following were assessed

  • High-sensitivity C-reactive protein (CRP)
  • Random glucose
  • Triglycerides
  • High density lipid level (HDL-cholesterol)
  • Low density lipid level (LDL-cholesterol)
  • Total serum cholesterol
  • Glycated Hemoglobin (HbA1c%)
  • Cardiac risk ratio.


Ultrasonographic measurement of carotid intima-media thickness

Posture of the patient

The patient was examined in a supine position, and the head is inclined by about 30°. Depending on the patient's physique, a pillow or towel was placed externally at the origin of the common carotid artery.

Assessment of carotid intima-media thickness

CIMT was bilaterally assessed at the common carotid artery in both Group I and Group II patient in the supine position. A single experienced physician blinded with respect to periodontal condition assessed both groups.

CIMT was measured with an orthogonal incidence of the ultrasonic beam to the axial course of the artery, on a 10 mm segment of the far wall of the common carotid artery (longitudinal projection) avoiding nonlinear segments, using a dedicated software (Acuson X300 version 2.0, Niranjan Ultrasound India (P) Ltd, Calicut, Kerala, India Swami Vivekananda Diagnostic Centre). The real-time measurement of CIMT represented the mean of 10 measures on each side. The average of both right and left IMT was considered for all subsequent computations.

[Figure 1] shows ultrasonographic imaging of the right common carotid artery.
Figure 1: Imaging of the right common carotid artery

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[Table 1] shows the normal values for CIMT according to age.[4]
Table 1: Normal values for carotid intima media thickness according to age

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Statistical analysis

Statistical analysis was done using software SPSS (19.0, version for Windows https://spss.en.softonic.com/) (19.0, version for Windows). Descriptive statistics were expressed as mean ± standard deviation for both the groups. Odd's ratio (OR) was calculated using IMT (≥0.6 mm) as the outcome variable. The correlation between periodontal parameters, cardiac risk ratio, and CIMT was assessed using Karl Pearson's correlation coefficient. Multiple linear regression model (forward stepwise method; criteria: Probability-of-F-to-enter ≤0.05, probability-of-F-to-remove ≥0.10) was assessed with mean IMT as outcome variable. The final model of stepwise logistic regression using binomial IMT (>0.6) as outcome variable was fitted.


  Results Top


The study sample consisted of a total number of 60 individuals in two groups (Group I and Group II). Descriptive statistics and details of matching criteria for Group I and Group II are shown in [Table 2], and laboratory variables in Group I and control Group II are shown in [Table 3].
Table 2: Descriptive statistics and details of matching criteria for Group I and Group II

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Table 3: Laboratory variables in Group I and control Group II

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Correlation between periodontal parameters, IMT, and cardiac risk ratio are shown in [Table 4]. The OR of random blood sugar level, serum cholesterol level, triglyceride level were <1 which was statistically significant. The random blood sugar level was with OR of 0.66 with upper limit of 0.87 and lower limit of 0.51 which was statistically significant. The serum cholesterol level was with OR of 0.69 with the upper limit of 0.88 and lower limit of 0.54 which was statistically significant. The triglyceride level was with OR of 0.69 with the upper limit of 0.88 and lower limit of 0.54 which was statistically significant.
Table 4: Correlation between periodontal parameters and intima.media thickness and cardiac risk ratio

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[Table 5] shows the bivariate analysis considering the binomial IMT (≥0.6) as outcome variable.
Table 5: Bivariate analysis considering the binomial intima.media thickness (≥0.6) as outcome variable

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[Table 6] shows final model of forward stepwise logistic regression using binomial IMT (>0.6) as outcome variable showed BMI, random blood sugar, triglycerides, and serum cholesterol were not statistically significant (P > 0.05) whereas clinical attachment loss showed statistical significance (P = 0.009) suggesting that as the clinical attachment loss increases the carotid intima thickness also increases.
Table 6: Final model of stepwise logistic regression using binomial intima.media thickness (>0.6) as outcome variable

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[Figure 2] shows the mean carotid intima thickness in male (0.64 mm) had higher value compared to females (0.59 mm) in the Group II.
Figure 2: Comparison of mean carotid intima-media thickness between male and female in Group II

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  Discussion Top


The association between periodontal disease and increased CIMT has been described only in the middle-aged to elderly population with chronic/adult periodontitis.[5],[6],[7] The present study was conducted to evaluate the association between severe periodontitis and subclinical atherosclerosis in young otherwise systemically healthy individuals in the age range of 20–40 years.

Patients with severe generalized periodontitis were included in the study group suggesting that the threshold effect rather than a graded dose response exist, indicating that periodontal infections affecting ≥30% of the sites in the mouth may be needed to generate an infectious burden to cause systemic effects.[5]

The Group I included periodontally healthy individuals, and Group II consisted of individuals with severe generalized periodontitis.

It has been recognized that smoking habit is a risk factor for both periodontal disease and atherosclerosis.[8]

In this study, patient with smoking habit in Group I and Group II had higher IMT compared to nonsmokers. Recent experimental and clinical data support the hypothesis that cigarette smoke exposure increases oxidative stress which acts as a potential mechanism for initiating cardiovascular dysfunction.

Genco et al., 2005[9] analyzed the National Health and Nutrition Examination Survey III data and demonstrated that BMI was positively correlated with the severity of periodontal attachment loss; they found that this relationship is modulated by insulin resistance. In this study, the BMI for Group II was higher compared to Group I and it was statistically insignificant.

The mean plaque index score, mean PBI score, mean probing depth, and mean clinical attachment level was higher in Group II and was statistically significant as these individuals were diagnosed with periodontitis.

Emerging evidence suggests that periodontitis may have a role in chronic infection, the associated inflammatory responses in atherosclerosis and its complications, or both, and experimental and clinical studies have indicated a potentially deleterious effect of periodontitis.[10] Periodontal pathogens in vitro can promote platelet aggregation [11] and foam-cell formation.[10] Severe periodontal disease had 1.3 times the odds of having thick carotid arterial walls (≥1 mm) compared with individuals with less severe disease, after adjustment for traditional risk factors for atherosclerosis.[5] In this study, the right and left carotid intima thickness and mean carotid intima thickness were higher in Group II when compared to Group I.

Women tend to develop heart disease later in life than men. This difference has been attributed to the loss of estrogen during the menopausal transition.[12] It is proposed that cholesterol losing effects of estrogen cause movement of cholesterol from atheroma toward plasma and thereby retard the progress of atherosclerosis. These cholesterol-losing effects of estrogen enable women to enjoy freedom from coronary heart disease (CHD) during their reproductive age as compared to men of comparable age group.[13] As the females included in this study was within age range of 20–40 years, they showed lesser IMT value compared to males. The mean carotid intima thickness in male had higher value compared to females in the Group II, and the mean IMT in Group II males and females was higher compared to Group I males and females.

This was the first study where cardiac risk ratio was correlated with the plaque index, bleeding on probing, probing depth, and clinical attachment level and it was found to be statistically significant. Potential mechanisms by which periodontal infections might contribute to the pathogenesis of CHD and increased intima thickness are by the effects of endotoxins in the circulation, role of heat shock proteins, infection induced perturbations in lipid profiles, and by the formation of acute-phase reactants.

CRP represents an emerging and reliable marker of the acute-phase response to infectious burdens and/or inflammation. As a consequence of its kinetics, CRP best describes the inflammatory status of the individual.[14] Periodontitis may add to the inflammatory burden of the individual and may result in increased levels of cardiovascular risk based on serum CRP concentrations. The individuals in Group II had high sensitivity CRP level compared to Group I which was statistically significant (P = 0.04). In individuals with increased high-sensitivity CRP level, the odds for having increased IMT was 7.6.

The mean glucose level and HbA1c% in Group II were higher when compared with Group I and the difference was not statistically significant but the odds for having increased IMT was 0.66 and was statistically significant, chronic Gram-negative periodontal infection may result in increased insulin resistance and poor glycemic control.[15] Uncontrolled diabetes may lead to cardiovascular complications.[16]

The mean total serum cholesterol level and mean low density lipid level (LDL) in Group II were higher when compared with Group I, and the difference was statistically significant. The mean triglycerides level of the Group II was higher when compared with that of the Group I and the difference was not statistically significant (P = 0.15). The mean high density lipid level (HDL) of the Group II was lower when compared with that of the Group I, and the difference was statistically significant (P = 0.001). The odd's for increased IMT in individuals with high serum cholesterol level, and triglyceride level was 0.69 which was statistically significant. Increase in pro-inflammatory cytokine in response to chronic periodontitis causes a rise in serum lipid levels.[17]

Although IMT increase in the elderly [5],[6],[7] might have been caused by periodontitis, this finding cannot rule out the well-known influence of aging on both IMT thickening [18] and the prevalence of periodontal disease.[1],[19] The correlation between periodontal parameters and the CIMT in Group I and II suggests that probing depth significantly correlates with right IMT (P = 0.015), left IMT (P = 0.018), and mean IMT (P = 0.001).

Periodontal patients showed severe tooth loss, generalized loss of attachment and periodontal pockets, and extensive gingival inflammation, with esthetic, functional, and psychological problems when compared with the healthy individuals without signs of periodontitis.[20]

Positive relationship exists between the increased tooth loss and increased IMT in the arteries,[21] Severe bone loss,[22] overall periodontal bacterial burden,[23] and tooth loss [24] were associated with increased CIMT. In this study, the clinical attachment level shows statistical significance (P = 0.001) suggesting that when the clinical attachment loss increases the mean carotid intima thickness level also can increase. The odd's for increased IMT in individuals with increased probing pocket depth, and clinical attachment level was 16. The bivariate analysis was associated with binary IMT, with threshold value of greater than or equal to 0.6 mm. According to the Society of Vascular Ultrasound, Annual Conference 2009,[4] the normal carotid intima thickness range for adults between 30 and 39 years is 0.40 ± 0.03 mm and 40–49 years is 0.50 ± 0.03 mm. As the age group included in this study was in the range of 20–40 years of age, 0.60 mm was taken as the threshold value.

Relatively young patients with severe periodontal disease exhibit perturbed flow-mediated dilatation of the brachial artery compared with carefully matched controls.[25],[26] Endothelial dysfunction occurs early in the pathogenesis of arterial disease, in response to a wide range of risk factors that have been shown to predict cardiovascular events in epidemiologic studies.[26] This study showed statistical significant clinical attachment level with P = 0.009. The odd's for having increased CIMT in individuals with increased clinical attachment level was OR = 16 which was statistically significant. This suggest that as the clinical attachment loss increases the carotid intima thickness also increases.

Limitations of the present study include the differences in age between Group I and Group II. Even if a minimal age-related increase (~0.02 mm/year)[1] in CIMT was reported, the difference between Group I and Group II is only partially explained in this study by age difference.


  Conclusion Top


Periodontitis seems to contribute to systemic inflammation and individuals with increased clinical attachment loss are more prone to have increased carotid intima thickness. Thus, periodontal disease may predict a systemic atherosclerosis condition decades before the occurrence of clinical cardiovascular events. Further, studies are required to assess the stronger association between periodontitis and subclinical atherosclerosis.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Hugoson A, Norderyd O, Slotte C, Thorstensson H. Distribution of periodontal disease in a Swedish adult population 1973, 1983 and 1993. J Clin Periodontol 1998;25:542-8.  Back to cited text no. 1
    
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Ross R. Atherosclerosis – An inflammatory disease. N Engl J Med 1999;340:115-26.  Back to cited text no. 2
    
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Vieira CL, Caramelli B. The history of dentistry and medicine relationship: Could the mouth finally return to the body? Oral Dis 2009;15:538-46.  Back to cited text no. 3
    
4.
Alipour M, Doan HA, Bean B. Normal values of intima-media thickness (IMT) in patients with no traditional risk factors (RF) for atherosclerosis. Society of Vascular Ultrasound; Annual Conference 2009. Arch Cardiovasc Imaging 2013;1:27-31.  Back to cited text no. 4
    
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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.  Back to cited text no. 5
    
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Leivadaros E, van der Velden U, Bizzarro S, ten Heggeler JM, Gerdes VE, Hoek FJ, et al. A pilot study into measurements of markers of atherosclerosis in periodontitis. J Periodontol 2005;76:121-8.  Back to cited text no. 6
    
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Söder PO, Söder B, Nowak J, Jogestrand T. Early carotid atherosclerosis in subjects with periodontal diseases. Stroke 2005;36:1195-200.  Back to cited text no. 7
    
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Hujoel PP, Drangsholt M, Spiekerman C, DeRouen TA. Periodontitis-systemic disease associations in the presence of smoking – Causal or coincidental? Periodontol 2000 2002;30:51-60.  Back to cited text no. 8
    
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Genco RJ, Grossi SG, Ho A, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J Periodontol 2005;76 11 Suppl: 2075-84.  Back to cited text no. 9
    
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Herzberg MC, Weyer MW. Dental plaque, platelets, and cardiovascular diseases. Ann Periodontol 1998;3:151-60.  Back to cited text no. 10
    
11.
Qi M, Miyakawa H, Kuramitsu HK. Porphyromonas gingivalis induces murine macrophage foam cell formation. Microb Pathog 2003;35:259-67.  Back to cited text no. 11
    
12.
Bhupathy P, Haines CD, Leinwand LA. Influence of sex hormones and phytoestrogens on heart disease in men and women. Womens Health (Lond) 2010;6:77-95.  Back to cited text no. 12
    
13.
Paranjape SG, Turankar AV, Wakode SL, Dakhale GN. Estrogen protection against coronary heart disease: Are the relevant effects of estrogen mediated through its effects on uterus – such as the induction of menstruation, increased bleeding, and the facilitation of pregnancy? Med Hypotheses 2005;65:725-7.  Back to cited text no. 13
    
14.
D'Aiuto F, Parkar M, Andreou G, Suvan J, Brett PM, Ready D, et al. Periodontitis and systemic inflammation: Control of the local infection is associated with a reduction in serum inflammatory markers. J Dent Res 2004;83:156-60.  Back to cited text no. 14
    
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Katz J. Elevated blood glucose levels in patients with severe periodontal disease. J Clin Periodontol 2001;28:710-2.  Back to cited text no. 15
    
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Hayashida H, Kawasaki K, Yoshimura A, Kitamura M, Furugen R, Nakazato M, et al. Relationship between periodontal status and HbA1c in nondiabetics. J Public Health Dent 2009;69:204-6.  Back to cited text no. 16
    
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Iacopino AM, Cutler CW. Pathophysiological relationships between periodontitis and systemic disease: Recent concepts involving serum lipids. J Periodontol 2000;71:1375-84.  Back to cited text no. 17
    
18.
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.  Back to cited text no. 18
    
19.
Cairo F, Castellani S, Gori AM, Nieri M, Baldelli G, Abbate R, et al. Severe periodontitis in young adults is associated with sub-clinical atherosclerosis. J Clin Periodontol 2008;35:465-72.  Back to cited text no. 19
    
20.
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.  Back to cited text no. 20
    
21.
Chin UJ, Ji S, Lee SY, Ryu JJ, Lee JB, Shin C, et al. Relationship between tooth loss and carotid intima-media thickness in Korean adults. J Adv Prosthodont 2010;2:122-7.  Back to cited text no. 21
    
22.
Engebretson SP, Lamster IB, Elkind MS, Rundek T, Serman NJ, Demmer RT, et al. Radiographic measures of chronic periodontitis and carotid artery plaque. Stroke 2005;36:561-6.  Back to cited text no. 22
    
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Desvarieux M, Ryan T, Demmer Rundek T, Boden-Albala B. Periodontal microbiota and carotid intima-media thickness. The oral infections and vascular disease epidemiology study (INVEST). Circulation 2005;111:576-82.  Back to cited text no. 23
    
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Castillo R, Fields A, Qureshi G, Salciccioli L, Kassotis J, Lazar JM. Relationship between aortic atherosclerosis and dental loss in an inner-city population. Angiology 2009;60:346-50.  Back to cited text no. 24
    
25.
Amar S, Gokce N, Morgan S, Loukideli M, Van Dyke TE, Vita JA. Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammation. Arterioscler Thromb Vasc Biol 2003;23:1245-9.  Back to cited text no. 25
    
26.
Tonetti MS, D'Aiuto F, Nibali L, Donald A, Storry C, Parkar M, et al. Treatment of periodontitis and endothelial function. N Engl J Med 2007;356:911-20.  Back to cited text no. 26
    


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

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



 

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