141

Coronary Artery Disease and

Periodontal Disease: Is There a Link?
Suzan Abou-Raya, MD,* Amr Naeem, MD,* Hassan Abou-El Kheir, DMD,
†
Sheriff El Beltagy, MD,* Alexandria, Egypt

Background: Cardiovascular disease is the number one killer worldwide. The so-called classic
risk factors of coronary heart disease do not account for all of its clinical and epidemiological
features. Recent evidence suggests that certain infections, among them dental infections and
in particular periodontal disease, are involved in the pathogenesis of coronary artery disease.
Aim: To evaluate the association between periodontal disease and coronary artery disease.
Patients and Methods: Fifty patients referred for diagnostic coronary angiography were
assessed for periodontal disease. All patients underwent a thorough physical examination,
routine laboratory testing, cardiac evaluation and dental examination which included panto-
mography x-ray evaluation.
Results: Pantomography x-rays and coronary angiograms of the participants were scored
blindly by a dentist and cardiologists respectively. The association between periodontal disease
and coronary atheromatosis remained significant after adjustment for age, smoking, blood
lipids, body mass index, hypertension and the presence of diabetes.
Implications: Periodontal disease was still significantly associated after all the known risk
factors were accounted for. The implication here is that periodontal disease could be a
potential risk factor for heart disease by predisposing the individual to chronic low-grade infec-
tions. If so, then dental health becomes an important parameter for medical health.

Introduction
Coronary artery disease (CAD) is the number
one cause of morbidity and mortality world-
wide.’ Numerous epidemiological studies have
shown that several risk factors such as smoking,
hypertension, high levels of low density lipopro-
Angiology 53:141-148, 2002 tein (LDL), low levels of high-density lipoprotein
From the Department of Internal Medicine and Cardiology
Unit, Faculty of Medicine; and the ’Department of Oral
(HDL), diabetes mellitus, obesity, and age are
Medicine, Faculty of Dentistry, University of Alexandria, significant in the development of coronary
Alexandria, Egypt artery disease .2,3 However, these so-called clas-
Presented at the 47th Annual Meeting of the American College sic risk factors do not explain all of the clinical
of Angiology, Orlando, FL, October 29-November 3, 2000 and epidemiological features of coronary heart
Correspondence: Suzan Abou-Raya, MD, Department of disease. Although substantial gains have been
Internal Medicine and Cardiology Unit, Faculty of Medicine,
achieved through control or elimination of the
University of Alexandria, Alexandria, Egypt
©2002 Westminster Publications, Inc., 708 Glen Cove Avenue, established risk factors for CAD, it is important
Glen Head, NY 11545, USA to consider cumulative data that shows that ap-

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142

proximately half of all patients suffering a coro- (Matilla et al, 1989; De Stefano et al, 1993;
nary heart disease event have no readily appar- Joshipura et al, 1993; and Beck et al, 1996).28-31
ent risk factors. 4,5 The present study was designed to assess the as-
Basic science research indicates that inflam- sociation between periodontal disease and CAD.
mation and perhaps chronic infection may play
important roles in the pathogenesis of athero-
sclerosis and CAD.6-9 Pathological studies demon-
strate that atherosclerotic lesions are heavily in-
filtrated with cellular and inflammatory compo- Study Group
nents and that proinflammatory cytokines as well
as cellular adhesion molecules appear to be im- We studied 50 consecutive subjects referred to
portant in the early atherogenic process. 10-13 With the Main University Hospital of Alexandria for
regard to chronic infection, evidence of prior ex- coronary angiographic evaluation of chest pain
posure to Chlamydia pneumoniae, cytomegalo- suggestive of coronary heart disease. All individ-
virus, Helicobacter pylori, as well as a known pe- uals were interviewed, and data on hyperten-
riodontal pathogen, porphyromonas gingivalis, sion, smoking habits, and diabetes mellitus was
has been isolated from atherosclerotic obtained. The body mass index (defined as
plaques. 14-22 Furthermore, animal studies suggest weight/height2) was determined, and blood
that infection with cytomegalovirus and perhaps pressure measurements were recorded. All sub-
other agents can lead to endothelial lesions simi- jects underwent a physical examination and
lar to that of human atherosclerosis.23-24 Recent evaluations by radiography, electrocardiography,
evidence suggests that certain chronic infections and transthoracic echocardiography. Blood sam-
such as dental infections, in particular, periodon- ples were obtained, and total white blood cell
tal disease are involved in the pathogenesis of counts (WBC), serum total cholesterol and HDL
CAD. Periodontal disease, is one of the most com- concentrations, triglyceride levels, fibrinogen
mon diseases in humans, affecting 10% to 15% levels, erythrocyte sedimentation rates (ESR),
of all adults, and approximately one-third of all and serum C-reactive protein (CRP) concentra-
adults beyond the third decade of life.25 tions were determined.
Periodontitis, the leading cause of tooth loss in
adults, is a severe dental disorder involving in-
flammation and infection of the tissue and bone
that support teeth. Periodontal diseases are gen-
erally chronic in nature and can persist in the ab- Methods
sence of treatment. These diseases are the result
of exposure of the periodontium to dental Coronary Angiography
plaques, biofilms that accumulate on the teeth to
form bacterial masses containing up to 1 to 2 x Coronary angiography was performed using the
1011 bacteria/gram at or below the gingival mar- standard Judkin’s technique 32 with a femoral ap-
gin. Dental plaques are complex, with more than proach. Coronary injections were performed
400 bacterial species having been collectively iso- using multiple views, and images were recorded
lated from the plaques of patients with periodon- on Kodak film at a rate of 50 frames/s. Multiple
tal disease.25,26 Periodontal disease is believed to transverse projections of the right and left coro-
result from the action of various toxic products nary arteries were recorded. Cineangiograms
released from specific pathogenic subgingival were simultaneously digitally recorded. All an-

plaque bacteria as well as from the host respons- giograms were reviewed and interpreted by car-
es elicited against plaque bacteria and their prod- diologists without prior knowledge of the pa-
ucts. The inflammatory response may result in tient’s dental status. Analysis of coronary artery
gingival ulceration around the tooth that can stenosis was performed using the Jenkin’s et al
allow intact bacterial cells or their products, in- scoring system, the coronary atheromatosis score
cluding lipopolysaccharides, peptidoglycan frag- (CAS) .33 .

ments, and hydrolytic enzymes into the systemic

circulation.25-27 Dental Examination
Associations between poor dental health and
coronary heart disease have been observed in The dental examination, which was carried out
both cross-sectional and longitudinal studies blindly,included asystematic clinical and radio-

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 143

logical examination. Each subject underwent a Pearson correlation was used to study the degree
full-mouth periodontal examination, and dental of correlation between quantitative variables.
radiographs were taken. Periodontal disease was Multiple regression models were used to predict
assessed by gingival bleeding and recession, cal- factors significantly affecting the dependent fac-
culus (supra and/or subgingival), periodontal tor. (3) Graphical presentation: bar graph and
pocket depths, attachment levels, and loss of scatter diagram were used. The level of signifi-
teeth (missing teeth). Following this initial dental cance selected for this study was p equal to or
study, the pantomography index (PGI) was de- less than 0.05.
termined. This index consists of the sum of the
scores given to each patient according to the

severity of the dental disease.34 The index con-

sists of the sum of the numbers of periapical le-
sions, lesions caused by tertiary caries, vertical Results
bone pockets, lesions caused by pericoronitis, and
radiolucent areas at the furcation. The index The group consisted of fifty subjects, 78%
study
ranged from 0 to 10, increasing with the severity (n = 39) men and 22% (n =11) were
were
of the disease. women. The mean age of the subjects was 63.78

years, range 55 to 75. The mean body mass index

Laboratory Analyses (BMI) was 27.88 ±2.27, range 23.90-33.00.
Fifty-six percent (n 28) of the subjects were
=

Total serum cholesterol was determined by a smokers, 20% (n = 10) were diabetic, and 32%
semiautomated calorimetric method 3’ and tri- (n = 16) were hypertensive (Table I).
glyceride levels were determined by a semi- The CRP concentrations ranged be-
serum
automated fluorometric method.36 HDL was iso- tween 4 and 21/Lg/mL (the upper limit of the
lated from the serum by ultracentrifugation, and normal range [using ELISA] lies between 5 and 8
the concentration was determined. 31 WBC counts fLg/mL) with a mean of 11.26 ±3.94. The fib-
were determined on a Coulter Fn (Coulter Elec- rinogen levels ranged between 223 and 464
tronics) .38 Erythrocyte sedimentation rates were
measured using the Westergren method.39 Fib-
rinogen was assayed using the thrombin time test
(Fibri-Prest). 40,41 CRP determinations were done
using the enzyme-linked immunosorbent assay
(ELISA) method-(Eurogenetics CRP ELISA). 41 Table I. Demographics of study group.
The detection range by this method is between 5
and 8 ,ug/mL.

Statistical Analysis
Data wascollected, coded and transferred into a
specially designed format suitable for computer
feeding. To avoid error, checking and verification
processes were carried out after data entry.
Frequency analysis, crosstabulation, and manual
revision were all used to detect error.
The EPI INFO statistical program was utilized
for both data presentation and statistical analysis
of the results. The following statistical measures
were used: (1) Descriptive measures: Count, per-

centage, arithmetic mean, and standard devia-

tion, minimum and maximum. (2) Statistical
tests: Z test, Chi square, and Fisher exact test for
analysis of qualitative variables. Student t test,
paired t test, one-way analysis of variance
(F), and Scheffe’s test (for pair-wise compari-
son) were used for quantitative analysis. The

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144

280 mg/dL with a mean of 204.14 ±30.49. HDL

concentrations ranged between 30 and 68 mg/dL
Table II. Laboratory data. with a mean of 42.74 ±9.56. The triglyceride lev-
els ranged between 125 and 209 mg/dL with a
mean of 161.32 ± 15.94 (Table II).
Of the 50 subjects studied, 84% (n 42) had =

angiographically demonstrable CAD, of which 40

also had periodontal disease. The prevalence of
the various dental parameters are shown in Figure
1. The mean coronary atheromatosis score (CAS)
was 17.46 ± 13.83, range 0-42. The pantomogra-
phy index (PGI) mean was 4.60 ±3.23, range
0-10. Factors significantly correlating with the
CAS were utilized in the multiple logistic regres-
sion analysis. The CAS was positively correlated
to the PGI (r 0.4141, p < 0.003) (Figure 2). The
=

model used: CAS = 9.309 + 1.77 (PGI).

Age was positively correlated to the CAS (the
score used to measure the degree of coronary

artery stenosis) (r = 0.4030, p < 0.004), whereas

body mass index, smoking, diabetes, and hyper-
tension were not. CRP serum concentrations, fib-
rinogen levels, WBC counts, and erythrocyte
sedimentation rates were all positively correlat-
ed to the CAS: r = 0.6246, p < 0.000, r = 0.6243,
p < 0.006, r = 0.6243, p < 0.000, r = 0.4132,
p < 0.007, respectively, and also positively cor-
mg/dL with a mean of 380.32 ±69.68. The mean related to the PGI: r = 0.4132, p < 0.003,
WBC count was 8200 cells/mm3 ± 1108.78 with a r = 0.6805, p < 0.000, r = 0.4385, p < 0.005,
range of 4800-9000 cells/mm3. The mean values r = 0.4311, p < 0.006, respectively. Risk analy-
for the erythrocyte sedimentation rate for the first sis, using the odds ratio (OR) showed that peri-
hour and the second hour were 28.85 ±5.98 and odontitis (PGI) proved to be a significant risk
37.24 ±8.91, respectively. The serum total cho- factor for coronary artery disease (CAS).
lesterol concentrations ranged between 144 and OR = 9.5, 1.69-53.42.

Figure 1. Relation between dental variables and coronary artery disease (CAS).
GB gingival bleeding, PGI pantomography index.
= =

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 145

Figure 2. Relationship between coronary atheromatosis score and

pantomography index.

Discussion parameter, namely missing teeth (expressing sus-

tained oral infections) showed a significant asso-
This study demonstrates an association between ciation with ischemic heart disease.
periodontal disease and CAD. Our results show Traditional risk factors (except for age which
that periodontitis is associated with a 9.5-fold in- was positively associated with coronary athero-
creased risk of CAD independent of the tradition- matosis), such as smoking, hypertension, total
al risk factors. cholesterol and HDL concentrations, triglyceride
In this study, periodontal disease was as- levels, and diabetes, were not significant predic-
sessed radiologically, based on radiographs of tors of CAD when included in our model that con-
the teeth and jaws (called the pantomography tained dental variables.
index) and clinically by oral health parameters Significant elevations in the CRP serum con-
including gingival bleeding (bleeding on probe), centrations, fibrinogen levels, WBC counts, and
supragingival, and/or subgingival calculus, erythrocyte sedimentation rates were found in
probing depths > 4 mm, loss of attachment > 4 both individuals with periodontal disease and in
mm (indication of alveolar bone loss), and miss- those with angiographically demonstrable CAD.
ing teeth (an indirect indicator of periodontal The CRP serum concentrations, fibrinogen levels,
disease). Of the 50 subjects recruited in this white blood cell count, and erythrocyte sedimen-
study, 42 (84%) had angiographically demon- tation rates were positively correlated to both the
strable CAD and were given a score (the CAS CAS (indicating CAD) and to the pantomography
[Jenkins score]) according to the degree of coro- index (indicating periodontal disease). Elevations
nary artery stenosis. Forty of the 42 patients of these acute phase reactants presumably reflect
with CAD were simultaneously found to have the chronic nature of these diseases.
periodontal disease. Our findings are in accordance with a number
The oral parameters in our study group were of studies. Kweider et a145 (1993) showed that pe-
independent of and more strongly associated with riodontal patients had significantly higher levels
CAD than were recognized risk factors. These re- of fibrinogen and WBC counts when compared
sults are in agreement with previous data by with periodontally healthy subjects. Yarnell et a146
Matilla et al .43 However, in this study, age re- (Caerphilly and Speedwell Collaborative Heart
mained a significant predictor of CAD (age was Disease Study) showed that fibrinogen levels, vis-
positively correlated with the CAS). In yet anoth- cosity, and WBC count were all higher in individ-
er study by Paunio et al, 44 a single dental health uals who developed ischemic heart disease and

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146

concluded that jointly they constituted important our study group; and, since studied have shown
risk factors for coronary heart disease. In another that elevated fibrinogen and WBC are strong pre-
study, Gillum et al47 showed that relative risk for dictors of CAD, they could be the link between
coronary heart disease increased with a WBC periodontal disease and CAD. However, because
> 8100 cells/mm3. of the convenience sample studied, our findings
It has been suggested that because elevated cannot be generalized to other populations, and
fibrinogen and white blood cells are strong pre- thus a cause and effect relationship cannot be es-
dictors of coronary heart disease,48 they could be tablished.
the link between periodontal disease and CAD.
The two inflammatory markers and acute Implications
phase reactants, CRP and fibrinogen, were highly
associated with both periodontal disease and CAD It is increasingly difficult to ignore the possibility
in our study group. CRP, a marker of underlying that infection and, in particular, periodontal dis-
systemic inflammation and infective agents has ease, may be a novel cardiovascular risk factor. If
been shown to be associated with CAD. Anderson so, then dental health becomes an important pa-
et a149 (1998-JACC) confirm the association of el- rameter of medical health. The implications be-
evated CRP levels to patients with coronary ath- come particularly pertinent to the elderly popula-
erosclerosis (angiographically documented). tion. The proportion and therefore absolute num-
In the October 19, 2000 issue of the New ber of elderly individuals is increasing. People are
England Journal of Medicine, 2 reports, 1 by living longer, and adults are retaining more of
Lindahl et al and the other by Packard et al their teeth into old age (studies have reported
showed that levels of CRP and fibrinogen were that the elderly place significant importance on
predictive of the risk of coronary events.5o the role of oral health as a necessary condition
Evidence from this study as well as other studies for good quality of life). But with the current
confirms an association between periodontal dis- trends of increasing tooth retention in aging pop-
ease and CAD, especially so with increasing age. ulations, there is a corresponding greater risk of
The biological mechanism by which periodontal periodontal disease with a chronic bacteremic
disease could lead to coronary heart disease is not burden and increased acute phase reactants, in-
clearly established, but a plausible mechanism creased fibrinogen levels, and increased WBC
linking the 2 conditions would probably involve counts (both of which increase the risk of coro-
the interaction between bacterial products, in par- nary heart disease). Furthermore, coronary heart
ticular, lipopolysaccharides (LPS) and heat shock disease is the number one killer of the elderly.
proteins-60 (HSP-60), and hemostatic mecha- It is thus high time that physicians, in partic-
nisms. Individuals with periodontal disease have ular cardiologists and dentists, develop height-
higher plasma fibrinogen levels (probably stimu- ened awareness of the increasing evidence that
lated by inflammation) as well as higher WBC has come to the surface linking periodontal dis-
counts.45 Such increases in fibrinogen and WBC ease to CAD. In addition, the public should be en-
counts promote atherosclerosis and thrombosis, lightened about the association between peri-
which will lead to coronary heart disease. In ad- odontal disease and CAD and should be motivat-
dition, an interaction between specific bacteria in ed to maintain good dental health, to be prompt
plaque (streptococcus sanguis) and platelets leads with dental checkups, and to maintain good oral
to platelet aggregation.51 hygiene through regular brushing, flossing, and
use of oral antiseptics. It is important to remem-
ber that periodontal disease, if considered a risk
factor of CAD, is a &dquo;modifiable risk factor&dquo; and
’
amenable to treatment.
Conclusions .

Evidence from this and other studies confirms an

association between periodontal disease and
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