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.

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

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142
proximately half of all patients suffering a coro-
nary heart disease event have no readily appar-
ent risk factors. 4,5
Basic science research indicates that inflam-
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-
nents and that proinflammatory cytokines as well
as cellular adhesion molecules appear to be im-
portant in the early atherogenic process. 10-13 With
regard to chronic infection, evidence of prior ex-
posure to Chlamydia pneumoniae, cytomegalo-
virus, Helicobacter pylori, as well as a known pe-
riodontal pathogen, porphyromonas gingivalis,
has been isolated from atherosclerotic
plaques. 14-22 Furthermore, animal studies suggest
that infection with cytomegalovirus and perhaps
other agents can lead to endothelial lesions simi-
lar to that of human atherosclerosis.23-24 Recent
evidence suggests that certain chronic infections
such as dental infections, in particular, periodon-
tal disease are involved in the pathogenesis of
CAD. Periodontal disease, is one of the most com-
mon diseases in humans, affecting 10% to 15%
of all adults, and approximately one-third of all
adults beyond the third decade of life.25
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-
sence of treatment. These diseases are the result
of exposure of the periodontium to dental
plaques, biofilms that accumulate on the teeth to
form bacterial masses containing up to 1 to 2 x
1011 bacteria/gram at or below the gingival mar-
gin. Dental plaques are complex, with more than
400 bacterial species having been collectively iso-
lated from the plaques of patients with periodon-
tal disease.25,26 Periodontal disease is believed to
result from the action of various toxic products
released from specific pathogenic subgingival
plaque bacteria as well as from the host respons-
es elicited against plaque bacteria and their prod-
ucts. The inflammatory response may result in
gingival ulceration around the tooth that can
allow intact bacterial cells or their products, in-
cluding lipopolysaccharides, peptidoglycan frag-
ments, and hydrolytic enzymes into the systemic
circulation.25-27
Associations between poor dental health and
coronary heart disease have been observed in
both cross-sectional and longitudinal studies
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(Matilla et al, 1989; De Stefano et al, 1993;
Joshipura et al, 1993; and Beck et al, 1996).28-31
The present study was designed to assess the as-
sociation between periodontal disease and CAD.
Study Group
We studied 50 consecutive subjects referred to
the Main University Hospital of Alexandria for
coronary angiographic evaluation of chest pain
suggestive of coronary heart disease. All individ-
uals were interviewed, and data on hyperten-
sion, smoking habits, and diabetes mellitus was
obtained. The body mass index (defined as
weight/height2) was determined, and blood
pressure measurements were recorded. All sub-
jects underwent a physical examination and
evaluations by radiography, electrocardiography,
and transthoracic echocardiography. Blood sam-
ples were obtained, and total white blood cell
counts (WBC), serum total cholesterol and HDL
concentrations, triglyceride levels, fibrinogen
levels, erythrocyte sedimentation rates (ESR),
and serum C-reactive protein (CRP) concentra-
tions were determined.
Methods
Coronary Angiography
Coronary angiography was performed using the
standard Judkin’s technique 32 with a femoral ap-
proach. Coronary injections were performed
using multiple views, and images were recorded
on Kodak film at a rate of 50 frames/s. Multiple
transverse projections of the right and left coro-
nary arteries were recorded. Cineangiograms
were simultaneously digitally recorded. All an-
giograms were reviewed and interpreted by car-
diologists without prior knowledge of the pa-
tient’s dental status. Analysis of coronary artery
stenosis was performed using the Jenkin’s et al
scoring system, the coronary atheromatosis score
(CAS) .33 .
Dental Examination
The dental examination, which was carried out
blindly,included asystematic clinical and radio-
 143

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

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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Figure 2. Relationship between coronary atheromatosis score and
pantomography index.
Discussion
This study demonstrates an association between
periodontal disease and CAD. Our results show
that periodontitis is associated with a 9.5-fold in-
creased risk of CAD independent of the tradition-
al risk factors.
In this study, periodontal disease was as-
sessed radiologically, based on radiographs of
the teeth and jaws (called the pantomography
index) and clinically by oral health parameters
including gingival bleeding (bleeding on probe),
supragingival, and/or subgingival calculus,
probing depths > 4 mm, loss of attachment > 4
mm (indication of alveolar bone loss), and miss-
ing teeth (an indirect indicator of periodontal
disease). Of the 50 subjects recruited in this
study, 42 (84%) had angiographically demon-
strable CAD and were given a score (the CAS
[Jenkins score]) according to the degree of coro-
nary artery stenosis. Forty of the 42 patients
with CAD were simultaneously found to have
periodontal disease.
The oral parameters in our study group were
independent of and more strongly associated with
CAD than were recognized risk factors. These re-
sults are in agreement with previous data by
Matilla et al .43 However, in this study, age re-
mained a significant predictor of CAD (age was
positively correlated with the CAS). In yet anoth-
er study by Paunio et al, 44 a single dental health
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145
parameter, namely missing teeth (expressing sus-
tained oral infections) showed a significant asso-
ciation with ischemic heart disease.
Traditional risk factors (except for age which
was positively associated with coronary athero-
matosis), such as smoking, hypertension, total
cholesterol and HDL concentrations, triglyceride
levels, and diabetes, were not significant predic-
tors of CAD when included in our model that con-
tained dental variables.
Significant elevations in the CRP serum con-
centrations, fibrinogen levels, WBC counts, and
erythrocyte sedimentation rates were found in
both individuals with periodontal disease and in
those with angiographically demonstrable CAD.
The CRP serum concentrations, fibrinogen levels,
white blood cell count, and erythrocyte sedimen-
tation rates were positively correlated to both the
CAS (indicating CAD) and to the pantomography
index (indicating periodontal disease). Elevations
of these acute phase reactants presumably reflect
the chronic nature of these diseases.
Our findings are in accordance with a number
of studies. Kweider et a145 (1993) showed that pe-
riodontal patients had significantly higher levels
of fibrinogen and WBC counts when compared
with periodontally healthy subjects. Yarnell et a146
(Caerphilly and Speedwell Collaborative Heart
Disease Study) showed that fibrinogen levels, vis-
cosity, and WBC count were all higher in individ-
uals who developed ischemic heart disease and
146
concluded that jointly they constituted important
risk factors for coronary heart disease. In another
study, Gillum et al47 showed that relative risk for
coronary heart disease increased with a WBC
> 8100 cells/mm3.
It has been suggested that because elevated
fibrinogen and white blood cells are strong pre-
dictors of coronary heart disease,48 they could be
the link between periodontal disease and CAD.
The two inflammatory markers and acute
phase reactants, CRP and fibrinogen, were highly
associated with both periodontal disease and CAD
in our study group. CRP, a marker of underlying
systemic inflammation and infective agents has
been shown to be associated with CAD. Anderson
et a149 (1998-JACC) confirm the association of el-
evated CRP levels to patients with coronary ath-
erosclerosis (angiographically documented).
In the October 19, 2000 issue of the New
England Journal of Medicine, 2 reports, 1 by
Lindahl et al and the other by Packard et al
showed that levels of CRP and fibrinogen were
predictive of the risk of coronary events.5o
Evidence from this study as well as other studies
confirms an association between periodontal dis-
ease and CAD, especially so with increasing age.
The biological mechanism by which periodontal
disease could lead to coronary heart disease is not
clearly established, but a plausible mechanism
linking the 2 conditions would probably involve
the interaction between bacterial products, in par-
ticular, lipopolysaccharides (LPS) and heat shock
proteins-60 (HSP-60), and hemostatic mecha-
nisms. Individuals with periodontal disease have
higher plasma fibrinogen levels (probably stimu-
lated by inflammation) as well as higher WBC
counts.45 Such increases in fibrinogen and WBC
counts promote atherosclerosis and thrombosis,
which will lead to coronary heart disease. In ad-
dition, an interaction between specific bacteria in
plaque (streptococcus sanguis) and platelets leads
to platelet aggregation.51
’
Conclusions
Evidence from this and other studies confirms an
association between periodontal disease and
CAD. Periodontal disease proved to be a signifi-
cant risk factor for coronary atherosclerosis
(OR = 9.5 ; 1.69-53.42). The inflammatory mark-
ers and acute phase reactants CRP, fibrinogen,
and WBC counts were significantly elevated in
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our study group; and, since studied have shown
that elevated fibrinogen and WBC are strong pre-
dictors of CAD, they could be the link between
periodontal disease and CAD. However, because
of the convenience sample studied, our findings
cannot be generalized to other populations, and
thus a cause and effect relationship cannot be es-
tablished.
Implications
It is increasingly difficult to ignore the possibility
that infection and, in particular, periodontal dis-
ease, may be a novel cardiovascular risk factor. If
so, then dental health becomes an important pa-
rameter of medical health. The implications be-
come particularly pertinent to the elderly popula-
tion. The proportion and therefore absolute num-
ber of elderly individuals is increasing. People are
living longer, and adults are retaining more of
their teeth into old age (studies have reported
that the elderly place significant importance on
the role of oral health as a necessary condition
for good quality of life). But with the current
trends of increasing tooth retention in aging pop-
ulations, there is a corresponding greater risk of
periodontal disease with a chronic bacteremic
burden and increased acute phase reactants, in-
creased fibrinogen levels, and increased WBC
counts (both of which increase the risk of coro-
nary heart disease). Furthermore, coronary heart
disease is the number one killer of the elderly.
It is thus high time that physicians, in partic-
ular cardiologists and dentists, develop height-
ened awareness of the increasing evidence that
has come to the surface linking periodontal dis-
ease to CAD. In addition, the public should be en-
lightened about the association between peri-
odontal disease and CAD and should be motivat-
ed to maintain good dental health, to be prompt
with dental checkups, and to maintain good oral
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.
.
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