Correlation between the severity of periodontitis and

coronary artery stenosis in a Chinese population

J Yang,* L Feng,* J Ren,* G Wu, S Chen,* Q Zhou,* Z Du, S Zhang,* C Hu,
X Wu, L Ling
*Department of Stomatology, First Afliated Hospital of Sun Yat-sen University, China.
Department of Cardiovascular Medicine, First Afliated Hospital of Sun Yat-sen University, China.
Department of Medical Statistics and Epidemiology, School of Public Health, Sun Yat-sen University, China.
ABSTRACT
Background: The aim of this study was to evaluate the relationship between the severity of periodontitis and the extent
and degree of coronary artery stenosis in a Chinese population.
Methods: Patients (n = 853) with coronary artery stenosis conrmed by coronary angiography were eligible to take part
in the study. Only subjects that were 60 years old, had 50% stenosis in at least one coronary artery, and did not have
diabetes or a history of smoking were included (n = 115). After periodontal examination, including bleeding index, prob-
ing depth calculus index, plaque index and periodontal attachment loss, four groups were dened based on the severity
of periodontitis: no periodontitis/gingivitis (M0, n = 19); mild periodontitis (M1, n = 27); moderate periodontitis (M2,
n = 31); and severe periodontitis (M3, n = 38). The extent and degree of coronary artery stenosis was obtained by calcu-
lating the Gensini score (GS).
Results: The GS was signicantly greater in the M3 group compared with the M0 group. Multiple linear regression anal-
ysis revealed that probing depth and plaque index were signicantly correlated with the GS.
Conclusions: The extent and severity of coronary artery stenosis in Chinese patients 60 years old is positively correlated
with the severity of periodontitis.
Keywords: Coronary artery disease, periodontitis, coronary artery stenosis, Gensini score, clinical attachment loss.
Abbreviations and acronyms: BI = bleeding index; CAG = coronary angiography; CAL = clinical attachment loss; CHD = coronary
heart disease; CI = calculus index; GS = Gensini score; HDL-C = high density lipoprotein cholesterol; LAD = left anterior descending;
LDL-C = low density lipoprotein cholesterol; PB = probing depth; PLI = plaque index.
(Accepted for publication 12 October 2012.)
INTRODUCTION
Coronary heart disease (CHD) is a life-threatening
disease that has a serious impact on physical and
emotional well-being. CHD is also one of the major
causes of death worldwide. In-depth studies on the
aetiology, pathogenesis and clinical treatment of CHD
have identied other important pathogenic factors in
addition to the traditional risk factors of smoking,
hypertension, diabetes and dyslipidaemia.
1
Since the
1990s, researchers have provided evidence that infec-
tion is one of the risk factors for atherosclerosis and
thrombus formation and that systemic inammation
due to infection promotes and accelerates the initia-
tion and progression of atherosclerosis.
25
There are several similarities between CHD and peri-
odontitis. In particular, infection and inammation are
common mechanisms in both diseases.
6,7
Periodontitis is
one of the main causes of tooth loss in humans. Recur-
rent infection of the periodontium results in higher lev-
els of inammatory factors in the serum. As the severity
of periodontitis increases, there is a greater systemic
inammatory response.
810
Previous studies showed that
periodontitis leads to atherosclerosis through periodon-
tal pathogens and their by-products, or through the
release of inammatory mediators from periodontal tis-
sue that induce endothelial dysfunction.
11,12
Pathologi-
cal studies of atherosclerotic plaques have identied the
presence of periodontal pathogens.
13,14
Although not all studies have shown a signicant
association between periodontitis and CHD,
15
the
majority of studies, as summarized in a meta-analysis
by Bahekar et al.,
16
demonstrated a signicant associ-
ation between periodontal disease and CHD even
after adjusting for traditional risk factors such as
smoking, blood lipids, race, gender and obesity.
2013 Australian Dental Association 333
Australian Dental Journal 2013; 58: 333338
doi: 10.1111/adj.12087
Australian Dental Journal
The ofcial journal of the Australian Dental Association
A limitation of previous studies that investigated the
relationship between periodontal disease and CHD
was that the denition of periodontitis was highly vari-
able and not always based on a clinical examination.
Furthermore, the denition of CHD was variable, and
the presence of coronary artery occlusion or stenosis
was not always documented by coronary angiography
(CAG). Only a few studies have examined the relation-
ship between periodontitis and the presence of CHD
assessed by CAG.
1720
Although the results of these
studies suggested that there was a positive association
between periodontitis and coronary arterial stenosis,
these studies did not assess the severity and extent of
stenosis throughout the entire coronary arterial tree.
Because of limitations in the denitions of periodontitis
and CHD in previous studies, we performed a retro-
spective analysis to systemically evaluate the relation-
ship between periodontitis and CHD in a Chinese
population with coronary stenosis (50%) documented
by CAG. We used a standardized scoring method, the
Gensini method,
21
to evaluate the extent and severity
of coronary artery stenosis throughout the entire coro-
nary arterial tree. In addition, a standardized grading
method, the Armitage method,
22
was used to grade the
severity of periodontitis.
MATERIALS AND METHODS
Subjects
There were 853 patients with CHD disease who were
admitted to our hospital from January 2011 to Febru-
ary 2012 that were eligible for the study. The study
was approved by the medical ethics committee at the
First Afliated Hospital of Sun Yat-sen University. All
examinations were acknowledged and consented by
the patients, and consent forms were signed.
All patients that were included in the study met the
following inclusion criteria: age 60 years old, steno-
sis >50% in at least one branch of a major coronary
artery conrmed by CAG, and at least 14 natural
teeth in full denture. Patients were excluded if they
met any of the following criteria: periodontal treat-
ment; antibiotic administration, or medications induc-
ing gingival overgrowth within six months of the
study; pregnancy; a history of smoking or alcoholism;
acute cerebrovascular disease, peripheral vascular dis-
ease or severe infection; systemic diseases including
diabetes, respiratory diseases, malignant tumours, or
liver or kidney dysfunction.
Study design
Although the study design was retrospective, the peri-
odontal examiners had no previous knowledge of the
coronary angiography results, and the physicians that
interpreted the coronary angiograms had no informa-
tion about the patients periodontal condition. All
subjects completed a questionnaire for general infor-
mation, that included gender, age, height, family his-
tory of periodontitis, history of smoking, blood
pressure, the degree of stenosis by coronary angiogra-
phy, history of systemic disease, triglycerides, total
serum cholesterol, high density lipoprotein cholesterol
(HDL-C), low density lipoprotein cholesterol (LDL-C),
and habit and status of oral hygiene (number, time
and method of daily toothbrushing, bleeding condi-
tions and regularity of oral examinations).
Diagnosis of CHD
CHD was diagnosed by CAG using Judkins tech-
nique with projections in multiple views. All angio-
grams were evaluated by experienced physicians from
visual assessment, and the degree of coronary stenosis
was determined. The extent and severity of coronary
artery stenosis was based on the Gensini score (GS).
21
To obtain the GS, the coronary arterial tree was
divided into 14 segments, and the degree of stenosis
evaluated in each segment. A score of 1 was given for
125% stenosis, 2 for 2650% stenosis, 4 for
5175% stenosis, 8 for 7690% stenosis, 16 for
9199% and 32 for total occlusion. The score of each
segment was then multiplied by a weighting factor
that represented the importance of a lesion in that
segment. The weighting factor was 5 for a left main
lesion; 2.5 for a proximal left anterior descending
(LAD) or left circumex (LCx) lesion; 1.5 for a mid-
segment LAD or LCx lesion, 1 for a lesion in the
distal LAD, LCx, rst diagonal branch, rst obtuse
marginal branch, right coronary artery, posterior
descending artery or septal artery; and 0.5 for a lesion
in the second diagonal or obtuse marginal branches.
The products in each of the 14 segments were then
summed to obtain the nal GS. The GS values ranged
from 2 to 190. A higher GS score indicated a greater
extent and severity of coronary stenosis.
Diagnosis of periodontitis
According to the diagnostic standard from Armit-
age,
22
the grouping of periodontitis severity was based
on clinical attachment loss (CAL) to determine sever-
ity. In the group with no periodontitis/gingivitis (M0),
the average CAL was 0.5 mm, the number of loci
(with proximal CAL 3 mm) was zero and the num-
ber of teeth lost was 2 (excluding the third molar,
orthodontic teeth, tooth extraction due to trauma or
injury, tooth loss due to severe caries and congenital
tooth loss). In the group with mild periodontitis (M1),
the average CAL 0.6 mm but 1.5 mm, the number
of loci (with proximal CAL 3 mm) was zero, and
334 2013 Australian Dental Association
J Yang et al.
the number of teeth lost was 3. In the moderate peri-
odontitis group (M2), the average CAL was 1.6 but
2.4 mm, loci (with proximal CAL 3 mm) were dis-
tributed in three different areas or the total number
was 6 and the number of teeth lost was 5. In the
severe periodontitis group (M3), the average CAL was
2.5 mm, loci (with proximal CAL 5 mm) were dis-
tributed in three to four different areas and the num-
ber of teeth lost was 14. All patients received an oral
examination by the same physician with a Hu-Friedy
periodontal probe. The complete intercuspal position
was examined, and six loci were probed in each tooth
(buccal surface, and the distal, central and proximal
lingual surfaces of the tooth) for the examination of
CAL, probing depth (PD), bleeding index (BI), calcu-
lus index (CI) and plaque index (PLI). The average
values of individual indexes were used as the corre-
sponding values for each patient.
Blood sampling and assays
On the morning (67 am) of the second day of hospital-
ization, a blood sample was collected by drawing 3 ml
of fasting venous blood. After storing at low tempera-
ture for 1 hour, the blood sample was delivered to the
medical laboratory at the First Afliated Hospital of
Sun Yat-sen University. The blood sample was centri-
fuged at 3600 rpm for 5 minutes (KDL-1044, USTC
Chuangxin Co. Ltd., Zonkia Branch, China). Total cho-
lesterol and triglycerides was determined with ELISA
kits, whereas HDL-C and LDL-C were detected by the
direct method. Normal ranges of blood lipid were as
follows: total cholesterol, 3.105.18 mmol/L; triglyce-
rides 0.331.7 mmol/L; HDL-C, 1.091.63 mmol/L;
and LDL-C, 1.943.61 mmol/L.
Statistical analysis
All statistical analyses were performed using SAS 9.2
(SAS Institute Inc., Cary, NC, USA). Continuous vari-
ables were expressed as mean SD; categorical vari-
ables were presented as the number (percentage) of
patients. The Chi-square test was used to detect any
difference in severity of periodontitis; the Mann
Whitney U test was used to detect any difference in
age, total cholesterol, triglyceride, HDL-C, LDL-C,
BMI, GS, CAL, PD, BI, CI, and PLI among the male
and female groups. The KruskalWallis test was used
to detect any difference among M0, M1, M2 and M3
groups, and when a signicant difference was
detected, the MannWhitney U test and Bonferroni
adjustment of critical p-values were used for between-
group comparisons. Multiple linear regression analysis
was used to examine the correlations between the GS
and CAL, PD, BI, CI and PLI. The signicance level a
was set at 0.05.
RESULTS
Patient demographic characteristics are shown in
Table 1. A total of 115 patients with CHD were
included in this study; 82 males and 33 females. There
were 19 patients in the M0 group, 27 in the M1
group, 31 in the M2 group and 38 in the M3 group.
The total cholesterol, triglycerides, HDL-C and LDL-C
were in the normal range in all patients. The demo-
graphic characteristics of the M0, M1, M2 and M3
groups are shown in Table 2. The four groups were
similar with respect to age, total cholesterol, triglycer-
ide, LDL-C and BMI (all p > 0.05). Compared with
the M0 group, the M1 and M3 groups had lower
HDL-C, although the values were still within the nor-
mal range. The GS was signicantly greater in the M3
group compared with that in M0 group. For the sever-
ity of periodontitis, the M1, M2 and M3 groups had
signicantly increased CAL and CI compared with the
M0 group. Furthermore, compared with the M1
group, the M2 and M3 groups had signicantly
increased CAL and the M3 group had a signicantly
increased CI. In addition, the M3 group had signi-
cantly increased CAL and CI compared with the M2
group. The PD, BI and PLI were signicantly higher in
the M2 and M3 groups compared with the M0 group,
and the BI in the M3 group showed a signicant
increase compared with that in the M1 group. The GS
among all the patients stratied according to the sever-
ity of periodontitis is shown in Fig. 1.
The correlation between the severity of CHD and
CAL, PD, BI, CI and PLI are shown in Table 3. Mul-
tiple regression analysis revealed that PD and PLI
were signicantly correlated with the GS. After adjust-
ing for CAL, PD, BI, CI and PLI, an increase in PD of
Table 1. Clinical characteristics
Variable Mean SD
Age (years) 65.0 3.6
Total cholesterol (mmol/l) 4.2 1.1
Triglyceride (mmol/l) 1.5 0.9
HDL-C (mmol/l) 1.1 0.3
LDL-C (mmol/l) 2.7 1.2
BMI (kg/m
2
) 23.8 4.0
Gender, n (%)
Male 82 (71.3%)
Female 33 (28.7%)
Severity of periodontitis, n (%)
M0 19 (16.5%)
M1 27 (23.5%)
M2 31 (27.0%)
M3 38 (33.0%)
Continuous variables are presented as mean standard deviation;
categorical variables are presented as number (percentage).
HDL-C = high density lipoprotein cholesterol; LDL-C = low density
lipoprotein cholesterol; GS = Gensini score; CAL = clinical attach-
ment loss; PD = probing depth; BI = bleeding index; CI = calculus
index; PLI = plaque index.
2013 Australian Dental Association 335
Periodontitis correlated to coronary heart disease
1 unit was associated with an increase in the GS of
0.62 points. Furthermore, an increase in PLI of 1 unit
was associated with an increase in the GS of 0.57
points.
DISCUSSION
This is the rst study that combined the Armitage
method for the evaluation of periodontitis with the
Gensini scoring system to assess the extent and sever-
ity of CHD. The results showed that the GS was sig-
nicantly higher in the M3 group with the most
severe periodontitis compared with the M0 group
with no peridontitis/gingivitis. Furthermore, multiple
linear regression analysis using all patients showed
that PD and PLI were positively correlated with the
GS. These results indicate that periodontitis might be
an independent risk factor for the severity of CHD.
An important aspect of the present study was that
it was conducted in a relatively homogenous popula-
tion. All patients were 60 years old and patients
with risk factors common for both periodontitis and
CHD such as smoking and diabetes were excluded as
these factors might confound the relationship between
periodontitis and CHD.
16,23
Furthermore, the Armit-
age method was used to classify the results of the
periodontal examination. Full-denture teeth were
examined, and six loci were taken for each tooth.
These approaches avoided data loss and selection
bias.
The Armitage method employs CAL as the index of
the severity of periodontitis. Although previous studies
have used CAL to dene peridontitis, other studies
have used pocket (probing) depth. There is a lack of
consensus on the best denition.
24
When patients in
the present study were stratied into four groups
using the Armitage method to dene the severity of
periodontitis, the M3 group with the most severe peri-
odontitis had a signicantly higher GS than the M0
group with no periodontitis/gingivitis. However, in
Table 2. Clinical characteristics among all patients stratied according to the severity of periodontitis
Variable M0 (n = 19) M1 (n = 27) M2 (n = 31) M3 (n = 38) p-value
Age (years) 64.2 3.1 64.4 3.3 64.5 3.2 66.1 4.0 0.171
Total cholesterol (mmol/l) 4.3 1.2 4.1 0.8 4.2 1.1 4.1 1.2 0.585
Triglyceride (mmol/l) 1.8 1.4 1.5 0.8 1.6 1.0 1.4 0.6 0.924
HDL-C (mmol/l) 1.2 0.2 1.0 0.2* 1.1 0.2 1.1 0.4* 0.004
LDL-C (mmol/l) 2.6 0.8 2.7 0.8 2.6 1.0 2.9 1.8 0.998
BMI (kg/m
2
) 22.9 6.3 24.8 4.2 23.2 3.3 24.1 2.5 0.552
GS 10.9 12.8 15.2 17.8 31.2 35.0 36.0 36.7* 0.006
Periodontitis Index
CAL 0.5 0.2 1.2 0.2* 2.0 0.2* 3.1 0.3* <0.0001
PD 2.8 0.3 3.2 0.5 3.3 0.7* 3.7 0.8* <0.0001
BI 1.2 0.7 1.6 0.6 1.9 0.6* 2.2 0.7* <0.0001
CI 0.8 0.5 1.7 1.0* 1.9 0.7* 2.6 0.8* <0.0001
PLI 1.6 1.0 2.3 0.9 2.5 0.5* 2.7 0.5* <0.0001
Data are presented as mean standard deviation and were tested by the KruskalWallis test; the MannWhitney U test and Bonferroni adjust-
ment of critical p-values were used for multiple comparisons.
Signicant difference among the four periodontitis groups.
*Signicant difference between M0 and M1/M2/M3.
Signicant difference between M1 and M2/M3.
Signicant difference between M2 and M3.
HDL-C = high density lipoprotein cholesterol; LDL-C = low density lipoprotein cholesterol; GS = Gensini score; CAL = clinical attachment
loss; PD = probing depth; BI = bleeding index; CI = calculus index; PLI = plaque index.
M0
G
e
n
s
i
n
i

s
c
o
r
e
0
20
40
60
80
100
120
140
160
M1 M2 M3
Fig. 1 Gensini score among all the patients stratied according to the
severity of periodontitis.
Table 3. Multiple regression analysis for the
association between the Gensini score and severity of
periodontitis
Variable Regression coefcient Standard error p-value
Intercept 0.82 0.72 0.259
CAL 0.19 0.17 0.280
PD 0.62 0.19 0.002
BI 0.33 0.22 0.129
CI 0.02 0.22 0.945
PLI 0.57 0.25 0.024
CAL = clinical attachment loss; PD = probing depth; BI = bleeding
index; CI = calculus index; PLI = plaque index.
336 2013 Australian Dental Association
J Yang et al.
multivariate linear regression analysis, the average
CAL was not correlated with the GS (p = 0.28). Only
the PD and PLI were correlated with the GS.
Although the mechanism for this is not clear, there
may have been complex relationships among these
three variables that were important in the multivariate
regression model.
A major strength of this study was that the degree
of coronary artery stenosis was assessed in 14 differ-
ent segments of the coronary arterial tree using CAG.
The Gensini scoring system assigned different weight-
ing factors to the 14 segments and generated a single
score that reected the overall extent and severity of
coronary stenosis in each patient. Although other
studies have used CAG to document the presence of
coronary artery stenosis in patients with periodonti-
tis,
1720
our study is the rst to show a relationship
between the extent and severity of coronary stenosis
throughout the coronary arterial tree and the severity
of periodontitis.
An interesting nding in the present study was that
17% of patients with CHD documented by CAG had
no periodontitis/gingivitis. Furthermore, the GS in this
group (M0) was not signicantly different from that
in the M1 group with mild periodontitis. These results
indicate that there are multiple factors that lead to
CHD and this may well account for the lack of a
strong association between periodontitis and CHD
that has been observed in some previous studies.
16
Alternatively, our results may have been inuenced by
the inclusion/exclusion criteria used in the study and
the analytical methods.
An important variable that was not controlled in
the present was gender. When regression analysis was
conducted separately in each gender, there was no sig-
nicant association between the severity of periodonti-
tis and CHD (data not shown). This may well have
been due to the reduction in statistical power due to a
decrease in sample size. It is possible that gender has
an inuence on the association between periodontitis
and CHD, but this will need to be evaluated in a lar-
ger population.
The results of our study indicated that periodontitis
might be an independent risk factor for CHD in the
population 60 years old. Persson et al.
25
showed a
correlation between alveolar bone loss (assessed by
radiography) and calcium accumulation in the carotid
arterial wall in 1064 subjects that ranged in age from
6075 years old. The same study also showed that
alveolar bone loss was associated with a self-reported
history of heart attack. Thus, the results of our study
tend to conrm these previous ndings that there is
an important association between periodontitis and
CHD in patients 60 years old.
This study has several important limitations. The
number of volunteers recruited in this study without
receiving medication for CHD (e.g. antilipaemic
agents) was small, the design was retrospective and
there was no control group. Furthermore, our study
population was limited to Chinese patients 60 years
old with CHD who did not have diabetes, a history
of smoking or a history of cerebral or peripheral vas-
cular disease. The relationship between periodontitis
and CHD may be different in more ethnically diverse
populations or younger patients or patients with more
risk factors. To clearly establish the relationship
between periodontitis and CHD, unied standards
should be formulated and a larger sample number
should be included. In addition, to further clarify the
effect of periodontitis on coronary artery stenosis,
CHD patients with periodontitis should receive peri-
odontal treatment and be followed in a longitudinal
manner to determine whether periodontitis treatment
improves the prognosis of CHD patients.
CONCLUSIONS
The extent and severity of coronary artery stenosis in
Chinese patients 60 years old with CHD is positively
correlated with the severity of periodontitis. Periodon-
titis might be an independent risk factor for CHD.
ACKNOWLEDGEMENTS
This study was supported by the Science and Technol-
ogy Planning Project of Guangdong Province, China;
project number: 2007B031500018; 2009B060700042.
CONFLICT OF INTEREST
The authors declare that they have no conict of
interest.
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Address for correspondence:
Jun-ying Yang MD
Department of Stomatology
First Afliated Hospital of Sun Yat-sen University
No. 58 Zhongshan Road 2
Guangzhou 510080
China
Email: yangjuny@mail.sysu.edu.cn
338 2013 Australian Dental Association
J Yang et al.