Open Journal of Stomatology, 2013, 3, 457-463 OJST Published Online November 2013 (
The relationship among periodontal condition, serum lipid,
and electrocardiographic abnormalities in the elderly: A
prospective cohort study
Lisdrianto Hanindriyo1,2, Akihiro Yoshihara3, Toshinobu Hirotomi1, Hideo Miyazaki1
1Division of Preventive Dentistry, Department of Oral Health Science, Graduate School of Medical and Dental Science, Niigata
University, Niigata, Japan
2Department of Preventive and Community Dentistry, Faculty of Dentistry, Gadjah Mada University, Yogyakarta, Indonesia
3Division of Oral Science for Health Promotion, Department of Oral Health and Welfare, Graduate School of Medical and Dental
Science, Niigata University, Niigata, Japan
Received 30 September 2013; revised 31 October 2013; accepted 11 November 2013
Copyright © 2013 Lisdrianto Hanindriyo et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Periodontal disease is recognized as a risk factor for
cardiovascular disease (CVD). Some studies have
suggested that serum lipids might play a role in the
association between periodontal disease and CVD.
However, this hypothesis remains unproven. Present
study evaluated the association between periodontal
disease and CVD-related parameters including elec-
trocardiographic (ECG) parameters and serum lipid
levels in the elderly. This study was a prospective
cohort study. A total of 107 subjects (57 males and 50
females) from Niigata City’s community-dwelling
elderly (all aged 75 years old) who possessed at least
20 teeth and did not exhibit ECG abnormalities at the
baseline underwent annual examinations for 5 years.
Logistic regression analysis was used to assess the
relationship between periodontal condition and the
presence of ECG abnormalities, after adjusting for
confounding factors including serum lipid levels. Lo-
gistic regression analysis showed that the subjects
who exhibited a poor periodontal condition at the
baseline had a 2.97 times greater risk of suffering
from ECG abnormalities than the subjects who dis-
played a good periodontal condition at the baseline (p
= 0.019). Furthermore, the subjects who displayed a
poor periodontal condition and an unfavorable se-
rum lipid profile at the baseline showed a signifi-
cantly higher frequency of ECG abnormalities (63.6%)
than those who exhibited a healthy periodontal condi-
tion and a favorable serum lipid profile (21.6%, p =
0.008) as well as those who displayed a healthy perio-
dontal condition and an unfavorable serum lipid pro-
file (21.4%, p = 0.010). As a conclusion, periodontal
condition could be a marker of CVD, even in the
healthy elderly.
Keywords: Periodontal Condition; Serum Lipid;
Cardiovascular Disease; Elderly People
It has been determined that poor oral health can have a
profound effect on general health, and several oral dis-
eases are known to be associated with chronic diseases
[1]. Besides the fact that periodontal disease is one of
two major dental diseases that display high prevalence
rates worldwide [2], the World Health Organization
(WHO) has also found that periodontal disease shares
some common risk factors with systemic diseases such
as cardiovascular disease (CVD) [3].
Previous studies have suggested that serum lipids
might play a role in the association between periodontal
disease and CVD, particularly in elderly patients. While
a reduced high-density lipoprotein cholesterol (HDL-C)
level is a well-recognized risk factor for CVD and
ischemic stroke [4,5]. Izumi et al. [6] found that a higher
total cholesterol (TC) level is associated with a lower
prevalence of periodontitis in non-smoking elderly peo-
ple. Moreover, two cross-sectional studies have been
conducted in Japan to assess the associations between
blood chemical parameters and periodontal status, and
both studies indicated that elevated HDL-C levels are
correlated with a reduced incidence of periodontal dis-
ease [7,8].
On the other hand, other studies failed to identify any
L. Hanindriyo et al. / Open Journal of Stomatology 3 (2013) 457-463
association between periodontal disease and CVD. Holm-
Pedersen et al. [9] investigated the correlations among
dental caries, periodontal disease, and cardiac arrhythmia
in community-dwelling elderly individuals who were
aged 80 or older and showed that there was no associa-
tion between periodontal disease and arrhythmia. In line
with this result, a case-control study by Sridhar et al. [10]
found that coronary heart disease did not exacerbate the
destruction of periodontal tissue.
The inconsistencies between these studies might have
been due to differences in study design, the adjustments
made for confounding variables, and other methodologi-
cal details. Some previous studies used a case-control
design, which is known to introduce various types of bias
[11], while other studies employed a cross-sectional de-
sign, which made it impossible to assess the direction of
the relationship between the assumed cause and effect
[12]. Furthermore, some previous studies might have
inadequately controlled for confounding factors such as
gender, age, smoking status/history, and body mass index
Therefore, the purpose of this study was to evaluate
the association between periodontal disease and CVD-
related parameters including electrocardiographic (ECG)
parameters and serum lipid levels in the elderly using a
prospective cohort study design. The result of this study
was considered to be important in giving more insights
for the elucidation of the correlation between oral and
general health.
2.1. Subjects
The subjects for this study was drawn from the Niigata
Elderly Study, which was a community-based prospec-
tive study that aimed to assess the relationship between
oral health and general health in the elderly. Invitations
were sent to all residents (n = 4542) who were born in
1927 based on the Niigata City’s resident registry. The
invitations also informed the recipients of the purpose of
the study. As a result, 81.4% (n = 3695) of the invitees
agreed to participate in the study. Considering the avail-
ability of resources, appointments for examinations could
only be arranged for 600 individuals. The final study
subjects (n = 600) were randomly selected so that they
included approximately equal numbers of men (306) and
women (294). We assessed the general condition of the
subjects using the Tokyo Metropolitan Institute of Ger-
ontology Index (TMIG-Index) of Competence subscale
questionnaires. All of the subjects were Japanese, in
good general health, and did not require special care for
their daily activities. The subjects’ mean score on the
TMIG-Index subscales was 11.9 ± 1.4, and the results of
this assessment were indicative of a high level of com-
petence among the study participants. The 600 subjects
were invited for annual examinations including oral and
general physical examinations from 1998 to 2008. All of
the subjects agreed and signed informed consent forms
regarding the examination protocols. Of the 600 subjects,
312 participated in all of the annual examinations from
2003 to 2008. An age of 75 years in 2003 was set as the
baseline for the present study since a recent review
showed that approximately 50% of patients with dys-
rhythmia, especially atrial fibrillation, were aged 75
years or older [13]. One hundred and seven (57 males
and 50 females) of the 312 subjects were selected for the
present study because they had at least 20 teeth and did
not display any atherosclerosis-related ECG abnormali-
ties at the baseline which was considered as the inclusion
criteria for this study. All of the subjects were examined
at local community centers in Niigata City. The ethics
committee of the Niigata University School of Dentistry
approved this study and protected the subjects’ rights.
2.2. Oral Examinations
The periodontal examinations were carried out by four
trained dentists under sufficient illumination with artifi-
cial light. Periodontal conditions was assessed using
dental mirrors and a specially designed constant-pressure
periodontal probe (Vivacare TPS Probe®; Schaan,
Liechtenstein), which was applied at a probing force of
20 g. The probing depth (PD) and clinical attachment
level (CAL) at six sites (mesiobuccal, mid-buccal, dis-
tobuccal, mesiolingual/palatal, mid-lingual/palatal, and
distolingual/palatal) were recorded for all teeth, include-
ing the third molars, and rounded to the nearest millime-
ter. The examiners were calibrated before and during the
survey, and inter-examiner reliability was assessed. Ac-
cording to replicated examinations of 10 patients, the
percentage agreement (within ± 1 mm) ranged from
87.5% to 100.0% for PD and 83.3% to 100.0% for CAL.
In addition, the Kappa value ranged from 0.8 to 1.0 for
PD and 0.7 to 1.0 for CAL. The National Health and
Nutrition Examination Survey (NHANES) III [14] found
that about 30.0% of 70- to 80-year-old subjects had
moderate to advanced periodontitis. Accordingly, we
used the 30th percentile to indicate a poor periodontal
condition. Therefore, each subject’s periodontal condi-
tion was classified according to whether their mean PD
was 1.8 mm or < 1.8 mm and whether their mean CAL
was 2.5 mm or < 2.5 mm [15]. Subjects with a mean
PD of 1.8 mm and a mean CAL of 2.5 mm were con-
sidered to exhibit a poor periodontal condition. The mean
PD was 2.05 mm, and the mean CAL was 2.98 mm. The
number of teeth present was also investigated.
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L. Hanindriyo et al. / Open Journal of Stomatology 3 (2013) 457-463 459
2.3. General Examinations
2.3.1. Electrocardiography
A resting 12-lead ECG recording was taken using a
standard ECG machine (CardioStar FCP-7411; Fukuda
ME Kogyo Co., Tokyo, Japan) equipped with an auto-
mated analysis system whilst the subject was in the su-
pine position, in accordance with standard recommenda-
tions [16]. The criteria established by Takata et al. [17]
were used to diagnose atherosclerosis-related ECG ab-
normalities. Atrial fibrillation was defined as a markedly
irregular R-R interval and the absence of P-waves, with
disorganized electrical activity being seen in their place.
VPC (Ventricular premature contractions) were defined
as an antecedent R-R interval of 0.8 × the mean R-R
interval, a subsequent R-R interval of 1.05 × the mean
R-R interval, and an abnormal QRS complex. SVPC
(Supraventricular premature contractions) were defined
as an antecedent R-R interval of 0.8 × the mean R-R
interval, a subsequent R-R interval of 1.05 × the mean
R-R interval, a normal QRS complex, and no evidence of
atrial fibrillation or sinus dysrhythmia. Sinus dysrhyth-
mia was defined as an irregular R-R interval with no
other dysrhythmia. Sinus tachycardia was defined as a
P-wave rate of greater than 100 beats/min, with no other
dysrhythmia. Sinus bradycardia was defined as a P-wave
rate of less than 60 beats/min, with no other dysrhythmia.
LVH (left ventricular hypertrophy) and ST-segment de-
pression as defined by the Minnesota Code were also
evaluated [18]. All of the abovementioned conditions
were considered to be abnormal ECG findings. The sub-
jects who displayed any of these ECG abnormalities
during a follow-up examination were categorized as “po-
sitive”, and those that did not were categorized as “nega-
2.3.2. Blood Pressure, Gender, Smoking History, BMI,
and Blood Measurements
The blood pressure (BP) measurement and blood sam-
pling were performed with the subjects in the supine po-
sition. The patients’ TC, HDL-C, and low-density lipo-
protein cholesterol (LDL-C) levels were determined by a
commercial laboratory (BML, Inc., Tokyo, Japan) under
non-fasting conditions. Based on the threshold for people
in the intermediate-risk group for CVD (possessing 1 - 2
major risk factors for CVD other than LDL-C; age 45
for males and 55 for females is a major risk factor)
suggested by the Japan Atherosclerosis Society [19],
subjects with serum LDL-C levels of < 140 mg/dL, se-
rum HDL-C levels of 40 mg/dL, and serum TC levels
of < 220 mg/dL were considered to display favorable
serum lipid profiles, while the subjects that exhibited the
opposite findings were considered to display unfavorable
serum lipid profiles. Personal interviews were conducted
to obtain information regarding the subjects’ smoking
habits and sex. Anthropometric evaluations including
measurements of weight and height were performed to
allow BMI calculations to be performed.
2.4. Statistical Analysis
Initially, the subjects’ characteristics were compared be-
tween the subjects with and without ECG abnormalities
using the t-test for quantitative data and the chi-square
test for categorical variables. During this analysis, base-
line data regarding the number of remaining teeth; HDL-
C, LDL-C, and TC levels; and mean PD and CAL were
Furthermore, to analyze the effects of periodontal con-
dition and the serum lipid profile on the presence/ab-
sence of ECG abnormalities during the study period, the
chi-square test was used to compare the following four
groups: the subjects who exhibited a healthy periodontal
condition and a favorable serum lipid profile (n = 37); a
healthy periodontal condition and an unfavorable serum
lipid profile (n = 28); a poor periodontal condition and a
favorable serum lipid profile (n = 31); and a poor perio-
dontal condition and an unfavorable serum lipid profile
(n = 11).
Finally, logistic regression analysis was performed to
examine the independent effect of periodontal condition
on the presence/absence of ECG abnormalities during the
study period. The presence of ECG abnormalities during
the study period was used as the dependent variable,
while the independent variables were periodontal condi-
tion at the baseline and other parameters that were found
to be significantly associated with ECG abnormalities in
the initial analysis. All calculations and statistical analy-
ses were performed using SPSS version 17. Statistical
significance was set at α = 0.05.
Table 1 shows the means and distributions of the study
variables according to the presence or absence of ECG
abnormalities during the study period. The subjects with
ECG abnormalities had significantly higher BMI values
at the baseline than those without (23.9 ± 2.8 vs 22.6 ±
2.8 kg/m2, p = 0.030). Furthermore, ECG abnormalities
were significantly associated with lower LDL and TC
levels at the baseline. While only 29.2% of the subjects
who did not exhibit ECG abnormalities displayed a poor
periodontal condition, 60.0% of the subjects with ECG
abnormalities displayed a poor periodontal condition (p =
As shown in Figure 1, a significantly higher percent-
age of the subjects who displayed a poor periodontal
condition and an unfavorable serum lipid profile at the
baseline suffered from EC abnormalities (63.6%) G
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L. Hanindriyo et al. / Open Journal of Stomatology 3 (2013) 457-463
Copyright © 2013 SciRes.
Table 1. Background characteristics of the subjects according to their ECG status.
ECG abnormalities
Negative Positive
n = 72 n = 35
Subjects’ characteristics
Mean ± SD p-valuea
Present teeth at the baseline 25.1 ± 2.9 25.4 ± 3.0 0.641
BMI at the baseline (kg/m²) 22.6 ± 2.8 23.9 ± 2.8 0.030
Mean BMI over 5 years (kg/m2) 22.1 ± 2.7 23.2 ± 2.9 0.060
Systolic BP at the baseline (mmHg) 129.9 ± 15.3 133.8 ± 17.4 0.231
Mean systolic BP over 5 years (mmHg) 132.5 ± 10.1 134.9 ± 12.2 0.259
Diastolic BP at the baseline (mmHg) 70.3 ± 9.3 71.8 ± 9.7 0.433
Mean diastolic BP over 5 years (mmHg) 71.8 ± 6.5 72.4 ± 8.7 0.734
Mean PD at the baseline (mm) 2.0 ± 0.4 2.1 ± 0.3 0.287
Mean CAL at the baseline (mm) 2.9 ± 0.7 3.1 ± 0.7 0.138
HDL level at the baseline (mg/dL) 60.3 ± 15.6 59.8 ± 21.5 0.893
LDL level at the baseline (mg/dL) 119.7 ± 25.6 104.1 ± 26.8 0.005
TC level at the baseline (mg/dL) 206.2 ± 28.8 194.1 ± 28.5 0.044
N (%) p-valueb
Male 36 (50.0) 21 (60.0) 0.331
Female 36 (50.0) 14 (40.0)
Periodontal condition at the baseline
Healthy 51 (70.8) 14 (40.0) 0.002
Poor conditionc 21 (29.2) 21 (60.0)
Lipid condition at the baseline
Favorable 46 (63.9) 22 (62.9) 0.917
Unfavorabled 26 (36.1) 13 (37.1)
Smoking statuse
Non-smoker 64 (88.9) 30 (85.7) 0.921
Smoker 8 (11.1) 4 (11.4)
BMI; Body mass index, BP; Blood pressure, PD; Probing depth, CAL; Clinical attachment level, HDL; High density lipoprotein, LDL; Low density lipoprotein,
TC; Total cholesterol; at-test; bChi-square test; cMean PD 2 mm and mean CAL 2.5 mm; dSerum LDL-C level 140 mg/dL and/or serum HDL-C level < 40
mg/dL and/or serum TC 220 mg/dL; eData was missing for 1 subject.
compared with the subjects who exhibited a healthy pe-
riodontal condition and a favorable serum lipid profile
(21.6%, p = 0.008), or a healthy periodontal condition
and an unfavorable serum lipid profile, at the baseline
(21.4%, p = 0.010). Furthermore, the frequency of ECG
abnormalities was significantly lower in the latter two
groups than in the other two groups (21.5% vs 50.0%, p
= 0.002).
The results of the multivariate logistic regression
analysis are shown in Table 2. The subjects who dis-
played a poor periodontal condition at the baseline were
found to be at a 2.97 times higher risk of exhibiting ECG
abnormalities than the subjects who displayed a healthy
periodontal condition at the baseline (p = 0.019). More-
over, BMI at the baseline was positively associated with
the presence of ECG abnormalities (OR = 1.22, p = 0.019)
while the LDL-C level at the baseline had a significant
negative effect on the risk of ECG abnormalities (OR =
.96, p = 0.019).
Figure 1. Percentage of subjects that displayed
ECG abnormalities over 5 years in four groups
according to their periodontal condition and se-
rum lipid level [P (H); Healthy periodontal con-
dition, P (P); Poor periodontal condition, SL (F);
Favorable serum lipid profile, SL (U); Unfavor-
able serum lipid profile]. *p < 0.05, **p < 0.01. 0
L. Hanindriyo et al. / Open Journal of Stomatology 3 (2013) 457-463 461
Table 2. Binary logistic regression analysis of the effects of the explanatory variables including periodontal condition on the presence
of ECG abnormalities.
Dependent variable: Presence of ECG abnormalities over 5 years
Independent variable Coefficient SE p-value OR 95% CI
Periodontal condition (0: healthy/1: poor) 1.09 0.47 0.019 2.97 1.19 - 7.38
TC at the baseline 0.02 0.02 0.227 1.02 0.99 - 1.05
LDL at the baseline 0.04 0.02
0.019 0.96 0.92 - 0.99
BMI at the baseline 0.20 0.09 0.019 1.22 1.03 - 1.45
TC; Total cholesterol, LDL; Low density lipoprotein, BMI; Body mass index, SE; Standard error, OR; Odds ratio, CI; Confidence interval.
An association between periodontal condition and the
presence of ECG abnormalities was detected in this study.
It has been suggested that dental caries and periodontal
disease are related to myocardial infarction [20], dys-
rhythmia [21], coronary heart disease [4], and abnormal
ECG findings in octogenarians [17]. Furthermore, some
studies have reported that periodontitis results in higher
systemic levels of C-reactive protein and interleukin-6
and increased numbers of neutrophils, suggesting that
elevated levels of these inflammatory substances cause
inflammatory changes in atherosclerotic lesions, in-
creasing the risk of cardiac or cerebrovascular disease
events [22,23]. Other recent studies have suggested that
S. mutans migrates to cardiovascular endothelial tissue
[24] and binds to extracellular matrix molecules and fi-
brinogen [25]. Moreover, DNA from periodontal patho-
gens was highly prevalent in coronary artery atheroscle-
rosis samples taken from patients with coronary artery
disease [26]. These findings support the view that infec-
tion with oral bacterial species could be a risk factor for
coronary heart disease.
A negative association between the serum LDL-C
level and the presence of ECG abnormalities during the
study period was found in this study. One possible ex-
planation for this inverse association is the effect of se-
lective survival; i.e., those who are susceptible to the
biological effects of high cholesterol levels tend to die
before reaching an advanced age [27,28]. Thus, the indi-
viduals who lived longer would form an unintentionally
selected group with lower cholesterol levels and a ge-
netic background (or other factors) that protects them
from the effects of higher cholesterol concentrations [29].
This explanation agrees with the fact that the subjects in
the present study were relatively healthy and did not re-
quire special assistance for their daily activities. Another
study stated that in the very elderly, changes in the vessel
wall might lower their susceptibility to cholesterol [28].
This finding might also explain our study results. The
subjects who exhibited a poor periodontal condition and
unfavorable serum lipid levels at the baseline displayed
the highest frequency of ECG abnormalities during the
study period. The difference in the frequency of ECG
abnormalities was greatest between the subjects who did
and did not display a healthy periodontal condition, re-
gardless of their baseline serum lipid levels. Moreover,
no significant difference in the frequency of ECG ab-
normalities was found between the subjects with and
without favorable serum lipid levels who displayed the
same periodontal condition. Therefore, periodontal con-
dition was more closely associated with ECG abnormali-
ties than serum lipid levels at the baseline. One possible
explanation for this is that the subjects were relatively
healthy and independent community-dwelling elderly
individuals who had few problems with their general
health, particularly with their serum lipid profiles. An-
other possible explanation is that we did not include se-
rum triglycerides when assessing serum lipid condition
since non-fasting blood samples were collected. Since
serum triglycerides might influence a patient’s lipid pro-
file, this should be considered as one of the limitations of
our study. Another possible limitation of our study was
the fact that we did not possess information about the
medication being taken by the subjects, which might
have also had an influence on the presence/absence of
ECG abnormalities, nor did we have any information
about the other medical conditions suffered by the sub-
jects, such as their blood glucose levels, which could
have affected their systemic condition.
Our results suggest that in the elderly periodontal condi-
tion has a significantly positive effect on the risk of ECG
abnormalities, while the LDL-C level has the opposite
effect. These findings indicate that periodontal condition
could be used as a marker of coronary heart disease, even
in the healthy elderly. Therefore, it is important to recog-
nize periodontitis as a possible marker for coronary heart
disease with an inverse association of serum lipid condi-
tion in the elderly.
The authors declare that they have no conflict of interests. This study
Copyright © 2013 SciRes. OPEN ACCESS
L. Hanindriyo et al. / Open Journal of Stomatology 3 (2013) 457-463
was supported by a grant-in-aid from the Ministry of Health and Wel-
fare of Japan (H10-Iryo-001). We are profoundly grateful to the study
participants for their assistance.
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