The relationship among periodontal condition, serum lipid, and electrocardiographic abnormalities in the elderly: A prospective cohort study

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Open Journal of Stomatology, 2013, 3, 457-463 OJST

http://dx.doi.org/10.4236/ojst.2013.38076 Published Online November 2013 (http://www.scirp.org/journal/ojst/)

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

Email: [email protected]

Received 30 September 2013; revised 31 October 2013; accepted 11 November 2013

License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

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

1. INTRODUCTION

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

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L. Hanindriyo et al. / Open Journal of Stomatology 3 (2013) 457-463

458

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

(BMI).

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. MATERIALS AND METHODS

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.

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-

tive”.

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

compared.

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.

3. RESULTS

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 =

0.002).

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

L. Hanindriyo et al. / Open Journal of Stomatology 3 (2013) 457-463

460

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

Gender

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

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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.

4. DISCUSSION

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.

5. CONCLUSION

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.

6. ACKNOWLEDGEMENTS

The authors declare that they have no conflict of interests. This study

L. Hanindriyo et al. / Open Journal of Stomatology 3 (2013) 457-463

462

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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