Introduction

Periodontal disease is an inflammatory disease in which the host's defenses are weakened and
periodontal tissue is destroyed due to intracellular and extracellular toxins produced by
periodontal pathogens such as Porphyromonas gingivalis [1]. Periodontal disease is the main
cause of tooth loss and has been recognized as a representative health problem that reduces
an individual's quality of life [2]. Although the causes and prevention methods of periodontal
disease have been largely discovered, it is still one of the most common diseases in the world
[2]. In addition, according to data from the Health Insurance Review and Assessment Service in
2018, periodontal disease has maintained the second place among the most common
outpatient diseases among Koreans over the past five years [3], placing a significant burden on
the National Health Insurance finances.

Recently, a two-way relationship between periodontitis, an inflammatory disease, and

non-infectious chronic diseases is gradually being revealed. Periodontal disease affects the
development of cardiovascular disease, coronary artery disease [4], and diabetes [5], and
furthermore, the invasion of periodontal pathogens into the blood promotes a systemic
inflammatory response, increasing the incidence of rheumatoid arthritis [6]. . Therefore, all
medical personnel, including oral health personnel, must be aware that a healthy periodontal
condition plays a cornerstone role in maintaining and promoting overall health.

Recently, interest in the relationship between dyslipidemia and periodontal health status is
increasing [7]. Dyslipidemia is when the concentration of total cholesterol, low density
lipoprotein cholesterol, and triglyceride is higher than normal, or the concentration of high
density lipoprotein cholesterol is normal. It means a more reduced state [8]. So far, the types of
blood lipids associated with periodontal disease have been reported in various ways depending
on the demographic characteristics or control factors of the study subjects. In particular, high
concentrations of total cholesterol among lipids are not only a trigger for diabetes but also a risk
factor for periodontal disease [7]. In the study by Griffiths and Barbour [8], high levels of
low-density lipoprotein cholesterol and triglycerides were associated with periodontal disease. In
addition, recent research results showed that 8-OHdG (8-OHdG), a marker of periodontal
disease, was found in the saliva of a group with hyperlipidemia.
An increase in hydroxy-2'-deoxyguanosine) was confirmed [9]. In addition, even after controlling
for factors such as age and obesity, the ratio of triglycerides to high-density lipoprotein
cholesterol was positively correlated with the incidence of periodontal disease [10]. Conversely,
since periodontal disease is associated with a decrease in high-density lipoprotein cholesterol or
an increase in low-density lipoprotein cholesterol, periodontal inflammation has been reported
as a factor that impairs lipid metabolism [11]. At a time when the prevalence of both dyslipidemia
and periodontal disease is continuously increasing [12], there are only a few studies reporting
the influence of dyslipidemia on the development of periodontal disease in Koreans.
Therefore, this study evaluated the relationship between periodontal health status and
dyslipidemia using highly reliable National Health and Nutrition Examination Survey data that
can represent the health status of Koreans, and especially analyzed the types of blood lipids
that can predict the occurrence of periodontitis. I wanted to do it. The results of this study are
expected to reduce the prevalence of periodontal disease in adults and provide meaningful
information for effective periodontal health management in patients with periodontal disease.

Research method

1. Research subject

This study was analyzed using raw data from the 6th 2015 Korea National Health and Nutrition
Examination Survey. The 2015 data is the most recent data for which oral examination results
are available. The National Health and Nutrition Survey is a statutory survey on citizens' health
behavior, food and nutritional intake, and chronic disease prevalence based on Article 16 of the
National Health Promotion Act [12]. The survey was divided into a health survey, a check-up
survey, and a nutrition survey. The health survey and check-up survey were conducted at a
mobile check-up center, and the nutrition survey was conducted by directly visiting the target
households. The sampling method of the National Health and Nutrition Survey was a two-stage
stratified cluster sampling method with survey districts and households as the first and second
sampling units, and the 6th period was 192 survey districts were extracted. Within the sample
survey district, 20 sample households were selected from households excluding nursing homes,
etc., and all household members over the age of 1 who met the appropriate requirements within
the sample households were selected as survey subjects. Among the 7,380 people who
participated in the 2015 National Health and Nutrition Survey, this study included 3,992 (54.1%)
who were between 30 and 80 years old and who completed the health survey and examination
(blood test and oral examination). was selected. According to the National Health and Nutrition
Examination Survey, people over 30 years of age are a group with a prevalence of periodontal
disease that requires periodontal disease treatment of more than 10% [12]. This study received
exemption approval from the Bioethics Review Committee of 00 University (IRB NO.
1044396-201912-HR-218-01).

2. Research tools

This study used the results of the study subjects' health survey (social and demographic
characteristics and health behavior), blood test, and oral examination. Socio-demographic
characteristics consisted of gender, age, education level, and individual income level. Health
behaviors consisted of the number of daily tooth brushing, use of interdental cleaning tools, oral
examination in the past year, lifetime drinking experience, and lifetime smoking experience. The
frequency of toothbrushing was 2 or less times and 3 or more times, and if dental floss or
interdental brushes were used, the subjects were reclassified as users of interdental cleaning
tools. Obesity was reclassified into underweight (less than 18.5 kg/m2), normal (18.5-24.9
kg/m2), and obese (more than 25 kg/m2) based on body mass index [13].
Blood test results used the concentrations of glycated hemoglobin, total cholesterol,
high-density lipoprotein cholesterol, low-density lipoprotein cholesterol, and neutral fat. COBAS
8000 C702 (Roche, Germany) was used to analyze all lipids. Total cholesterol and triglycerides
were measured using the enzymatic method, and two types of lipoprotein cholesterol were
measured using the homogeneous enzymatic colorimetric method [12]. If glycated hemoglobin
was 6.5% or higher, the patient was reclassified as a group with high blood sugar [14].
According to NCEP-ATP III (National Cholesterol Education Program-adult Treatment Panel III)
[15] and the standards of the Korean Society of Laboratory Medicine [16], total cholesterol is
more than 240 mg/dL, high-density lipoprotein cholesterol is less than 40 mg/dL, and
low-density lipoprotein cholesterol is They were classified as cholesterol 160 mg/dL or higher
and triglyceride 200 mg/dL or higher, respectively.

Periodontal health status was investigated for teeth 11, 16, 17, 26, 27, 31, 36, 37, 46, and 47
using the Community Periodontal Index (CPI). The CPI score is based on healthy periodontal
tissue (CPI cord 0), gingival bleeding on probing (CPI cord 1), tartar deposition (CPI cord 2),
periodontal pocket depth of 4-5 mm (CPI cord 3), and periodontal pocket depth of 6 mm or more
( It was classified as CPI cord 4). In this study, those with a CPI of 3 or higher were classified as
periodontitis patients [12,17].

3. Data analysis

Complex sample analysis was performed on the data using the IBM SPSS program (ver. 25.0;
IBM Co., Armonk, NY, USA). A planning file was created using the variance estimation layer for
the pre-analysis layer, the survey district number for the cluster, and the survey and screening
survey weights for the weights. A complex sample cross-analysis was conducted to analyze
differences in the prevalence of periodontitis according to the socio-demographic characteristics
and glycated hemoglobin and lipid concentrations of the study subjects. Logistic regression
analysis was performed to analyze the strength of influence of each lipid in the development of
periodontitis. During the logistic regression analysis, the dependent variable was the presence
of periodontitis, and the independent variables were variables that showed significant
differences in the cross-tabulation results. The evaluation of statistical significance was based
on α=0.05.

Results

1. Relationship between social and demographic characteristics of study subjects and

periodontitis

As a result of analyzing the relationship between the socio-demographic characteristics of the

study subjects and periodontitis, the prevalence of periodontitis was higher in men (40.8%) than
in women, and in the group aged 70 or older (47.7%) compared to those aged 69 or younger
(p<0.001). . In addition, the prevalence of periodontitis was found to be higher in the group with
a personal income level of less than 25% (42.3%) than in the group with the bottom 25% or
more, and in the group with an education level of high school or lower (41.8%) rather than
college or higher (p<0.001) <Table 1>

2. Relationship between study subjects’ health behavior characteristics and periodontitis

As a result of analyzing the relationship between the health behavior characteristics of the
research subjects and periodontitis, the prevalence of periodontitis was found in the group who
brushed their teeth twice or less per day rather than 3 or more times (39.1%), and the group that
did not use interdental cleaning tools (41.4%) compared to the group that used interdental
cleaning tools. was found to be higher (p<0.001). In addition, the prevalence of periodontitis was
higher in the group that did not have a dental check-up in the past year (36.7%), and in the
group with no lifetime drinking experience (45.1%) or smoking experience (42.3%) than in the
group without dental check-up. (p<0.05)<Table 2>.
3. Relationship between study subjects’ systemic health-related characteristics and periodontitis

As a result of analyzing the relationship between the study subjects' systemic health-related
characteristics and periodontitis, the prevalence of periodontitis was found to be higher in the
obese group (42.0%) or with a glycated hemoglobin of 6.5% or more (52.4%) compared to the
normal group (p<0.001) ). In addition, compared to the normal group, the prevalence of
periodontitis was found to be higher in the group with abnormal concentrations of total
cholesterol (41.7%), high-density lipoprotein cholesterol (45.5%), low-density lipoprotein
cholesterol (41.6%), and triglyceride (44.9%) (p <0.05)<Table 3>.
4. Strength of association between dyslipidemia and periodontitis

As a result of performing multiple logistic regression analysis to analyze the strength of the
association between dyslipidemia and periodontitis, the group with abnormal triglyceride
concentration in blood lipids (≥200 mg/dL) was found to be the normal group even after
controlling for factors related to periodontitis. Compared to the group, the risk of periodontal
disease was found to be 1.3 times higher (OR: 1.305; p<0.05). In addition, the risk of
periodontitis increased with age, including groups with personal income levels in the bottom
25% or 25-50%, groups with an education level of high school or lower, groups that do not use
interdental cleaning tools, and those who have smoked throughout their lives. The obese group
(BMI≥25 kg/m2 or more) was found to have a higher risk of periodontitis compared to each
control group (p<0.05) <Table 4>.
Overview and design

Recently, dyslipidemia has been highlighted as a factor associated with poor periodontal health
[18]. The prevalence of both dyslipidemia and periodontal disease is increasing, and only a few
studies have reported the relationship between these two factors in Koreans. Therefore, this
study analyzed the relationship between periodontitis and dyslipidemia in a total of 3,992 adults
aged 30 years or older using the National Health and Nutrition Examination Survey (2015),
which is highly reliable in representing the health status of Koreans. We aimed to identify the
types of blood lipids that can predict the occurrence of periodontitis. The results of this study are
expected to provide meaningful information that can reduce the occurrence of periodontal
disease in adults and contribute to effective periodontal treatment. The main results and
implications of this study are as follows.

The prevalence of periodontitis was higher in the group with abnormal concentrations of total
cholesterol, high-density lipoprotein cholesterol, low-density lipoprotein cholesterol, and
triglycerides (p<0.05). However, in a logistic regression model that controlled for factors related
to periodontitis, the risk of periodontitis was found to be about 1.3 times higher in the group with
a concentration of neutral fat in the blood lipids above 200 mg/dL than in the normal group
(<200 mg/dL). This result showed a similar trend to previous studies [8,19]. Previous studies
have reported various types of lipids that contribute to the development of periodontitis. In the
research results of Griffiths and Barbour [8], high concentrations of low-density lipoprotein
cholesterol and triglycerides were associated with periodontal disease. Additionally, in a study
targeting Japanese people, high concentration of neutral fat (>149 mg/dL) was reported as a
potential factor for the development of periodontitis [19]. In another study, total cholesterol It was
found that low-density lipoprotein cholesterol was associated with an increase in the amount of
clinical attachment loss, and the concentration of neutral fat was related to the depth of
periodontal pockets [20]. In a study conducted on Koreans by Han et al. [21], a decrease in the
concentration of high-density lipoprotein cholesterol or an increase in triglycerides was
associated with periodontitis, and in particular, the correlation between decreased high-density
lipoprotein cholesterol and the occurrence of periodontitis in heavy smokers was confirmed. did.
On the other hand, in a cohort study by Katz et al. [22], periodontal pocket depth was positively
correlated with total cholesterol and low-density lipoprotein cholesterol, but no correlation with
triglycerides was confirmed. In a study by Golpasand Hagh et al. [23], the concentrations of
high-density lipoprotein cholesterol and low-density lipoprotein cholesterol showed a tendency
to be related to periodontal inflammation, but it was not statistically significant. Meanwhile, the
excessive increase in neutral fat among lipids increases the levels of IL-8 (interleukin-8) and
MCP-1 (monocyte chemoattractant protein-1) in the blood. It has been known to be
independently associated with an increase in cytokines, including: In particular, the increase in
free fatty acid resulting from the breakdown of neutral fat plays an important role in increasing
various inflammatory cytokines and changing the body into an inflammatory state. [24]. Although
the mechanism of the relationship between blood lipid concentration and periodontitis has not
been clearly elucidated so far, Lutfioğlu et al. [25] reported that the high concentration of lipids in
the blood increases oxidative stress in the gingival sulcus. In addition, an increase in lipids
causes excessive secretion of inflammatory cytokines such as TNF-α (tumor necrosis factor-α),
and it has been suggested that this hyperinflammatory state is related to intra- and extra-oral
inflammatory diseases [26]. Therefore, considering the results of previous studies and this study
together, we suggest that abnormally high concentration of neutral fat is a preceding factor that
can predict the occurrence of periodontitis. Accordingly, oral health personnel must be aware of
the importance of lipid metabolism for optimal periodontal health in adults, and there is a need
to periodically monitor the concentration of lipids in the blood through collaboration with internal
medicine medical staff.

Dyslipidemia itself does not cause any special symptoms, but is a representative risk factor for
cardiovascular disease that contributes to mortality [15]. The main risk factors for dyslipidemia
include old age, heredity, high-lipid diet, overweight, lack of exercise, diabetes, and high blood
pressure [14]. In addition, considering the research results showing that the concentration of
neutral fat was high in smokers and the level of high-density lipoprotein cholesterol in
non-smokers [27], smoking can be considered a factor that interferes with lipid metabolism.
Therefore, considering the results of this study suggesting dyslipidemia as a risk factor for
periodontitis, oral health personnel should increase their interest in dyslipidemia and strive to
practice comprehensive care.

In addition, in this study, as age increases (OR: 1.035), individual income level is in the bottom
25% (OR: 1.508) or in the 25-50% group (OR: 1.360), and education level is high school or
lower (OR: : 1.319), the group that does not use interdental cleaning tools (OR: 1.366), and the
group with a body mass index of 25 kg/m2 or more (OR: 1.343) showed a higher risk of
periodontitis compared to the control group (p<0.05). Additionally, it was confirmed that the
group with no lifetime smoking experience had a lower risk of periodontitis compared to the
group with experience (OR: 0.589, p<0.001). As shown in the results of this study, many
previous studies have reported that low socioeconomic status and poor lifestyle habits such as
smoking are risk factors for periodontal disease [28]. In particular, factors such as older age,
high levels of glycated hemoglobin, and smoking contribute to the development of chronic
diseases, but are also risk factors for periodontal disease [2,14]. Therefore, in clinical practice,
the influence of not only oral risk factors but also external factors should be reviewed in depth in
promoting oral health. In particular, among health behaviors, the use of interdental cleaning
tools is a major factor in reducing periodontal disease due to its high effectiveness in removing
dental plaque [29]. The use of interdental cleaning tools among Koreans is still low [30].
Therefore, oral health personnel need to recommend the most appropriate cleaning tools for
their oral health status and provide periodic intervention to help patients achieve optimal oral
health. In addition, toothbrushing is the most basic factor in preventing periodontal disease, but
the correlation between the number of toothbrushing times and periodontitis was not confirmed
in this regression model. Regarding this result, we interpreted that the method for effectively
removing dental plaque is more important than the number of toothbrushing periods for
periodontal health, and future research should be re-evaluated by considering the toothbrushing
method as well.

This study has several limitations. First, as a cross-sectional research study, it is difficult to
reveal causal relationships between the variables used. In other words, the results of this study
did not reveal whether periodontitis increases lipid concentration in the blood or whether
dyslipidemia is a risk factor for periodontitis. Second, although the logistic regression model
demonstrated an association between the concentration of neutral fat in blood lipids and
periodontitis, the association was not as high as expected (OR:1.305; p<0.05). We interpreted
this result as being due to the overall low rate of dyslipidemia in our study subjects. In particular,
among the subjects of this study, the proportion of those with total cholesterol over 240 mg/dL
was approximately 9.7%, and the proportion of low-density lipoprotein cholesterol over 160
mg/dL was 8.6%, which was somewhat low. Additionally, because the prevalence of
dyslipidemia tends to increase with age [14], it is necessary to apply a research design that can
minimize the effect of age on the relationship between the two factors in the future. Third,
because the main purpose of this study was to prove the relationship between blood lipid types
and periodontitis, the factors involved in the development of periodontitis could not be
comprehensively used. In particular, the final logistic regression model did not confirm the
relationship between drinking experience and periodontitis, but univariate analysis results
showed that, contrary to our assumption, the prevalence of periodontitis was higher in the group
with no lifetime drinking experience. Therefore, in future studies, various confounding variables
should be considered along with longitudinal studies, and it is necessary to apply multifaceted
and in-depth evaluation methods rather than single questions. Despite these limitations, this
study used the results of the National Health and Nutrition Examination Survey, which can
represent the health status of Koreans at a time when dyslipidemia, a disease group that has
recently emerged as a health problem, is increasing, and neutral fat content was used as a
predictive factor for periodontitis. There is significance in suggesting an increase in .

conclusion

This study analyzed the relationship between dyslipidemia and periodontitis in 3,992 adults
aged 30 or older using data from the 2015 National Health and Nutrition Examination Survey,
and came to the following conclusions.

1. The prevalence of periodontitis was higher in the group of men, over 70 years of age, with
income level in the bottom 25%, and with education level of high school or lower than each
control group (p<0.001).
2. The prevalence of periodontitis was higher in groups who brushed their teeth less than twice
a day, did not use interdental cleaning tools, did not perform a dental examination in the past
year, and had never consumed alcohol or smoked in their lifetime (p< 0.05).

3. The prevalence of periodontitis was higher in groups with body mass index over 25 kg/m2
and glycated hemoglobin over 6.5% (p<0.001). Additionally, the prevalence of periodontitis was
higher in the group with abnormal concentrations of total cholesterol, high-density lipoprotein
cholesterol, low-density lipoprotein cholesterol, and triglycerides (p<0.05).
4. In a logistic regression model that controlled factors related to periodontitis, an increase in
triglycerides among serum lipids was found to increase the risk of periodontitis (p<0.05).

Through the above results, this study confirmed that dyslipidemia, especially
hypertriglyceridemia, is associated with the development of periodontitis. Therefore, we suggest
that prevention and management of dyslipidemia can improve periodontal health. Accordingly,
oral health personnel must recognize the importance of lipid metabolism for optimal oral health
and strive to provide comprehensive oral health interventions.

The authors declared no conflict of interest.

Journal of Korean society of Dental Hygiene (한국치위생학회지)

​ Volume 20 Issue 1
​ /
​ Pages.53-62
 ​ /
​ 2020
​ /
​ 2287-1705(pISSN)
​ /
​ 2288-2294(eISSN)

Korean Society of Dental Hygiene