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Eurheartj 40 14 1138
Eurheartj 40 14 1138
Received 24 May 2018; revised 3 September 2018; editorial decision 22 November 2018; accepted 22 November 2018; online publish-ahead-of-print 18 December 2018
See page 1146 for the editorial comment on this article (doi: 10.1093/eurheartj/ehz060)
Aims Oral health problems such as periodontal disease, dental caries, and tooth loss have been suggested to have associ-
ations with cardiovascular disease. This study aimed to evaluate whether oral hygiene behaviour can alleviate car-
diovascular risk associated with oral health status using a nationwide population-based cohort.
...................................................................................................................................................................................................
Methods The data of 247 696 healthy adults aged 40 years or older who underwent an oral health screening programme
and results and had no history of major cardiovascular events were extracted from the National Health Insurance System-
National Health Screening Cohort. After a median follow-up of 9.5 years, 14 893 major cardiovascular events
occurred including cardiac death, myocardial infarction, stroke, and heart failure. The risk of cardiovascular events
was higher when a subject had periodontal disease, a higher number of dental caries, or more tooth loss.
Performing one more tooth brushing a day was associated with a 9% significantly lower risk of cardiovascular
events after multivariable adjustment. Regular dental visits (once a year or more) for professional cleaning were
also shown to reduce cardiovascular risk by 14%. Improved oral hygiene behaviours were shown to attenuate the
cardiovascular risk originating from periodontal disease, dental caries, and tooth loss.
...................................................................................................................................................................................................
Conclusion Oral hygiene care such as frequent tooth brushing and regular dental visits for professional cleaning reduced the
risk of future cardiovascular events in healthy adults. This study also suggests that improved oral hygiene behaviour
may modify the association between oral health and cardiovascular diseases.
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..
.. cardiovascular disease is yet unclear.7,8 The two diseases share com-
Introduction .. mon risk factors such as smoking, diabetes, and advanced age. The
..
The link between oral health and cardiovascular disease has been .. issue has potential impact because both the conditions have a high in-
debated.1,2 Observational studies have shown a positive association .. cidence; while cardiovascular disease is the leading cause of death
..
between the two diseases.3–5 Periodontal disease causes transient .. worldwide, oral health disease is one of the most common diseases
bacteraemia, systemic inflammation, and endothelial dysfunction, .. and is closely linked to daily activities.9–11
..
which are possible mechanisms underlying atherogenesis.6 However, .. Periodontal diseases are preventable.12 Bacterial plaque on the
limited evidence supports a causal relationship between the two dis-
.. dental surface is the main cause of gingivitis and periodontitis,
..
eases, and the therapeutic benefit of periodontal treatment for . which may result in dental caries and tooth loss.13 Daily personal
* Corresponding author. Tel: 182 31 787 7027, Fax: 182 31 787 4290, Email: eandp303@snu.ac.kr
Published on behalf of the European Society of Cardiology. All rights reserved. V
C The Author(s) 2018. For permissions, please email: journals.permissions@oup.com.
Oral health disease, oral hygiene, and cardiovascular outcomes 1139
Definitions
Periodontal disease was defined as the presence of the following
..
International Statistical Classification of Diseases and Related Health Problems, .. chronic periodontitis (K053), periodontosis (K054), other periodontal
Tenth Revision (ICD-10) codes more than two times or a periodontal .. disease (K055), and unspecified periodontal disease (K056). Dental caries
treatment with the following ICD-10 codes: acute periodontitis (K052),
.. and tooth loss were ascertained by dentists during the oral examination.
1140 S.-Y. Park et al.
The number of dental caries was categorized as 0, 1–5, and >_6. The num- .. occurrence of major cardiovascular events. Hazard ratios (HRs) and 95%
..
ber of lost teeth was categorized as 0, 1–7, 8–14, 15–21, and 22–28. .. confidence intervals (CIs) were calculated. Multivariable regression mod-
Personal oral hygiene behaviour was classified by the number of tooth .. els were constructed with adjustment for (i) age and sex; (ii) age, sex,
brushings a day: 0–1, 2, and >_3 times a day. Regular dental visits for pro-
.. hypertension, diabetes, dyslipidaemia, renal disease, body mass index, sys-
..
fessional cleaning were classified as <1 and >_1 time a year. .. tolic blood pressure, malignancy, income level, regular physical activity,
The main study outcome was the occurrence of major cardiovascular
.. and current smoking status; and (iii) for the variables listed above, as well
..
events, which was defined as a composite of cardiovascular death, acute .. as for oral health and hygiene variables. The assumption of proportional
myocardial infarction, heart failure, and stroke. Cardiovascular mortality .. hazards was tested on the basis of scaled Schoenfeld residuals. When the
.. assumption was violated, an interaction term between covariates and a
was defined using specific causes of death according to the ICD-10 codes ..
(I00–I99). Acute myocardial infarction was defined as a hospitalization .. function of time was included. Variance inflation factors were used to de-
with ICD-10 codes I21–23 as the primary or secondary diagnosis. Heart
.. tect multi-collinearity in the regression models.
..
failure was defined based on discharge diagnosis (ICD-10 codes: I11.0, .. Next, we assessed whether the associations between oral hygiene
I13.0, I13.2, I25.5, I42, I50, and O90.3) after a hospitalization. Stroke was .. care and cardiovascular risk differed according to the presence of oral
..
defined by a discharge diagnosis (ICD-10 codes: I60–64) among patients .. health diseases. The cardiovascular effect of oral hygiene was stratified by
who had been hospitalized and had undergone brain imaging studies such .. oral health status. Interactions of oral health status and oral hygiene be-
as computed tomography and magnetic resonance imaging.20 .. haviour regarding cardiovascular outcomes were calculated. Significance
..
.. of the unadjusted and adjusted effects of each independent variable on
Statistical analysis .. major cardiovascular events was judged by Bonferroni-corrected a levels
.. of 0.0025 (=0.05/20). Statistical analyses were conducted using STATA
Baseline characteristics are reported using numbers (%) for categorical ..
variables and means ± standard deviation for continuous variables. The
.. (STATA/SE14 software, Stata Corp, College Station, TX, USA) and R
.. programming version 3.2.4 (http://www.R-project.org; The R Foundation
v2 test was performed for categorical variables and Student’s t-test or ..
analysis of variance test was used for continuous variables. Kaplan–Meier .. for Statistical Computing, Vienna, Austria).
..
survival curves were constructed to determine the effects of oral health ..
diseases and oral hygiene behaviours on the incidence of cardiovascular ..
events. The 10-year events were calculated by dividing the number of
.. Results
..
patients with major cardiovascular events by the sum of the follow-up ..
duration. Age- and sex-adjusted event rates were estimated using stand- .. The study population comprised 247 696 healthy adults who had no
.. history of major cardiovascular events. The median participant
ardized incidence ratio. Cox proportional hazard models were used to ..
evaluate the associations between the independent variables and the . age was 52 years; 58.0% were men, 19.9% had hypertension, and
Table 2 Risk of composite cardiovascular events according to oral health disease and oral hygiene care
Events/n Event rate (%) Unadjusted model Age, sex-adjusted model Multivariable adjusted (1) Multivariable adjusted (2)
..................................... .......................................... ............................................ ............................................
HR (95% CI) P-value HR (95% CI) P-value HR (95% CI) P-value HR (95% CI) P-value
................................................................................................................................................................................................................................................................................................
Periodontal disease
Absent 10 098/172 043 6.6 Reference <0.001 Reference 0.031 Reference 0.228 Reference 0.964
Present 4594/75 653 7.6 1.17 (1.13–1.21) 1.04 (1.00–1.08) 0.98 (0.94–1.01) 1.00 (0.96–1.04)
Number of dental caries
0 12 001/203 050 6.7 Reference <0.001 Reference <0.001 Reference <0.001 Reference -<0.001
1–5 2686/42 372 7.1 1.04 (1.00–1.09) 1.10 (1.06–1.15) 1.09 (1.04–1.14) 1.07 (1.02–1.12)
>_6 206/2274 10.6 1.56 (1.36–1.79) 1.32 (1.15–1.51) 1.28 (1.11–1.48) 1.22 (1.06–1.42)
Number of missing teeth
0 10 183/187 160 6.2 Reference <0.001 Reference <0.001 Reference <0.001 Reference <0.001
Oral health disease, oral hygiene, and cardiovascular outcomes
1–7 3670/53 366 7.9 1.29 (1.25–1.34) 1.12 (1.07–1.16) 1.05 (1.01–1.09) 1.04 (0.99–1.08)
8–14 598/4743 15.3 2.49 (2.29–2.70) 1.30 (1.20–1.41) 1.20 (1.10–1.31) 1.16 (1.06–1.27)
15–21 258/1505 21.7 3.54 (3.13–4.00) 1.45 (1.28–1.64) 1.30 (1.14–1.48) 1.27 (1.11–1.45)
22–28 184/922 26.0 4.24 (3.66–4.90) 1.42 (1.22–1.64) 1.44 (1.24–1.67) 1.43 (1.23–1.66)
Number of tooth brush (times/day)
0–1 3282/36 417 10.4 Reference <0.001 Reference <0.001 Reference <0.001 Reference <0.001
2 7149/111 038 7.3 0.70 (0.67–0.73) 0.86 (0.82–0.89) 0.86 (0.82–0.90) 0.87 (0.83–0.91)
>_3 4462/100 241 5.1 0.49 (0.46–0.51) 0.74 (0.70–0.77) 0.78 (0.74–0.82) 0.79 (0.75–0.83)
Professional dental cleaning
<1/year 3115/181 048 7.3 Reference <0.001 Reference <0.001 Reference <0.001 Reference <0.001
>_1/year 11 580/63 266 5.6 0.78 (0.75–0.81) 0.90 (0.86–0.93) 0.89 (0.86–0.93) 0.90 (0.87–0.94)
Event rates were reported in 10-year event rates (%). Multivariable model (1) was adjusted for age, sex, income levels, regular exercise, body mass index (kg/m2), systolic blood pressure (mmHg), hypertension, diabetes, dyslipidaemia, cur-
rent smoker, renal disease, and malignancy history. Multivariable model (2) was adjusted for the variables listed above as well as periodontal disease, dental caries, missing teeth, tooth brushing, and professional dental cleaning. P-values indi-
cate P-values for trend.
CI, confidence interval; HR, hazard ratio.
1141
..
21.8% were current smokers (Table 1). The medians of body .. cleaning reduced the risk by 14%, independent of potential confound-
mass index, blood pressure, and total cholesterol were 23.9 kg/m2, .. ing factors or oral health problems (HR: 0.86; 95% CIs: 0.82–0.90;
..
125/80 mmHg, and 197 mg/dL, respectively. Approximately 30%, .. P < 0.001). Frequent tooth brushing and regular professional cleaning
20%, and 25% of the participants had periodontal disease, at least one .. provided additive benefits (Figure 2). Analyses for each component of
..
dental caries, and had lost one or more teeth, respectively. .. cardiovascular events are shown in Supplementary material online,
According to the self-reported questionnaires, 40.5% of the study .. Tables S6–S10.
..
subjects brushed their teeth three times or more a day, 44.8% twice .. The interplay between oral health status and oral hygiene is shown
a day, and 14.7% once or less a day. More than one-fourth (25.9%) .. in Figure 3 (see Supplementary material online, Tables S11–S13).
..
reported having dental visits for professional cleaning at least once a .. Frequent tooth brushing and regular professional cleaning were asso-
year. Supplementary material online, Tables S1–S5 compare the base- .. ciated with improved cardiovascular outcomes even in subjects with
..
line characteristics of the study subjects according to their dental .. poor oral conditions. However, the benefit of tooth brushing was
health status, tooth brushing habits, and number of dental visits for .. more remarkable when periodontal disease was absent, and the
..
professional cleaning procedures. .. number of dental caries was low. The favourable effect of tooth
After a median follow-up of 9.5 years, 14 893 major cardiovascu- .. brushing was not modified by the number of tooth loss. The advan-
..
lar events occurred (10-year event rate of 6.84%). The estimated .. tage of professional cleaning was consistent across all stratified
10-year event rates were 5.31% for all-cause mortality, 1.01% for
.. analyses.
..
cardiac death, 1.48% for acute myocardial infarction, 2.21% for ..
heart failure, and 3.58% for stroke. Figure 1 shows the survival
..
..
curves free from cardiovascular events according to oral health .. Discussion
disease and oral hygiene behaviour. The risk for cardiovascular
..
..
events was higher when a subject was diagnosed as having peri- .. In this study, we found that periodontal disease, an increased number
odontal disease, had a higher number of dental caries, and had lost
..
.. of dental caries, and greater tooth loss were associated with future
a higher number of teeth. In contrast, healthy oral hygiene behav- .. adverse cardiovascular events. In contrast, better oral hygiene care
..
iours including frequent tooth brushing and regular dental visits for .. such as frequent tooth brushing and regular dental visits for profes-
professional cleaning procedures were associated with significantly .. sional cleaning procedures were associated with a lower cardiovascu-
..
better cardiovascular outcomes. .. lar risk. The benefit of oral hygiene was independent of potential
Table 2 shows the multivariable-adjusted analysis for the impact of .. confounding factors and oral health status. This study suggests that
..
dental health and behavioural variables on composite cardiovascular .. better oral hygiene behaviour may modify the risk associated with
events. The effects of the independent variables were largely attenu- .. periodontal disease, dental caries, and tooth loss.
..
ated after adjustment for age and sex. While the effect of periodontal .. Previous observational studies have reported the association of
disease lost statistical significance after adjustment, the number of .. oral health problems such as periodontal disease, dental caries, and
..
missing teeth and dental caries, tooth brushing, and professional .. tooth loss with atherosclerotic cardiovascular disease.21,22 However,
cleaning remained significant. Brushing teeth one more time a day .. as stated by the American Heart Association, evidence supporting a
..
was associated with a 9% lower risk of cardiovascular events (HR: .. causal relationship is weak.1 The present study also found that the as-
0.91; 95% CIs: 0.89–0.93; P < 0.001), while regular professional .. sociation between periodontal disease and adverse cardiovascular
Oral health disease, oral hygiene, and cardiovascular outcomes 1143
Figure 3 Interaction between oral health disease and oral hygiene behaviours. Periodontal disease with (A) tooth brushing and (B) professional
dental cleaning. The number of dental caries with (C) tooth brushing and (D) professional dental cleaning. The number of tooth loss with (E) tooth
brushing and (F) professional dental cleaning. The squares and vertical lines indicate the hazard ratio and 95% confidence intervals, respectively. The
models were adjusted for age, sex, hypertension, diabetes, dyslipidaemia, renal disease, body mass index, systolic blood pressure, malignancy, and cur-
rent smoking status. Int P, interaction P-values.
1144 S.-Y. Park et al.
..
of periodontal disease or dental caries. In contrast, if the subject has .. Funding
already lost a significant number of teeth, an improvement in personal .. This work was supported by the Seoul National University Bundang
..
oral health behaviour would be insufficient to reduce cardiovascular .. Hospital Research Grant (18-2018-012).
risk. However, we still believe higher-quality evidence is required to ..
.. Conflict of interest: none declared.
establish the role of oral hygiene in cardiovascular prevention. ..
..
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