CLINICAL RESEARCH STUDY

The Association of Tooth Scaling and Decreased Cardiovascular

Disease: A Nationwide Population-based Study
Zu-Yin Chen, MD,a,e Chia-Hung Chiang, MD,a,e Chin-Chou Huang, MD,a,b,e Chia-Min Chung, PhD,c
Wan-Leong Chan, MD,a,d Po-Hsun Huang, MD,a,e,g Shing-Jong Lin, MD, PhD,a,b,e,g Jaw-Wen Chen, MD,a,b,e,f*
Hsin-Bang Leu, MDa,d,e,g,h*
a
Division of Cardiology, Department of Medicine, bDepartment of Medical Research and Education, Taipei Veterans General Hospital,
Taipei, Taiwan; cInstitute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan; dHealthcare and Management Center, Taipei
Veterans General Hospital, Taipei, Taiwan, eCardiovascular Research Center, fInstitute of Pharmacology, gInstitute of Clinical
Medicine, National Yang-Ming University, Taipei, Taiwan, hNational Defense Medical Center, Taipei, Taiwan.

ABSTRACT

OBJECTIVE: Poor oral hygiene has been associated with an increased risk for cardiovascular disease.
However, the association between preventive dentistry and cardiovascular risk reduction has remained
undetermined. The aim of this study is to investigate the association between tooth scaling and the risk of
cardiovascular events by using a nationwide, population-based study and a prospective cohort design.
METHODS: Our analyses were conducted using information from a random sample of 1 million persons
enrolled in the nationally representative Taiwan National Health Insurance Research Database. Exposed
individuals consisted of all subjects who were aged ⱖ 50 years and who received at least 1 tooth scaling
in 2000. The comparison group of non-exposed persons consisted of persons who did not undergo tooth
scaling and were matched to exposed individuals using propensity score matching by the time of
enrollment, age, gender, history of coronary artery disease, diabetes, hypertension, and hyperlipidemia.
RESULTS: During an average follow-up period of 7 years, 10,887 subjects who had ever received tooth
scaling (exposed group) and 10,989 age-, gender-, and comorbidity-matched subjects who had not received
tooth scaling (non-exposed group) were enrolled. The exposed group had a lower incidence of acute
myocardial infarction (1.6% vs 2.2%, P ⬍ .001), stroke (8.9% vs 10%, P ⫽ .03), and total cardiovascular
events (10% vs 11.6%, P ⬍ .001) when compared with the non-exposed group. After multivariate analysis,
tooth scaling was an independent factor associated with less risk of developing future myocardial infarction
(hazard ratio [HR], 0.69; 95% confidence interval [CI], 0.57-0.85), stroke (HR, 0.85; 95% CI, 0.78-0.93),
and total cardiovascular events (HR, 0.84; 95% CI, 0.77-0.91). Furthermore, when compared with the
non-exposed group, increasing frequency of tooth scaling correlated with a higher risk reduction of acute
myocardial infarction, stroke, and total cardiovascular events (P for trend ⬍ .001).
CONCLUSION: Tooth scaling was associated with a decreased risk for future cardiovascular events.
© 2012 Elsevier Inc. All rights reserved. • The American Journal of Medicine (2012) 125, 568-575

KEYWORDS: Cardiovascular disease risk; National Health Insurance; Tooth scaling

Cardiovascular disease has become the leading cause of mor-

Funding: This work was supported by a project grant from the Taipei
Veterans General Hospital (Grant No.V98B1-010, V99B1-023, V100B-004).
Conflict of Interest: None.
Authorship: All authors had access to the data and played a role in
writing this manuscript.
*HB Leu and JW Chen contributed equally to this study.
Reprint requests should be addressed to: Hsin-Bang Leu, MD, Health-
care and Management Center, Division of Cardiology, Taipei Veterans
General Hospital, Taipei, Taiwan.
E-mail address: hbleu@vghtpe.gov.tw; jwchen@vghtpe.gov.tw
tality worldwide, accounting for approximately 30% of all
deaths. Atherosclerosis is considered not just a cholesterol
storage disorder but a sustained, dynamic, and inflammatory
process in vasculature. Because inflammation plays an impor-
tant role in the atherosclerosis process, there is continued
interest in the implication of chronic infections and inflamma-
tory diseases in atherosclerosis and cardiovascular disease.
There have been reports that poor oral hygiene, specifi-
cally periodontal disease, is associated with an increased

0002-9343/$ -see front matter © 2012 Elsevier Inc. All rights reserved.
doi:10.1016/j.amjmed.2011.10.034
Chen et al Tooth Scaling and Cardiovascular Disease 569

risk for cardiovascular disease,1 probably by adding to the Each patient’s original identification number has been
inflammatory burden of individuals. Proinflammatory me- encrypted to protect privacy by a consistent procedure, so
diators, such as C-reactive protein (CRP), interleukin-6, that the linkage of claims belonging to the same patient is
fibrinogen, von Willebrand factor, and serum amyloid A, feasible within the NHI Research Database. Because it con-
have been shown to be elevated in patients with periodontal sists of de-identified secondary data released to the public
disease.2-4 The meta-analyses dem- for research purposes, this study
onstrated poor oral hygiene with was exempt from full review by
periodontal disease had an overall the institutional review board.
CLINICAL SIGNIFICANCE
increased risk of 24% to 35% for
coronary heart disease and a higher ● Tooth scaling was associated with a de- Study Sample
risk for stroke ranging from 1.2% to creased risk of myocardial infarction The study design was a prospec-
3.0%,5-6 suggesting that poor oral hy- and stroke. tive case-cohort study. We se-
giene with periodontal disease is lected all subjects who were aged
one risk factor contributing to the ● Greater risk reduction could be obtained 50 years or more in 2000 and who
formation of cardiovascular dis- with higher frequency of tooth scaling. had received full-mouth tooth
ease. In addition, tooth brushing scaling or localized tooth scaling
● We suggest performing good oral hy-
was reported to reduce cardiovas- (exposed group) from January 1 to
cular disease risk,12 further sup-
giene and regular preventive dentistry
December 31, 2000. We used the
porting the importance of oral for all individuals, especially those with
NHI Bureau coding for treatment
hygiene in cardiovascular risk high cardiovascular risk. procedures to identify dental scal-
management. ing (91004c for full-mouth scaling
Subgingival scaling in individ- and 91003c for localized scaling).
uals with widespread periodontitis reduced serum inflam- We excluded patients who had acute myocardial infarction
matory markers.13 In the Periodontitis and Vascular (International Classification of Diseases, Ninth Revision,
Events study, any preventive or periodontal care signif- Clinical Modification [ICD-9-CM] code 410.xx) or ische-
icantly reduced the percentage of people with elevated mic stroke (ICD-9-CM codes 433.xx, 434.xx, 436, and
high-sensitivity CRP (values ⬎ 3 mg/L).9 However, there 437.1) diagnosed before 2000 to increase the likelihood of
is limited information on whether tooth scaling, meaning identifying only new cases of acute myocardial infarction
a more generalized tooth cleaning with removal of dental and stroke.
plaque and calculus, could reduce cardiovascular disease The non-exposed group was matched to the exposed
risk. The Taiwan National Health Insurance (NHI) pro- group using a propensity score, which has been widely used
gram allows beneficiaries to receive tooth scaling, unre- in control selection in large sample size databases.10,11 A
lated to the presence of severe periodontitis, or not. 1:1 propensity-score matching was performed with receiv-
Therefore, we conducted a nationwide population-based ing or not receiving tooth scaling as the dependent variable.
study using the Taiwan National Health Research Insur- The following variables were included to balance known
ance database to investigate the impact of tooth scaling risk factors across groups: the time when subjects were
on the risks for cardiovascular disease and stroke with a enrolled, age, gender, history of coronary artery disease,
prospective cohort study design. diabetes, hypertension, and hyperlipidemia. The non-ex-
posed group comprises subjects who had never received any
MATERIALS AND METHODS tooth scaling at enrollment or any time after, so there are no
cross-over subjects in our study.
Database Study end points were defined by ICD-9-CM codes for
The Taiwan NHI program, which has operated since acute myocardial infarction or ischemic stroke appearing
1995, enrolls nearly all the inhabitants of Taiwan any 1 time during hospitalization or 2 times in the ambula-
(21,869,478 beneficiaries of 22,520,776 inhabitants at the tory care center. Similar identifications for cases have been
end of 2002). The NHI Research Database at the National proven valid, and the sensitivity and specificity of identifi-
Health Research Institute in Miaoli, Taiwan, is in charge cation for events using ICD-9-CM in the National Health
of the complete NHI claims database and released a Research Insurance database compared with direct chart
dataset for research purposes. This cohort dataset com- review were 100% and 95%, respectively.12 More details
prises 1,000,000 randomly sampled beneficiaries still en- have been described in previous studies.13,14 Other covari-
rolled in the NHI program during 2000 and collected all ates, including age and preexisting (in the year before treat-
records on these individuals from 1995 to 2007. Accord- ment) hypertension (401.xx-405.xx), diabetes mellitus
ing to the Taiwan National Health Research Institute, (250.xx), hyperlipidemia (272.xx), and coronary artery dis-
there were no statistically significant differences in age, ease (411.xx-414.xx) were identified via ICD-9-CM coding.
gender, or health care costs between the sample group All patients were followed up to the study end point or
and all beneficiaries under the NHI program. December 31, 2007.
570 The American Journal of Medicine, Vol 125, No 6, June 2012

in determining the occurrence of acute myocardial infarc-

Table 1 Demographic Data of Study Population
tion, stroke, or total cardiovascular events. Subsequent sub-
Tooth Scaling group analysis was performed to investigate the effects of
tooth scaling among other risk factors for cardiovascular event,
Yes No P such as age, gender, history of diabetes mellitus, hyperlipid-
(n ⫽ 10,887) (n ⫽ 10,989) Value
emia, hypertension, and coronary heart disease. Statistical sig-
Age, y 61.09 ⫾ 8.64 61.24 ⫾ 8.8 .19 nificance was inferred at a 2-sided P value of ⬍.05.
Male, n (%) 5406 (49.7) 5423 (49.4) .65
Hypertension, n (%)* 3492 (32.1) 3597 (32.7) .30
DM, n (%)† 1734 (15.9) 1810 (16.5) .28 RESULTS
Dyslipidemia, n (%)‡ 1627 (14.9) 1712 (15.6) .19 We obtained a sample size of 21,876 subjects, including
CAD, n (%)§ 1607 (14.6) 1607 (14.6) .64 10,887 subjects who had received full-mouth or localized
Chronic renal 615 (5.7) 667 (6.1) .19
tooth scaling at least once during the study period (exposed
disease, n (%)储
group) and propensity score matched with another 10,989
Arrhythmia, n (%)¶ 759 (7.0) 695 (6.3) .06
subjects without tooth scaling (non-exposed group). There
DM ⫽ diabetes mellitus; CAD ⫽ coronary artery disease.
were no significant differences in age, gender, history of
All chronic conditions were defined by administrative claims using
ICD-9-CM codes: hypertension, diabetes, dyslipidemia, and coronary artery
*Hypertension ⫽ ICD-9-CM code: 401.xx-405.xx. diseases between these 2 groups (Table 1).
†DM ⫽ ICD-9-CM code: 250.xx. During an average follow-up period of 7 years, 408
‡Dyslipidemia ⫽ ICD-9-CM code: 272.xx. (1.8%) of the 21,876 subjects who had ever received tooth
§CAD ⫽ ICD-9-CM code: 411.xx-414.xx.
scaling therapy had acute myocardial infarction and 2062
储Chronic renal disease ⫽ ICD-9-CM code: 580.xx-587.xx.
¶Arrhythmia ⫽ ICD-9-CM code: 427.xx. subjects (9.4%) had an episode of stroke (Table 2). By
comparison, the non-exposed group had a significantly
higher incidence of acute myocardial infarction (239/10,989
subjects, 2.17%) and stroke (1099 patients, 10.00%), indi-
Statistical Analysis cating that tooth scaling was associated with a reduced risk
We used Microsoft SQL Server 2005 (Microsoft Corp, of cardiovascular event development. During the follow-up
Redmond, Wash) for data management and computing and period, the patients with full-mouth or localized tooth scal-
SPSS software (v. 15.0, SPSS Inc, Chicago, Ill) for statis- ing had significantly higher acute myocardial infarction–
tical analysis. All data were expressed as the frequency free survival (Figure 1A), higher stroke-free survival (Fig-
(percentage) or mean ⫾ standard deviation. The parametric ure 1B), and higher total cardiovascular event-free survival
continuous data between the exposed and non-exposed (Figure 1C) than subjects in the non-exposed group. The
groups were compared by unpaired Student’s t-test. The results of log-rank test and Kaplan-Meier survival analyses
categoric data between the 2 groups were compared with of acute, stroke, and total cardiovascular events are shown
chi-square test and Yates’ correction or Fisher exact test as in Figure 1A-C, respectively. In addition, the association
appropriate. Survival analysis was assessed using Kaplan- between tooth scaling and malignancy occurrence was an-
Meier analysis, with the significance based on the log-rank alyzed, and there was no difference in cancer incidence
test. The survival time was calculated from the date of between the exposed and non-exposed groups (10.48% vs
enrollment to the date of diagnosis of acute myocardial 10.21%, P ⫽ .52).
infarction or stroke. Multiple regression analysis was car- Cox proportional hazard regression model analysis
ried out using Cox proportional hazard regression analysis showed that tooth scaling was independently associated
to evaluate whether tooth scaling was an independent factor with less risk of developing future myocardial infarction

Table 2 Association Between Tooth Scaling and Cardiovascular Events

Events Crude HR (95% CI) Adjusted HR (95% CI)*

Tooth Tooth Tooth Tooth Tooth Tooth

Total Scaling (⫺) Scaling (⫹) Scaling (⫺) Scaling (⫹) Scaling (⫺) Scaling (⫹)
AMI 408 239 (2.2%) 169 (1.6%) 1 (referent) 0.72 (0.59-0.87)† 1 (referent) 0.69 (0.57-0.85)†
Stroke 2062 1099 (10%) 963 (8.9%) 1 (referent) 0.87 (0.80-0.95)† 1 (referent) 0.85 (0.78-0.93)†
Total cardiovascular 2366 1274 (11.6%) 1092 (10%) 1 (referent) 0.86 (0.79-0.93)† 1 (referent) 0.84 (0.77-0.91)†
events
HR ⫽ hazard ratio; AMI ⫽ acute myocardial infarction.
*Adjusted for age, gender, history of hypertension, diabetes mellitus, hyperlipidemia, dysrhythmia, and chronic kidney disease.
†P ⬍.05.
Chen et al Tooth Scaling and Cardiovascular Disease
Figure 1 Kaplan-Meier estimates of survival free of cardio-
vascular events, including acute myocardial infarction (A), stroke
(B), and total cardiovascular event (C) in subjects categorized by
tooth scaling. The event-free survival was significantly different
in the 2 groups (log-rank test, P ⫽ .001, P ⫽ .002, and P ⬍.001,
respectively). AMI ⫽ acute myocardial infarction.
571
(hazard ratio [HR], 0.69; 95% confidence interval [CI],
0.57-0.85), stroke (HR, 0.85; 95% CI, 0.78-0.93), and com-
posite events (HR, 0.84; 95% CI, 0.77-0.91) after adjusting
for age, gender, hypertension, diabetes mellitus, hyperlip-
idemia, chronic renal failure, and history of coronary artery
disease (Table 2).
Furthermore, the HR of experiencing a myocardial in-
farction during the 7-year follow-up period was 0.61 times
less in patients receiving tooth scaling more than once every
2 years (95% CI, 0.46-0.81) and 0.80 (95% CI, 0.63-1.00)
times less in the less frequent tooth scaling group than in the
group without tooth scaling during the follow-up period. As
for stroke, a greater risk reduction was observed in patients
who received tooth scaling at a frequency of more than once
every 2 years (HR, 0.81; 95% CI, 0.73-0.92 vs HR, 0.92;
95% CI, 0.83-1.02 for tooth scaling at a frequency of less
than once every 2 years) (Figure 2). This association be-
tween frequency of tooth scaling and reduced risk also
remained for total cardiovascular events (HR, 0.90; 95% CI,
0.82-0.99 vs HR, 0.79; 95% CI, 0.71-0.88 for frequent and
occasional tooth scaling, respectively). The decreased risk
of acute myocardial infarction, stroke, and total cardiovas-
cular complications decreased gradually in association with
increasing tooth scaling frequency (P for trend ⬍ .001), indi-
cating tooth scaling was associated with a reduced risk in
developing cardiovascular events. The subgroup analyses fur-
ther demonstrated that the association existed independently
with other established cardiovascular risk factors (Figure 3).
DISCUSSION
Our study showed that patients who received tooth scaling
had a significantly lower incidence of acute myocardial
infarction and stroke when compared with the non-exposed
group. Further analysis showed that the frequency of tooth
scaling was strongly associated with the risk reduction of
cardiovascular events, further suggesting a negative associ-
ation between tooth scaling and cardiovascular disease risk.
There is considerable attention on oral hygiene and its
role in the cause of cardiovascular disease. Poor oral hy-
giene is the major cause of periodontal disease, which is an
infectious disease of the periodontium caused by a group of
predominantly anaerobic Gram-negative bacteria present on
the tooth surface. Periodontal disease has been reported to
be associated with an increased risk for cardiovascular dis-
ease, peripheral vascular disease, and stroke.15-20 In their
analysis of different observational study designs, Bahekar et
al6 demonstrated a higher risk of developing cardiovascular
disease in patients with periodontal disease in prospective
cohort studies (relative risk, 1.14; 95% CI, 1.07-1.21),
cross-sectional studies (odds ratio [OR], 1.59; 95% CI,
1.33-1.91), and case-control studies (OR, 2.22; 95% CI,
1.59-3.12). A study of 9962 adults who participated in the
First National Health and Nutrition Examination Survey
found that the relative risk for incident non-hemorrhagic
stroke was 1.24 (95% CI, 0.74-2.08) for gingivitis, 2.11
(95% CI, 1.30-3.42) for periodontitis, and 1.41 (95% CI,
572
Figure 2 The association between tooth scaling frequency and cardiovascular events by
proportional hazards regression analysis, adjusted for age, gender, history of hypertension,
diabetes mellitus, hyperlipidemia, dysrhythmia, and chronic kidney disease.
0.96-2.06) for edentulousness.17 Data from the Normative
Aging Study and Dental Longitudinal Study of the US
Department of Veterans Affairs (follow-up period of 25-30
years) also demonstrated that periodontal disease was a
significant independent risk factor for peripheral vascular
disease (OR, 2.27; 95% CI, 1.3-3.9).20 This association was
even more significant with increasing severity of periodon-
tal disease,1,21,22 indicating the close relationship between
periodontal disease and cardiovascular risk.
There are many proposed mechanisms to explain the
relationship between periodontal disease and cardiovascular
disease. First, periodontal disease represents a chronic in-
fection that leads to chronic inflammation, increasing circu-
lating cytokines such as CRP, interleukin-1␤, interleukin-6,
tumor necrosis factor-␣, fibrinogen, von Willebrand factor,
and serum amyloid A,18,23,24 which would in turn increase
atherosclerosis. Periodontitis also is associated with in-
creased concentrations of plasma lipids, such as total and
low-density lipoprotein cholesterol and triglycerides, per-
haps by increased systemic inflammatory burden.25 Peri-
odontal infection may lead to endothelial dysfunction, in-
flammation, and atherosclerosis.23 Furthermore, the
atherosclerotic process impairs endothelial functions and
induces functional and structural changes in vascular
smooth muscle in patients with periodontitis.26 Periodontal
pathogens, such as Porphyromonas gingivalis, Fusobacte-
rium nucleatum, and Actinobacillus actinomycetemcomi-
tans, have been identified in atherosclerotic plaques.27,28
The Atherosclerosis Risk in Communities Study reported
that patients with poor oral hygiene and severe generalized
periodontitis have higher carotid intima-media wall thick-
ness,29 furthermore highlighting the relationship between
The American Journal of Medicine, Vol 125, No 6, June 2012
periodontal disease and increased risk of cardiovascular
disease.
Dental calculus (plaque) consists of bacterial content that
may irritate and inflame gingiva, leading to periodontitis.
Periodontal treatment, defined as subgingival scaling and
root planning, was associated with decreased levels of in-
flammatory cytokines.30 Periodontal treatment decreases se-
rum inflammatory markers, such as CRP and periodontal
interleukin-6.8,31,32 In addition to decreasing inflammatory
markers, periodontal treatment may decrease the surrogate
end point of cardiovascular disease, including lipoprotein-
associated phospholipase A2,33-35 endothelial dysfunction,36
and intima-media thickness.37 To our knowledge, the cur-
rent study is the first to investigate the association between
tooth scaling and future cardiovascular events by using a
large nationwide population-based study. Our study finding
that the risk of acute myocardial infarction, stroke, and total
cardiovascular complications decreased gradually in asso-
ciation with increasing tooth-scaling frequency further ex-
tends the clinical observation that periodontal treatment
may provide a protective benefit in decreasing the develop-
ment of cardiovascular disease. The self-reported frequency
of tooth brushing was associated with decreased cardiovas-
cular disease events (HR, 1.7; 95% CI, 1.3-2.3) and CRP
levels in a study of 11,869 individuals in the Scotland
Health Survey,7 which is in concordance with our study,
indicating that oral hygiene may provide an additional ben-
efit in preventing cardiovascular events.
Study Strengths and Limitations
The strength of our study is the use of a population-based
dataset, which enrolls a large sample size and enables us to
Chen et al Tooth Scaling and Cardiovascular Disease 573

Figure 3 HRs of tooth scaling for events of acute myocardial infarction (A), stroke (B), and total cardiovascular events
(C) in subgroup analysis; by proportional hazards regression analysis, adjusted for age, gender, history of hypertension,
diabetes mellitus, hyperlipidemia, dysrhythmia, and chronic kidney disease. AMI ⫽ acute myocardial infarction;
CI ⫽ confidence interval; HR ⫽ hazard ratio.

prospectively trace the differences between 2 groups. How-
ever, there are still some limitations in our study. First, the
diagnoses of acute myocardial infarction and stroke are
identified using the ICD-9 codes from the database. Al-
though diagnoses rely largely on administrative claims data
reported by physicians or hospitals, and may be less accu-
rate than diagnoses made according to standardized criteria,
previous studies using ICD-9 coding in the same database
have shown high sensitivity (100%) and specificity (95%) in
identifying cardiovascular events.12-14 Second, a common
574
Figure 3
bias in studies using databases is the immortal time bias.
However, our study enrolled subjects in the exposed
group if their first tooth scaling was performed in 2000,
and the enrolled index date is the first day they receive
tooth scaling. Therefore, there is no immortal time bias in
our study. Third, some important cardiovascular disease
risk factors, such as smoking, body mass index, alcohol
consumption, dietary factor, and family history are not
available and may result in compromised findings and an
inadequate adjustment of confounding factors. Smoking,
in particular, is of major concern. However, oral hygiene
studies conducted in Taiwan have shown that approxi-
mately 10% to 20% of the study population are smok-
ers,38,39 suggesting smokers are less likely to seek pre-
ventive dental care. Fourth, the NHI provides tooth
scaling for all beneficiaries once per year. It is not man-
datory and may be unrelated to clinical severity of peri-
odontitis. Because of the limitation of the database, the
prevalence of periodontitis cannot be identified in both
groups. Therefore, the possibility of selection bias cannot
be excluded. Finally, more than 98% of the residents in
Taiwan are of Chinese ethnicity. The ability to generalize
the results to other racial/ethnic groups is unclear. Fur-
ther study is needed to confirm our findings and their
relevance in relation to other ethnic groups.
CONCLUSIONS
The present study suggests that tooth scaling is associated
with a decreased risk for acute myocardial infarction,
The American Journal of Medicine, Vol 125, No 6, June 2012
Continued
stroke, and total cardiovascular events, with the greatest risk
reduction observed in patients who received tooth scaling at
higher frequencies. It supports the growing evidence of poor
oral hygiene as a risk factor for cardiovascular disease. Our
findings support tooth scaling in addition to daily tooth
brushing to improve oral hygiene and reduce the risk of
cardiovascular disease.
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