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J Clin Periodontol 2009; 36: 750–755 doi: 10.1111/j.1600-051X.2009.01448.

Periodontal health, oral health Zuomin Wang1, Xuan Zhou1,n,


Jing Zhang1, Liangqiong Zhang1,
Yiqing Song2, Frank B. Hu3 and

behaviours, and chronic Chen Wang4


1
Department of Stomatology, Beijing
ChaoYang Hospital, Capital Medical

obstructive pulmonary disease University, Beijing, China; 2Division of


Preventive Medicine, Brigham & Women’s
Hospital, Harvard Medical School, Boston,
MA, USA; 3Departments of Nutrition and
Epidemiology, Harvard School of Public
Wang Z, Zhou X, Zhang J, Zhang L, Song Y, Hu FB, Wang C. Periodontal health, oral Health, Boston, MA, USA; 4Department of
health behaviours, and chronic obstructive pulmonary disease. J Clin Periodontol Respiratory Medicine, Beijing ChaoYang
2009; 36: 750–755. doi: 10.1111/j.1600-051X.2009.01448.x. Hospital, Capital Medical University, Beijing,
China
Abstract
Aim: To evaluate the associations of periodontal health status and oral health
behaviours with chronic obstructive pulmonary disease (COPD).
Materials and Methods: We conducted a case–control study of 306 COPD patients
and 328 controls with normal pulmonary function. Their periodontal status and
respiratory function were clinically examined and information on oral health
behaviours was obtained using a validated questionnaire.
Results: Patients with COPD had fewer teeth and a higher plaque index than the
controls. Univariate analysis showed that tooth brushing times and method, experience
of dental floss use, dental visit and regular supra-gingival scaling, and oral health
knowledge were significantly related to the risk of COPD. After adjusting for age, sex,
and body mass index and stratifying by smoking status, inappropriate tooth brushing
method (p 5 0.025 among non-smokers), lower regular supra-gingival scaling
(p 5 0.027 among non-smokers and po0.0001 among former smokers), and poorer
oral health knowledge (po0.0001 among non-smokers and p 5 0.019 among former
smokers and p 5 0.044 among current smokers) remained significantly associated with
COPD.
Key words: case–control study; Chinese
Conclusions: Poor periodontal health, dental care, and oral health knowledge were subjects; chronic obstructive pulmonary
significantly associated with an increased risk of COPD. Our findings indicate the disease; oral health; periodontitis; risk factors
importance of promoting dental care and oral health knowledge that can be integrated
into the prevention and treatment of COPD. Accepted for publication 7 June 2009

Conflict of interest and source of Chronic obstructive pulmonary disease periodontal lesions induce systemic
funding statement (COPD) is one of the most common and inflammation, which may contribute to
costly respiratory diseases. The high the pathogenesis of COPD (Terpenning
The authors declare that they have no
conflict of interests related to this study.
prevalence and mortality of COPD 2001).
This study was supported by the Interna- worldwide pose an immense public Recent reports have implicated that
tional Science and Technology Coopera- health and medical challenge for the periodontitis is associated with several
tion research grant of Beijing Municipal implementation of effective preventive other diseases including type 2 diabetes
Science and Technology Commission and treatment strategies (Murray & mellitus, cardiovascular disease, and
(2006, Beijing, China). The funding orga- Lopez 1997). The aetiology of COPD respiratory system diseases (Ryan
nization played no role in the design and is complex and multifactorial, involving et al. 2003, Taylor 2003, Seymour
conduct of the study; in the collection, multiple genetic and environmental fac- et al. 2007). Three cross-sectional epi-
analysis, and interpretation of the data; or tors such as smoking and air pollution demiological studies suggested an asso-
in the preparation, review, or approval of
(Rabe et al. 2007). Periodontitis is a ciation between poor oral health
the manuscript.
chronic inflammatory reaction to bacter- (including oral hygiene index, alveolar
ial infections that results in the destruc- bone loss, and periodontal attachment
tion of the supporting connective tissue loss) and chronic pulmonary disease
and bone of the dentition. Oral patho- (Hayes et al. 1998, Scannapieco et al.
n
Co-first author with equal contribution.
gens and inflammatory cytokines from 1998, Scannapieco & Ho 2001),

750 r 2009 John Wiley & Sons A/S


Oral health and COPD 751

although the precise mechanisms under- were conducted throughout the survey fixed ratio post-bronchodilator FEV1/
lying such relationships remain unclear. to repeatedly assess intra-examiner FVCo0.70.
A weak association between periodontal reliability. The k value of agreement
disease and COPD has also been was 0.82. The evaluation included
Measurement of oral health behaviour-
described (Scannapieco et al. 2003, periodontal probing, oral hygiene, num-
related variables
Katancik et al. 2005, Azarpazhooh & ber of teeth present, and X-ray exam-
Leake 2006). One case–control study ination of alveolar bone. Periodontal Detailed information on oral health
reported a significant association probing included probing depth (PD), behaviours was obtained using a stan-
between periodontal disease and airway location of the cemento-enamel junction dardized questionnaire as validated and
obstruction, particularly in former smo- (CEJ) to determine clinical attachment widely used in a Chinese National Oral
kers (Kowalski et al. 2005); another level (CAL), and bleeding index (BI) on Health Epidemiology Survey (Qi et al.
study suggested that worse periodontal probing. PD and CEJ were measured 2008). The questionnaire included tooth
diseases significantly increased the risk with a Williams periodontal probe at six brushing times, tooth brushing methods,
of COPD in subjects who were current sites of all teeth (excluding third molars) dental floss use, frequency of dental
smokers (Garcia et al. 2001). Didilescu and recorded in millimetres. Recession visits, periodontal treatment, and assess-
et al.’s (2005) study indicated that den- was recorded as a positive value if the ment of oral health knowledge. Twenty-
tal plaque in patients with chronic lung free gingival margin occurred apical to one oral health questions were asked to
diseases often serves as a reservoir of the CEJ, whereas it was recoded as a assess oral health knowledge using a
bacteria known to cause nosocomial negative value if it was coronal to the score based on their answers to ques-
pneumonia in susceptible individuals. CEJ. CAL was calculated using the tions such as do you think dental plaque
Because of limited data, little is known formula PD1CEJ 5 CAL. BI on prob- is the main cause of periodontitis or do
about the relation of oral health care ing was scored on a 0–5 scale when any you think oral diseases can cause other
with COPD. Therefore, we conducted a visual evidence of bleeding was noted diseases such as diabetes mellitus or
case–control study to examine the rela- (Mazza et al. 1981). The plaque index cardiovascular disease? In addition,
tion of periodontal health status and oral (PLI) for each tooth was determined on information on smoking status and alco-
health-related behaviours with the risk a 0–3 scale after air drying (Silness & hol drinking status was also collected
of COPD in a Chinese population. Löe 1964). Alveolar bone loss was using the same questionnaire.
examined using full-mouth series of
intra-oral periapical films. Bone loss at
Statistical analysis
Materials and Methods each mesial and distal interproximal site
Study population was assessed: 1 5 alveolar bone loss SPSS statistical package (Version 12.0,
less than 1/3 of the root in length; SPSS Inc., Chicago, IL, USA) was used
We conducted a case–control study in 2 5 alveolar bone loss between 1/3 and for the data analysis. An independent-
which a total of 306 COPD patients and 2/3 of the root in length; and 3 5 alveo- sample t-test, and w2-test were used to
328 participants with normal pulmonary lar bone loss more than 2/3 of the root in compare the baseline characteristics and
function were recruited from Beijing length. Dental caries and oral mucosal periodontal status between cases and
ChaoYang hospital and other seven hos- were also evaluated. controls for continuous variables and
pitals in Beijing. From March 2007 to categorical variables, respectively.
November 2008, consecutive patients Logistic regression was performed to
who were 30 years of age or older were calculate the odds ratio (OR) and 95%
recruited. The patients should have more Diagnosis of COPD and assessment of
lung function confidence interval (CI) for evaluating
than 15 teeth, all in stable stage and have the associations of periodontal health
no exacerbations of symptoms in the past The criteria used for the diagnosis of status and oral health behaviours with
1 month at recruitment (Rabe et al. 2007). COPD are based on the Global Initiative the risk of COPD. In the multivariate-
All COPD cases were clinically diag- for Chronic Obstructive Lung Disease adjusted models, we included age, gen-
nosed and confirmed by lung function (GOLD) spirometry guidelines: Global der, and body mass index (BMI) to
examination. Controls were randomly Strategy for the Diagnosis, Manage- control for potential confounding.
selected from all eligible patients with ment, and Prevention of COPD (update Because smoking could be an important
normal lung function in the same hospi- 2007) (Rabe et al. 2007). effect modifier for the relation of perio-
tals. All participants were interviewed at Lung function was measured using dontal disease and COPD (Hyman &
recruitment by trained interviewers. spirometry. The spirometric measure- Reid 2004), our logistic regression ana-
The human research ethnical board ments were conducted by trained and lyses were stratified by smoking status
from Beijing ChaoYang hospital ap- certified technicians. During at least (non-smoker, former smoker, and cur-
proved the study, and written informed five forced expirations, the technician rent smoker).
consent was obtained from all the parti- attempted to obtain three acceptable
cipants. spirograms, at least two of which
showed similar results for forced expira- Results
Periodontal examination
tory volume (FEV) in 1 s (FEV1) and Demographics
forced vital capacity (FVC). The pul-
The oral health examinations were con- monary evaluation was based on the The basic demographic characteristics
ducted by two trained dentists who were FEV1/FVC and then used the percent of the study population are presented in
blinded to the study design and patients of predicted FEV1 to categorize sever- Table 1. The mean age of the COPD
COPD status. Replicate examinations ity. Air limitation was defined using the group was 63.94  9.84 years; 68.6%
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752 Wang et al.

were males and 31.4% were females. There was no significant difference in o0.17). Compared with the control
The mean age of the control group was other periodontal indexes (PD, BI, and group, the group of COPD patients had
63.26  8.98 years; 50.0% were males alveolar bone loss) between COPD lower tooth brushing times (po0.0001)
and 50.0% were females. Compared cases and controls. After adjusting for and oral health knowledge scores
with the controls, COPD patients had a age, gender, and BMI and stratifying by (po0.0001) (Table 4). Also, patients
greater proportion of former and current smoking status in the logistic regression had a higher proportion of the use of
smokers (po0.0001). There was no models, the number of remaining teeth the horizontal tooth brushing method
difference in the mean BMI of patients (p 5 0.045) among non-smokers and (51.2% versus 36.1%, po0.0001), a
(24.97  3.83) and controls (25.32  PLI (p 5 0.044) among current smokers lower proportion of the vertical tooth
3.73) (p 5 0.242). were also significantly associated with brushing method (44.2% versus 57.2%;
COPD (Table 3). In particular, the p 5 0.004), and a lower proportion of
adjusted OR of COPD for each unit dental floss use (4.5% versus 11.4%;
Periodontal health status and COPD increase in PLI was 2.34 (95% CI, p 5 0.002) than those without COPD.
COPD patients had fewer remaining 1.03–5.34) among current smokers. COPD patients were less likely to have
teeth (21.54  6.27 versus 23.07  dental visits (42.0% versus 59.3%;
5.63) (p 5 0.001), a higher PLI (2.61  po0.0001) and receive regular supra-
Univariate analysis of oral health gingival scaling treatment (25.2% ver-
0.53 versus 2.41  0.94) (p 5 0.001), behaviour condition with COPD
and had more site percentages of CAL sus 45.8%; po0.0001).
(CALX4 mm site: p 5 0.011; CALX There were low correlations between
3 mm site: p 5 0.033) than the controls any two of the oral health covariates
Multivariate-adjusted analyses of oral
with normal pulmonary function (Table 2). (all Pearson’s correlation coefficients health behaviour condition with COPD

Table 1. Basic characteristics of the study population To minimize a potential confounding


effect, we adjusted for the variables
Characteristic COPD group Control group p-valuen of age, gender, and BMI in logistic
(n 5 306) (n 5 328) regression models. We also treated
Mean  standard deviation smoking status as an important effect
Age 63.94  9.84 63.26  8.98 0.366 modifier and stratified it in the logistic
Body mass index (BMI) 24.97  3.83 25.32  3.73 0.242 regression analyses (Table 5). When
Distribution of subjects (%) these oral health behaviour variables
Gender o0.0001 were adjusted simultaneously, the hor-
Male 210 (68.6) 164 (50.0) izontal tooth brushing method was sig-
Female 96 (31.4) 164 (50.0) nificantly associated with COPD only
Smoking status o0.0001
among non-smokers (p 5 0.025), while
Non-smoker 105 (34.3) 231 (70.4)
Former smoker 154 (50.3) 56 (17.1) lower regular supra-gingival scaling
Current smoker 47 (15.4) 41 (12.5) retained statistically significant associa-
Marriage status 0.503 tions with COPD among non-smokers
Single 25 (8.2) 26 (7.9) (p 5 0.027) and among former smokers
Married 281 (91.8) 302 (92.1) (po0.0001). In particular, the adjusted
Living status 0.176 OR of lower regular supra-gingival scal-
Living alone 19 (6.2) 14 (4.3) ing among former smokers was 3.77
Living with family 287 (93.8) 314 (95.7)
(95% CI, 1.82–7.81). Poor oral health
n
p-value obtained from Student’s t-test for continuous variables and w2-test for categorical variables. knowledge was significantly associated
with COPD in all subgroups (po0.0001
among non-smokers, p 5 0.019 among
Table 2. Univariate analysis of periodontal health in COPD and control groups
former smokers, and p 5 0.044 among
Clinical parameter COPD group Control group p-valuew current smokers); the adjusted OR of
(Mean  standard deviation) (n 5 306) (n 5 328) poorer oral health knowledge was 2.85
(95% CI, 1.70–4.76) among non-smo-
Periodontal index kers, 2.41 (95% CI, 1.16–5.04) among
Number of remaining teeth 21.54  6.27 23.07  5.63 0.001n
PD 3.12  0.72 3.20  0.76 0.146
former smokers, and 2.69 (95% CI,
CAL 4.79  1.60 4.54  1.73 0.059 1.03–7.02) among current smokers.
BI 2.21  0.63 2.31  0.77 0.075
PLI 2.61  0.53 2.41  0.94 0.001n
Alveolar bone loss 1.49  0.46 1.43  0.44 0.067
Discussion
Moderate and severe site percentages
PDX4 mm site percentages 30.24  13.18 33.17  14.08 0.109 In this study, COPD patients appeared to
CALX3 mm site percentages 84.81  20.20 80.82  26.06 0.033n have a poorer periodontal health status
PDX5 mm site percentages 12.47  4.30 14.75  5.19 0.061 than controls with normal pulmonary
CALX4 mm site percentages 70.12  18.87 64.00  21.36 0.011n function. Specifically, COPD patients
n
po0.05 statistically significant. had fewer remaining teeth, a higher
w
p-value obtained from Student’s t-test. PLI, and greater CAL site percentages
PD, probing depth; CAL, clinical attachment level; BI, bleeding index; PLI, plaque index. than the controls. Our study also showed
r 2009 John Wiley & Sons A/S
Oral health and COPD 753

Table 3. Adjusted ORs and 95% CIs of COPD in relation to periodontal health stratified by that inappropriate oral health behaviours
cigarette smoking status including inappropriate tooth brushing
Smoking status Clinical parameter p-valuen OR 95% CI method, lower regular supra-gingival
scaling, and poorer oral health knowl-
Non-smoker Number of remaining teeth 0.045n 1.05 1.01–1.11 edge were significantly associated with
PLI 0.302 1.17 0.87–1.59 an increased risk of COPD. These find-
CALX3 mm site percentages 0.933 1.00 0.99–1.01 ings indicate the importance of pro-
CALX4 mm site percentages 0.901 1.00 0.99–1.01 moting dental care and oral health
Former smoker Number of remaining teeth 0.573 1.02 0.96–1.07
knowledge in the prevention and treat-
PLI 0.356 1.33 0.73–2.45
CALX3 mm site percentages 0.754 1.00 0.99–1.02 ment of COPD.
CALX4 mm site percentages 0.812 0.99 0.99–1.01 To the best of our knowledge, there
Current smoker Number of remaining teeth 0.162 1.06 0.98–1.14 are very limited data on the importance
PLI 0.044n 2.34 1.03–5.34 of oral health in the medical care of
CALX3 mm site percentages 0.870 0.99 0.97–1.02 COPD patients. Our case–control study
CALX4 mm site percentages 0.873 1.00 0.98–1.02 provided the first comprehensive analy-
n
po0.05 statistically significant. sis of oral health and behaviours in
The logistic regression analyses were stratified by smoking status and adjusted for age, gender, and relation to COPD. The observed asso-
body mass index. ciation between periodontal health sta-
OR, odds ratio; CI, confidence interval; PLI, plaque index; CAL, Clinical attachment level. tus and COPD was consistent with
previous studies (Scannapieco & Ho
2001, Katancik et al. 2005). Katancik
et al. (2005) studied 860 elderly patients
Table 4. Univariate analysis of oral health behaviours in COPD and control groups
and found that the CAL was signifi-
Oral health behaviours COPD group Control group p-valuen cantly higher in COPD patients than in
participants with normal pulmonary
Distribution of subjects (%) function. Specifically, among former
Tooth brushing times o0.0001
41 time/day 47.9 31.9
smokers, all periodontal measures
X2 times/day 52.1 68.1 including PLI and CAL were associated
Horizontal tooth brushing method o0.0001 with pulmonary disease status. Another
Yes 51.2 36.1 cross-sectional epidemiological study
No 48.8 63.9 suggested that current smokers with
Vertical tooth brushing method 0.004 X4 mm CAL had a high risk of COPD
Yes 44.2 57.2 (OR: 3.71) (Hyman & Reid 2004). We
No 55.8 42.8 also found that current smokers with
Using dental floss 0.002
Yes 4.5 11.4
higher PLI had a high risk of COPD
No 95.5 88.6 (OR: 2.34). The results of these studies
Dental visit in last year o0.0001 support an association between poor
Yes 42.0 59.3 periodontal health status and COPD. A
No 58.0 40.7 high PLI and moderate and severe CAL
Have regular supra-gingival scaling o0.0001 may be risk factors for the development
Yes 25.2 45.8 of COPD. The pathogenic mechanisms
No 74.8 54.2 linking periodontal health to COPD are
Mean  Standard deviation
Oral health knowledge score 71.2  17.8 80.6  12.9 o0.0001
not entirely understood, but chronic
inflammatory processes are likely to be
n 2
p-value obtained from w -test for categorical variables and Student’s t-test for continuous variables. involved. Periodontitis is a chronic
inflammatory reaction from which oral
pathogens and inflammatory cytokines
Table 5. Adjusted ORs and 95% CIs of COPD in relation to oral health behaviours
may induce systemic inflammation,
which has been implicated in the patho-
Smoking status Oral health behaviour states p-value OR 95% CI genesis of COPD (Terpenning 2001).
Although several studies have obse-
Non-smoker Horizontal tooth brushing method: Yes versus No 0.025n 1.65 1.07–2.56
rved the association between perio-
Regular supra-gingival scaling: No versus Yes 0.027n 1.81 1.07–3.04
Oral health knowledge: low versus High o0.0001n 2.85 1.70–4.76 dontal health status and COPD, this is
Former smoker Horizontal tooth brushing method: Yes versus No 0.306 1.45 0.71–2.93 the first study to evaluate the association
Regular supra-gingival scaling: No versus Yes o0.0001n 3.77 1.82–7.81 between oral health behaviours and
Oral health knowledge: low versus High 0.019n 2.41 1.16–5.04 COPD. Health-related knowledge, atti-
Current smoker Horizontal tooth brushing method: Yes versus No 0.185 1.80 0.76–4.26 tudes, and beliefs have been found to
Regular supra-gingival scaling: No versus Yes 0.265 1.71 0.67–4.40 influence one’s oral health behaviour
Oral health knowledge: low versus High 0.044n 2.69 1.03–7.02 and oral health. Our study showed rela-
n
po0.05 statistically significant. tively low correlations between any two
The logistic regression analyses were stratified by smoking status and adjusted for age, gender, and of the oral health behaviour variables
body mass index. (all r2o0.17), indicating that they may
OR, odds ratio; CI, confidence interval. independently reflect different aspects
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754 Wang et al.

of overall oral health. Because smoking power for our subgroup analyses strati- in dental plaque of hospitalized patients with
is a major risk factor for both perio- fied by smoking status because of the chronic lung Diseases. Clinical Oral Investi-
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disease, and COPD, the logistic regres- results. Also, oral health status may be a veira, M. D. & Rodrigues, C. R. (2007)
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because it could cause wedged cervical confounding or effect modification between alveolar bone loss and pulmonary
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that self-assessed poor oral health beha- In conclusion, our case–control study obstructive pulmonary disease. Journal of
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group. Thus, bacteria associated with cohort studies or clinical trials that are cervical lesions produced by toothbrushing.
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We would like to thank the dedicated
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and committed participants of our
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56. between infections and chronic respiratory E-mail: wzuomin@gmail.com

Clinical Relevance Principal findings: Higher PLI, inap- Practical implications: Promoting
Scientific rationale for study: The propriate tooth brushing method, oral health knowledge, appropriate
associations of periodontal health lower supra-gingival scaling, and tooth brushing method, and regular
status and oral health behaviours poorer oral health knowledge were supra-gingival scaling may be impor-
with COPD are unclear due to the significantly associated with the risk tant to be integrated into the preven-
lack of population data. of COPD. tion and treatment of COPD.

r 2009 John Wiley & Sons A/S

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