Oral hygiene, periodontal health

and chronic obstructive

pulmonary disease
exacerbations
Liu Z, Zhang W, Zhang J, Zhou X, Zhang L, Song Y, Wang Z. Oral hygiene,
periodontal health and chronic obstructive pulmonary disease exacerbations. J Clin
Periodontol 2012; 39: 4552. doi: 10.1111/j.1600-051X.2011.01808.x.
Abstract
Aim: To assess the associations of oral hygiene and periodontal health with
chronic obstructive pulmonary disease (COPD) exacerbations.
Material and Methods: In total, 392 COPD patients were divided into frequent
and infrequent exacerbation ( 2 times and <2 times in last 12 months) groups.
Their lung function and periodontal status were examined. Information on oral
hygiene behaviours was obtained by interview.
Results: In the univariate analysis, fewer remaining teeth, high plaque index
(PLI) scores, low tooth brushing times, and low regular supra-gingival scaling
were signicantly associated with COPD exacerbations (all p-values <0.05). After
adjustment for age, gender, body mass index, COPD severity and dyspnoea sever-
ity, the associations with fewer remaining teeth (p = 0.02), high PLI scores
(p = 0.02) and low tooth brushing times (p = 0.008) remained statistically signi-
cant. When stratied by smoking, fewer remaining teeth (OR = 2.05, 95% CI:
1.044.02) and low tooth brushing times (OR = 4.90, 95% CI: 1.2619.1) among
past smokers and high PLI scores (OR = 3.43, 95% CI: 1.199.94) among never
smokers were signicantly associated with COPD exacerbations.
Conclusions: Fewer remaining teeth, high PLI scores, and low tooth brushing
times are signicant correlates of COPD exacerbations, indicating that improving
periodontal health and oral hygiene may be a potentially preventive strategy
against COPD exacerbations.
Zhiqiang Liu
1
, Wei Zhang
2,*
, Jing
Zhang
1
, Xuan Zhou
1
, Liangqiong
Zhang
1
, Yiqing Song
3
and Zuomin
Wang
1
1
Department of Stomatology, Beijing
ChaoYang Hospital afliated to Capital
Medical University, Beijing, China;
2
Department of Stomatology, Beijing Hai Dian
Hospital, Beijing, China;
3
Division of
Preventive Medicine, Brigham & Womens
Hospital, Harvard Medical School, Boston,
MA, USA
*Co-rst author with equal contribution.
Key words: casecontrol study; chronic
obstructive pulmonary disease;
exacerbations; oral hygiene; periodontitis; risk
factors
Accepted for publication 12 September 2011
In recent years, periodontal diseases
have been associated with a number
of systemic diseases such as chronic
respiratory diseases (Wang et al.
2009, Sharma & Shamsuddin 2011),
cardiovascular disease (Ouyang et al.
2011), diabetes mellitus (Taiyeb-Ali
et al. 2011) and rheumatoid arthritis
(Martinez-Martinez et al. 2009). The
biological mechanisms underlying
these associations remain uncertain,
although several inammatory cyto-
kines such as C-reactive protein,
interleukin-1 (IL-1), and IL-6 may
be involved in mediating systemic
inammation in the human body
Conict of interest and source of funding statement
The authors declare no conict of interests related to this study.
This study was supported by the National Natural Science Foundation of China
(30872878), the Natural Science Foundation of Beijing (7093120), and Beijing Sci-
ence and Technology Programme Fund (Z101107050210031). The funding organiza-
tions played no role in the design and conduct of the study; in the collection,
analysis, and interpretation of the data; or in the preparation, review, or approval
of the manuscript.
2011 John Wiley & Sons A/S 45
J Clin Periodontol 2012; 39: 4552 doi: 10.1111/j.1600-051X.2011.01808.x
(Pischon et al. 2007, Seymour et al.
2007).
The relationship between peri-
odontitis and chronic obstructive
pulmonary disease (COPD) has
recently received much attention.
COPD is a highly prevalent respira-
tory disease characterized by gradual
irreversible airow limitation. It is
predicted that COPD will become
the third most common cause of
death and the fourth most important
disease leading to disability by the year
2020 (Murray & Lopez 1997a,b,c).
Periodontitis, one of the most com-
mon oral diseases, is a chronic
inammatory disease, which mani-
fests destruction of supporting con-
nective tissue and alveolar bone
(Smith et al. 2010). Data from the
National Health and Nutrition
Examination Survey III, a nationally
representative sample of the US pop-
ulation, has shown that COPD
patients have more severe periodon-
tal attachment loss than those with-
out COPD. There was also a trend
that lung function of COPD patients
diminished with increasing periodon-
tal attachment loss (Scannapieco &
Ho 2001). In a COPD casecontrol
study, our research team reported
that poor periodontal health and
lack of dental care and oral health
knowledge were signicantly associ-
ated with increased risk of COPD
(Wang et al. 2009). A 25-year longi-
tudinal study showed that alveolar
bone loss was an independent risk
factor for COPD and individuals
who had severe alveolar bone loss at
baseline had a higher risk of devel-
oping COPD during the follow-up
period (Hayes et al. 1998). Epidemio-
logic evidence of a systematic review
indicated that poor periodontal
health status may be an independent
predictor of COPD risk (Garcia
et al. 2001).
Furthermore, to our knowledge,
there is no evidence regarding the
relation of periodontal health and
COPD exacerbations. Acute exacer-
bation of COPD is acute in onset of
the disease, which is characterized by
deterioration in clinical symptoms
including increased dyspnoea, cough,
sputum volume or sputum purulence
compared with their baseline status,
and a change in regular medication
is usually needed. It is a main cause
of mortality (Soler-Catalun a et al.
2005). Hospitalization and medical
care for COPD exacerbations is a
source of large economic burden
(Miravitlles et al. 2002). Exacerba-
tions would also signicantly com-
promise life quality of COPD
patients (Miravitlles et al. 2004, Xu
et al. 2010). Thus, eective preven-
tion of COPD exacerbation has
important clinical and public health
implications. Many clinical factors
had been previously associated with
COPD exacerbations such as ageing,
COPD severity, forced expiratory
volume in 1 s (FEV
1
)% predicted
value, BODE index [a composite
score based on the body mass index
(BMI), the degree of airow obstruc-
tion and dyspnoea, and exercise
capacity], other comorbid condi-
tions, or depression (Miravitlles
et al. 2000, Donaldson et al. 2003,
Bahadori et al. 2009, Jennings et al.
2009, Faganello et al. 2010). How-
ever, whether other factors associ-
ated with chronic inammation such
as periodontal health status and oral
health behaviours are associated
with COPD exacerbations has yet to
be investigated.
We hypothesize that poor oral
hygiene and periodontal health may
partially contribute to the occurrence
or frequency of COPD exacerba-
tions. We therefore conducted a
cross-sectional study to examine the
associations of oral hygiene and
periodontal health with COPD exac-
erbations.
Material and Methods
Patient population
A total of 392 ambulatory COPD
patients were recruited from Beijing
ChaoYang hospital and other seven
hospitals in Beijing from March
2007 to November 2010. The inclu-
sion criteria are as follows: (1) aged
30 years; (2) having more than 10
teeth; (3) no exacerbations in the
past 4 weeks at recruitment; (4) no
diagnosed asthma; (5) no cancer;
and (6) no previous lung volume
reduction surgery, lung transplanta-
tion, or pneumonectomy. All COPD
patients were clinically diagnosed by
physicians and conrmed by lung
function examination. All partici-
pants were interviewed at recruit-
ment by trained dentists, who were
trained by an experienced physician
of department of respiratory medi-
cine.
Human research ethics board
from Beijing Chao Yang hospital
approved the study, and written
informed consent was obtained from
all participants.
Diagnosis of COPD and assessment of
lung function
Criteria used for the diagnosis of
COPD are based on the Global Ini-
tiative for Chronic Obstructive Lung
Disease (GOLD) spirometry guide-
lines: Global Strategy for the Diag-
nosis, Management, and Prevention
of Chronic Obstructive Pulmonary
Disease (Update 2007) (Rabe et al.
2007).
Lung function was measured
using spirometry. The spirometric
measurements were conducted by
trained and certied technicians. Of
at least ve forced expirations, the
technician attempted to obtain three
acceptable spirograms, at least two
of which had similar results for
FEV
1
and forced vital capacity
(FVC). The lung function was evalu-
ated based on the FEV
1
/FVC and
then categorized into severity using
the per cent of predicted FEV
1
. Air
limitation was dened by post-bron-
chodilator FEV
1
/FVC <0.70. Degree
of dyspnoea of all COPD patients
was evaluated by the Medical
Research Council (MRC) dyspnoea
scale, which was scored on a 15
(Bestall et al. 1999).
Denition of COPD exacerbations and
group classication
In this study, COPD exacerbations
were dened as acute deterioration
in clinical symptoms in accordance
with GOLD guideline denition
(Rabe et al. 2007), which is charac-
terized by increased dyspnoea,
cough, sputum volume or sputum
purulence compared with their base-
line status. Two or more of above
symptoms and a change in medica-
tion are required to conrm one
exacerbation. If two exacerbations
occurred within 2 weeks, it was con-
sidered one exacerbation. The exac-
erbation frequency in the last
12 months was reported by the
patient in the interview. Patients
who suered from <2 exacerbations
in the last 12 months were classied
2011 John Wiley & Sons A/S
46 Liu et al.
as the infrequent exacerbation
group, while those who suered
from 2 or more exacerbations in the
last 12 months were dened as the
group of frequent exacerbation (Mir-
avitlles et al. 2000, Wan et al. 2011).
Periodontal examination
Periodontal indices of all COPD
patients were clinically examined.
The periodontal health examinations
were conducted by two trained den-
tists blinded to COPD status. Repli-
cate examinations were conducted
throughout the survey to repeatedly
assess inter-examiner and intra-
examiner reliability. The Kappa val-
ues of agreement were all above 0.8
between the two trained dentists and
in self-comparison of each dentist.
The evaluation included periodontal
probing and the number of teeth
present. Periodontal probing
included probing depth (PD) and
location of the cemento-enamel junc-
tion (CEJ), which can further deter-
mine clinical attachment level
(CAL), and bleeding index (BI) on
probing. PD and CEJ were mea-
sured with a Williams periodontal
probe at six sites of all teeth (exclud-
ing third molars) and recorded in
millimetres. Recession was recorded
as a positive value if the free gingival
margin occurred apical to the CEJ,
and as a negative value if it was
coronal to the CEJ. CAL was calcu-
lated by summing PD and CEJ. BI
on probing was scored on a 05
scale when any visual evidence of
bleeding was noted (Mazza et al.
1981).
Assessment of oral hygiene status and
behaviours
Oral hygiene status of all patients
was evaluated by plaque index
(PLI), which for each tooth was
determined on a 03 scale after air
drying (Silness & Lo e 1964). Infor-
mation of their oral hygiene behav-
iours include tooth brushing time,
the use of dental oss and regular
supra-gingival scaling, were obtained
by interview at recruitment by
trained dentists.
Measurement of the other variables
Basic characteristic variables include
age, gender, education background,
lifestyle, and smoking status and
dental visit behaviour in last year
was also collected by interview.
Anthropometric variables, including
height and weight, were measured by
nurses and BMI was calculated.
Statistical analysis
SPSS statistical package (version
13.0; SPSS Inc., Chicago, IL, USA)
was used for the data analysis. An
independent samples t-test was used
for continuous variables and chi-
squared test was used for categorical
variables to compare their crude dif-
ferences between infrequent exacerba-
tion group and frequent exacerbation
group. Logistic regression was per-
formed to calculate the odds ratio
(OR) and 95% condence interval
(CI) for periodontal health status,
oral hygiene status and behaviours
and other factors in association with
COPD exacerbations. In the multi-
variate-adjusted logistic regression
analysis, age, gender, BMI, and
smoking were included in model 1,
and COPD severity and MRC scores
were additionally added in model 2 to
control for potential confounding of
respiratory variables. As smoking is
an important eect modier for the
relation between periodontal disease
and COPD (Hyman 2006), we also
stratied the analysis by smoking sta-
tus (current smoker, past smoker and
never smoker).
Results
The basic characteristics of 392
COPD patients are shown in
Table 1. The mean age and BMI of
the frequent and infrequent exacer-
bation groups were similar. Distribu-
tion of gender, smoking status and
living status were also similar.
Patients in infrequent exacerbation
group were more educated (25.8%)
than those in frequent exacerbation
group (16.9%) (p = 0.03). COPD
patients in frequent exacerbation
group were more likely to be in
GOLD stage III and IV (53.6% ver-
sus 37.8%; p = 0.002) and MRC
score of >2 (55.7% versus 33.5%;
p < 0.0001) than those in infrequent
exacerbation group.
Periodontal health variables in
COPD patients with frequent exacer-
bation and infrequent exacerbation
Table 1. Basic characteristics of 392 COPD patients with frequent exacerbation and infre-
quent exacerbation
Characteristics Frequent
exacerbation
(n = 183)
Infrequent
exacerbation
(n = 209)
p-value

Age (mean SD) 64.3 10.1 63.6 9.7 0.48

BMI (kg/m
2
) (mean SD) 24.6 3.8 24.7 3.9 0.77
Sex (%)
Male 132 (72.1) 155 (74.2) 0.65
Female 51 (27.9) 54 (25.8)
Education background (%)
Higher education 31 (16.9) 54 (25.8) 0.03*
Lower education 152 (83.1) 155 (74.2)
Smoking status (%)
Never smoker 51 (27.9) 68 (32.5) 0.38
Past smoker 110 (60.1) 111 (53.1)
Current smoker 22 (12.0) 30 (14.4)
Living status (%)
Living alone 15 (8.2) 16 (7.7) 0.84
Living with family 168 (91.8) 193 (92.3)
COPD severity (%)
GOLD stage I and II 85 (46.4) 130 (62.2) 0.002*
GOLD stage III and IV 98 (53.6) 79 (37.8)
Degree of dyspnoea (%)
MRC score 2 81 (44.3) 139 (66.5) <0.0001*
MRC score >2 102 (55.7) 70 (33.5)
BMI, body mass index; GOLD, Global Initiative for Chronic Obstructive Lung Disease;
MRC, Medical Research Council dyspnoea scale.
*p < 0.05 statistically signicant.

p-value obtained from independent samples t-test for continuous variables and v2 test for
categorical variables.
2011 John Wiley & Sons A/S
Periodontal health and COPD exacerbations 47
groups are showed in Table 2. There
was no signicant dierence in PD,
CAL and BI between the frequent
and infrequent exacerbation groups.
A higher proportion of patients with
frequent exacerbations had 25
remaining teeth (p = 0.02 both in the
univariate model and multivariate-
adjusted model). Comparing patients
with infrequent exacerbations with
those with frequent exacerbations,
the OR of remaining teeth 25 was
1.80 (95% CI: 1.092.99) after
adjusting for age, gender, BMI and
smoking.
Oral hygiene status and behav-
iours and dental visit behaviours of
COPD patients in the frequent exac-
erbation group and the infrequent
exacerbation group are showed in
Table 3. A higher proportion of
patients with frequent exacerbation
had PLI scores >2, tooth brushing
<1 time/day, and regular supra-gingi-
val scaling <1 time/year. After
adjusting for age, gender, BMI, and
smoking, only PLI scores >2
(OR = 1.97, 95% CI: 1.113.49) and
tooth brushing <1 time/day
(OR = 4.09, 95% CI: 1.4511.5)
were signicantly associated with fre-
quent exacerbations. The use of den-
tal oss and dental visit in last year
were not associated with COPD
exacerbations.
Multivariate analysis of periodon-
tal health with COPD exacerbation
is shown in Table 4. In the entire
sample, fewer remaining teeth
(p = 0.045), high PLI scores
(p = 0.02), and low tooth brushing
times (p = 0.004) were each signi-
cantly associated with COPD exacer-
bations in the adjusted model 1,
while only fewer remaining teeth
(p = 0.04) and low tooth brushing
times (p = 0.008) remained signi-
cantly associated with COPD exacer-
bations in the adjusted model 2.
When the analysis was stratied by
smoking status, fewer remaining
teeth (OR = 1.80 in model 1 and
2.05 in model 2) and low tooth
brushing times (OR = 5.23 in model
1 and 4.90 in model 2) were signi-
cantly associated with COPD exacer-
bations among past smokers, and
high PLI scores (OR = 3.79 in model
1 and 3.43 in model 2) was signi-
cantly associated with COPD exacer-
bations among never smokers. On
average, smoking years in current
smokers and past smokers were 43.5
(10.1) and 34.3 (12.7) years,
respectively.
Discussion
Our study of 183 COPD patients
with frequent exacerbation and 209
COPD controls with infrequent
exacerbation showed that fewer
remaining teeth, high PLI scores,
and low tooth brushing times were
each signicantly associated with
COPD exacerbations independent of
age, sex, BMI and smoking.
Although further studies are needed
to conrm our ndings, our results
indicate that improving oral hygiene
and periodontal health may be a
potentially preventive measure
against exacerbation in COPD
patients.
The denitions of COPD exacer-
bation are inconsistent and contro-
versial (Eng et al. 2009). A number
of studies have dened exacerbations
as worsening symptoms that require
additional medication, emergency
visit or hospitalization (Pauwels
et al. 2004). Although this event-
based denition is conveniently
useful, it would likely miss mild
exacerbations or severe exacerba-
tions, especially when the patients
does not seek treatment (Seemungal
et al. 2000, Miravitlles et al. 2004).
Other studies dened exacerbations
based solely on worsening symp-
toms, including increased dyspnoea,
cough, and/or sputum (Pauwels
et al. 2004). With this symptom-
based denition, exacerbation fre-
quency would be reported by the
patients themselves, especially in a
retrospective study, so recall bias
was inevitable. In this study, COPD
exacerbations were dened in accor-
dance with GOLD guideline deni-
tion, which is mainly based on
clinical symptoms (Rabe et al. 2007).
Basic characteristics, including
age, sex, BMI and living status, were
not associated with COPD exacerba-
tions in this study. In the univariate
analysis, we found that patients pos-
sessing a higher education back-
ground had lower risk to have
frequent exacerbations than patients
Table 2. Distributions of periodontal health variables in COPD patients and their associations with COPD exacerbation
Periodontal
variables
Frequent
exacerbation
(n = 183)
Infrequent
exacerbation
(n = 209)
Univariate model Adjusted model

OR (95% CI) p-value

OR (95% CI) p-value

Remaining teeth (%)
25 129 (70.5) 124 (59.3) 1.64 (1.082.49) 0.02* 1.80 (1.092.99) 0.02*
>25 54 (29.5) 85 (40.7) 1.00 1.00
PD (%)
3mm 94 (51.4) 107 (51.2) 1.00 0.97 1.00 0.43
>3mm 89 (48.6) 102 (48.8) 0.99 (0.671.48) 1.23 (0.732.07)
CAL (%)
4mm 60 (32.8) 68 (32.5) 1.00 0.96 1.00 0.33
>4mm 123 (67.2) 141 (67.5) 0.99 (0.651.51) 0.75 (0.431.33)
BI (%)
2.5 137 (74.9) 145 (69.4) 1.00 0.23 1.00 0.21
>2.5 46 (25.1) 64 (30.6) 0.76 (0.491.19) 0.72 (0.421.21)
PD, probing depth; CAL, clinical attachment level; BI, bleeding index.
*p < 0.05 statistically signicant.

p-value obtained from v

2
test.

The logistic regression analyses were adjusted for age, gender, body mass index and smoking.
2011 John Wiley & Sons A/S
48 Liu et al.
Table 3. Oral hygiene status and behaviours and dental visit behaviours in COPD patients with frequent exacerbation and infrequent exac-
erbation and their crude associations
Oral hygiene status and
behaviours and dental visit
behaviours
Frequent
exacerbation
(n = 183)
Infrequent
exacerbation
(n = 209)
Univariate model Adjusted model

OR (95% CI) p-value

OR (95% CI) p-value

Plaque index (PLI) (%)
2 23 (12.6) 45 (21.5) 1.00 0.02* 1.00 0.02*
>2 160 (87.4) 164 (78.5) 1.91 (1.103.30) 1.97 (1.113.49)
Tooth brushing times (%)
<1 time/day 17 (9.3) 5 (2.4) 4.18 (1.5111.6) 0.003* 4.09 (1.4511.5) 0.008*
1 time/day 166 (90.7) 204 (97.6) 1.00 1.00
Using dental oss (%)
Yes 12 (6.6) 17 (8.1) 1.00 0.64 1.00 0.999
No 171 (93.4) 192 (91.9) 1.26 (0.592.72) 1.00 (0.432.32)
Supra-gingival scaling (%)
1 time/year 3 (1.6) 12 (5.7) 1.00 0.04* 1.00 0.24
<1 time/year 180 (98.4) 197 (94.3) 3.66 (1.0213.2) 2.23 (0.588.59)
Dental visit in last year (%)
Yes 65 (35.5) 81 (38.8) 1.00 0.51 1.00 0.94
No 118 (64.5) 128 (61.2) 1.15 (0.761.73) 1.02 (0.661.57)
*p < 0.05 statistically signicant.

p-value obtained from v

2
test.

The logistic regression analyses were adjusted for age, gender, body mass index and smoking.
Table 4. Multivariate-adjusted ORs and 95% CIs of COPD exacerbations in relation to oral health variables in total and stratied by
smoking status
Periodontal variables Adjusted model 1

Adjusted model 2

OR (95% CI) p-value OR (95% CI) p-value

Total
Remaining teeth
25 versus >25 1.63 (1.012.61) 0.045* 1.69 (1.032.77) 0.04*
Plaque index (PLI)
>2 versus 2 1.93 (1.093.42) 0.02* 1.72 (0.953.10) 0.08
Tooth brushing times
<1 time/day versus 1 time/day 4.50 (1.6012.7) 0.004* 4.19 (1.4412.1) 0.008*
Smoking status
Current smoker
Remaining teeth
25 versus >25 2.20 (0.509.79) 0.30 2.15 (0.4510.3) 0.34
Plaque index (PLI)
>2 versus 2 0.61 (0.103.70) 0.59 0.52 (0.083.50) 0.50
Tooth brushing times
<1 time/day versus 1 time/day 2.74 (0.2037.4) 0.45 3.86 (0.2656.3) 0.32
Past smoker
Remaining teeth
25 versus >25 1.80 (0.953.41) 0.07 2.05 (1.044.02) 0.04*
Plaque index (PLI)
>2 versus 2 1.65 (0.753.63) 0.21 1.72 (0.753.95) 0.20
Tooth brushing times
<1 time/day versus 1 time/day 5.23 (1.4019.5) 0.01* 4.90 (1.2619.1) 0.02*
Never smoker
Remaining teeth
25 versus >25 1.13 (0.472.69) 0.79 1.02 (0.422.51) 0.96
Plaque index (PLI)
>2 versus 2 3.79 (1.3410.8) 0.01* 3.43 (1.199.94) 0.02*
Tooth brushing times
<1 time/day versus 1 time/day 4.58 (0.4052.5) 0.22 4.65 (0.3759.2) 0.24
*p < 0.05 statistically signicant.

Model 1 adjusted for age, gender, body mass index and smoking (for total cases and controls). When it was stratied by smoking status,
smoking was not included in the adjusted model.

Model 2 additionally adjusted for COPD severity, Medical Research Council (MRC) dyspnoea scores.
2011 John Wiley & Sons A/S
Periodontal health and COPD exacerbations 49
who did not receive higher educa-
tion. However, education did not
remain a signicant predictor after
controlling for confounders. It is
well accepted that smoking is the
most important causal factor of
COPD (Raherison & Girodet 2009),
but it seems not to be associated
with COPD exacerbations in this
study, as found also in other three
studies (Miravitlles et al. 2000,
Alamoudi 2007, Wan et al. 2011).
The associations of periodontal
health and oral health behaviours
with COPD have been shown in pre-
vious studies. To our best knowl-
edge, no studies have specically
examined whether and to what
extent periodontal health and oral
hygiene are also associated with
COPD exacerbations. Our study
showed that oral hygiene related
variables include PLI, tooth brush-
ing times, and regular professional
tooth cleaning frequency were signif-
icantly associated with COPD exac-
erbations and PLI and tooth
brushing times remained signicant
after adjusting for confounders.
Recent clinical studies had suggested
that COPD exacerbations are caused
by infections by bacteria and virus
(Erkan et al. 2008, Ko et al. 2008,
Sethi & Murphy 2008). Poor oral
hygiene results in dental plaque, deb-
ris and calculus adhering to the
tooth surface. Dental plaque is a
diverse community of various micro-
organisms. These microorganisms
are embedded within matrix and
adhere to each other and/or to sur-
faces or interface, which is called as
biolm nowadays (Marsh 2005). It
may increase the risk of lower respi-
ratory tract infection and COPD
exacerbations.
Periodontal health indices include
PD, CAL, BI were not associated
with COPD exacerbations frequency
in our study. Interestingly, these
periodontal health indices in fre-
quent exacerbation group seemed to
be better than those in the infre-
quent exacerbation group, although
their dierences were not signicant.
We speculate that this phenomenon
may be related to frequent antibiotic
therapy during COPD exacerbations.
Antibiotic therapy is widely used
and eective treatment for COPD
exacerbations (Ram et al. 2011).
Antibiotic used for COPD exacerba-
tions treatment likely inhibit peri-
odontal inammation to a certain
extent at the same time. Systematic
reviews concluded that the use of
systemic antimicrobials alone was
benecial to periodontitis, although
its eect was not statistically signi-
cant and it is not recommended
for periodontitis treatment; sys-
temic antimicrobials adjunctive with
mechanical treatment signicantly
improved periodontal health than
mechanical treatment alone (Haajee
et al. 2003, Herrera et al. 2008). The
number of remaining teeth was
strongly inversely associated with
exacerbation frequency in this study,
which was also consistent with the
ndings in our previous study (Wang
et al. 2009).
When multivariate analysis was
stratied by smoking status, the
results were dierent among never
smokers, past smokers and current
smokers groups. These seemed ine-
xplicable. Never smokers were more
aected by high PLI scores maybe
just because of microorganism infec-
tion as mentioned above. Smoking
is a generally accepted risk factor
of periodontitis, so periodontal
health of never smokers seemed bet-
ter than current smokers or past
smokers. They would have fewer
teeth loss and would be less aected
by fewer remaining teeth. Current
smokers were not aected by all the
three risk factors (high PLI scores,
fewer remaining teeth and low
tooth brushing times). Current
smokers did not quit smoking were
probably because their general
health status or COPD severity
were better than past smokers who
had quit smoking. So oral hygiene
and periodontal health may play
less important role in COPD exac-
erbations of current smokers as
their better general health status or
COPD severity. Past smokers fall in
between never smokers and current
smokers. They had more teeth loss
and had worse general health status
or COPD severity, so they were
more easily aected by all the three
risk factors.
It was well documented that
COPD severity evaluated by FEV
1%
predicted value or GOLD stage was
a risk factor of COPD exacerbations
(Miravitlles et al. 2000, Groenewe-
gen et al. 2008, Hurst et al. 2010).
Consistently, our ndings showed
that higher proportion of COPD
patients in frequent exacerbation
group (53.6%) were GOLD stage III
and IV than patients in infrequent
exacerbation group (37.8%)
(p = 0.002). Dyspnoea was also a
signicant risk factor of COPD exac-
erbations in a casecontrol cohort
study evaluated by modied MRC
score (Wan et al. 2011). In this
study, a higher proportion of
patients in frequent exacerbation
group had higher MRC score con-
trast to infrequent group (55.7% ver-
sus 33.5%) (p < 0.0001). COPD
severity and MRC score were
included in the adjusted model 2 to
control potential confounding.
There were several limitations to
our study. First, recall bias may exist
as exacerbation frequency was
reported by the patients. Secondly,
COPD exacerbations were associated
with many other known factors such
as comorbid conditions and depres-
sion. These factors were not col-
lected in this study, so residual
confounding may exist. Thirdly, as a
cross-sectional study, the results of
our study cannot provide causal
eect evidence of oral hygiene and
periodontal health with COPD exac-
erbations. Finally, the 95% CI of
oral hygiene related variables in
Table 2 were subject to large ran-
dom variation due to small sample
size. Only very few patients did not
have tooth brushing less than one
time everyday and have regular
supra-gingival scaling and use dental
oss. False positive results by chance
may also occur.
In summary, this is the rst
study to describe a relationship of
oral hygiene and periodontal health
with COPD exacerbations to our
best knowledge. The results of this
study showed that fewer remain-
ing teeth, high PLI scores, and low
tooth brushing times were signi-
cantly associated with COPD
exacerbations and indicated that
improving periodontal health and
oral hygiene may be a potentially
preventive strategy against COPD
exacerbations. In the future, large
cohort studies and random clinical
trials will be needed to investigate
the causal eect of oral hygiene and
periodontal health with COPD exac-
erbations.
2011 John Wiley & Sons A/S
50 Liu et al.
Acknowledgements
The authors would like to thank the
clinical sta of Department of Respi-
ratory Medicine, Beijing ChaoYang
Hospital aliated to Capital Medi-
cal University for their kind assis-
tance.
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Address:
Z. Wang
Department of Stomatology
Beijing ChaoYang Hospital aliated to
Capital Medical University
Chao Yang District
Beijing 100020
China
E-mail: wzuomin@gmail.com
Clinical Relevance
Scientic rationale for study: Peri-
odontal health and oral health
behaviours have been associated
with chronic obstructive pulmo-
nary disease (COPD), but whether
they are associated with COPD
exacerbations has not been studied
yet.
Principal ndings: Fewer remaining
teeth, high plaque index scores, and
low tooth brushing times are signi-
cantly associated with COPD exac-
erbations.
Practical implications: Improving
periodontal health and oral hygiene
may be a potential target in pre-
venting COPD exacerbations.
2011 John Wiley & Sons A/S
52 Liu et al.
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