COPD, 10:567572, 2013

ISSN: 1541-2555 print / 1541-2563 online

Copyright Informa Healthcare USA, Inc.
DOI: 10.3109/15412555.2013.781579

ORIGINAL RESEARCH

The Association between BMI and COPD: The Results of Two

Population-based Studies in Guangzhou, China
Yumin Zhou,1 Dali Wang,2 Shengming Liu,1,3 Jiachun Lu,4 Jingping Zheng,1 Nanshan Zhong,1 and Pixin Ran1

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State Key Laboratory of Respiratory Disease,

Guangzhou Institute of Respiratory Diseases, First
Afliated Hospital, Guangzhou Medical University,
Guangzhou, Guangdong, China

The Second Hospital of Liwan District of

Guangzhou, Guangzhou, Guangdong, China

First Afliated Hospital of Jinan University,

Guangzhou, Guangdong, China

Department of Epidemiology, Guangzhou Medical

University, Guangzhou, Guangdong, China

Abstract
Background and Objective: An association between chronic obstructive
pulmonary disease (COPD) and low body mass index (BMI) has been well
established in cross-sectional studies. However, there have been few cohort
studies investigating this issue. We therefore aimed to address this gap.
Methods: Two population-based studies, a cross-sectional study including 1818
subjects and a subsequent 4-year cohort study consisting of 759 individuals
without COPD, were conducted in Guangzhou, China. Every subject was 40 years
old or older at the time of recruitment and completed questionnaire interviews,
anthropometric measurements and spirometry testing. As a follow-up, each
subject underwent annual pre-bronchodilator spirometry testing. Subjects
with a pre-bronchodilator FEV1/FVC <0.7 were required to undergo postbronchodilator spirometry testing. Subjects with a post-bronchodilator FEV1/
FVC <0.7 were diagnosed with COPD. Results: Compared to subjects with
normal BMI (18.5 to 23.9 kg/m2), those with low BMI (<18.5 kg/m2) had a
higher prevalence of COPD (21.1% vs. 7.5%), with an adjusted OR of 2.75 [95%
condence intervals (CI): 1.69 to 4.47]. Both low BMI and obese (28.0 kg/m2)
subjects had lower FEV1 after adjustment. This association was further
conrmed in the cohort study; non-COPD subjects with low BMI at baseline
were more likely to develop COPD (RR = 2.88, 95% CI: 1.06 to 7.85), independent
of smoking status and other confounders. Conclusions: Low BMI was not only
a systemic consequence of COPD but also an important risk factor for the
development of COPD, which raises the possibility that early intervention in
subjects with low BMI may reduce the incidence of COPD.

Introduction

Keywords: Pulmonary disease, chronic obstructive;

body mass index; epidemiology
Correspondence to: Pixin Ran, MD, PhD, Guangzhou
Institute of Respiratory Diseases, The First Afliated
Hospital, Guangzhou Medical University, 151 Yanjiang
Road, Guangzhou, Guangdong, 510120, China,
phone: +862081340482,
E-mail: pxran@gzhmc.edu.cn

Chronic obstructive pulmonary disease (COPD) primarily aects

cts thee lun
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ungs
ystemic
mi consemic
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w body
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m
quences is nutritional abnormalities, mainly represented byy a low
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atio
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index (BMI) (1). BMI, the body weight (kg) to height squared
neea, and
nd
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erc
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is
part of the BODE index (BMI, airow obstruction, dyspnea,
ndicator
or of
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oggn sis
is
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uggg
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o date,, however,
ho
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weight might be a risk factor for COPD (5). To
onship
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few cohort studies addressing the relationship
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Therefore, we evaluated the association
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cross-sectional study and a subsequent
China.
567

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Zhou et al.

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Methods
Study design and subjects
Two population-based epidemiological studies were
conducted in an urban area of Guangzhou, China,
including a cross-sectional survey including 1818
subjects aged 40 years that was conducted in 2002
and a subsequent 4-year follow-up survey (from
2003 through 2007) of 759 subjects who did not have
COPD at the baseline test. In both surveys, multistage
cluster sampling strategies were used, and spirometry testing and questionnaires interviews were conducted.
The detailed study protocols have been described
in previous publications (6, 7). Ethical approval of the
study protocols was obtained from the Medical Ethics
Committee of the Guangzhou Institute of Respiratory
Diseases, and informed consent was obtained from all
participants. The studies adhered to the principles of the
Helsinki Declaration.
Spirometry
In both surveys, spirometry testing was performed using
portable spirometers (Micro Medical Ltd., Chatham,
Kent, UK) by professional sta. The spirometry testing procedure recommended by American Thoracic
Society (8) and Enright PL et al. (9) was applied to all
eligible subjects. Subjects with a pre-bronchodilator
FEV1/FVC <0.7 underwent post-bronchodilator testing;
i.e., spirometry carried out within 15 to 20 minutes after
taking a dose of 200 g (in the cross-sectional study) or
400 g (in the 4-year follow-up survey) of Salbutamol
(Ventolin; GlaxoSmithKline, Middlesex, UK) inhaled
through a 500-ml spacer.
The use of short- and long-acting bronchodilators
within 12 or 24 hours prior to the test, respectively,
was prohibited. We determined a quality grade (AF)
based on acceptable maneuvers and repeatability of the
FEV1 and FVC (10). At baseline, spirometry results with
Grades A, B or C (at least two acceptable maneuvers,
with FEV1 values matching within 0.2 L) was considered
acceptable for analysis.
In our follow-up, spirometry testing was performed
annually at the same time, and a stricter standard
was required for analysis: at least three acceptable
and two reproducible measurements (i.e., the highest
and second highest values of the forced vital capacity (FVC) and FEV1 were within 150 ml or 5%) were
required for analysis. According to the current criteria
of the global initiative for chronic obstructive lung disease (GOLD) (11), subjects with post-bronchodilator
FEV1/FVC <0.7 were diagnosed with COPD, and
the stage (I-IV) of COPD was determined in each
diagnosed patient. Predicted normative values of
FEV1 in Chinese population were derived from ECSC93
(European Coal and Steel Community in 1993) equations and adjusted using the appropriate conversion
factors (12).

Questionnaire
The questionnaires used in the two studies have been published elsewhere (6, 7) and include questions about demographic variables, respiratory symptoms/disease history,
co-morbidities, health care utilization, activity limitation,
nutritional status, smoking and other potential risk factors
for COPD. Body weight was measured in light clothing to
the nearest 0.1 kg with a calibrated balance beam scale;
height without shoes on was measured to the nearest 0.5 cm
using a vertical ruler; and BMI (kg/m2) was computed as
the ratio of body weight (kg) to height squared (m2).
BMI status was classied as low (<18.5 kg/m2),
normal (18.523.9 kg/m2), overweight (24.027.9 kg/
m2) or obese ( 28.0 kg/m2) (13). Smoking status was
recorded as currently smokes, has never smoked, or
previously smoked at each visit. Subjects who had
smoked for at least six months or had smoked at least
100 cigarettes in their lifetime were dened as ever
smokers(14), otherwise, they were categorized as never
smokers. Former smokers were dened as subjects
who had quit smoking for at least 6 months.
Current smokers included continual smokers and
those who had quit but restarted or relapsed or had
quit for less than 6 months (7). The following factors
were measured at baseline and coded as dichotomous
variables: occupational exposure (yes or no, classied
with a cut-o point of occupational exposure to dusts/
fumes/gases for one year), co-morbidity (any physicianconrmed COPD-related disease), and family history of
respiratory disease (any parent or sibling diagnosed with
chronic bronchitis, emphysema, asthma or COPD).
Statistical analysis
Statistical analyses were performed with Stata software
(Version 7.0, Stata Corporation, College Station, TX,
USA) and SAS version 9.1 software (SAS Institute, Cary,
NC). The association between BMI and COPD was evaluated using dichotomous logistic regression, and odds
ratios (ORs) and relative risk ratios (RRs) for COPD
were calculated after adjustment for clusters, gender,
education level, smoking status, family history of respiratory disease, history of exposure to occupational dust/
fume/gases, and age. No interaction was added to the
nal logistic regression model. A p-value of <0.05 was
considered statistically signicant.

Results
Baseline characteristics of the two study populations
The mean age of the population in the cross-sectional
study was 59.11 (the standard deviation (SD), 11.82) yrs;
40.2% were male; the mean FEV1 was 2.06 (SD, 0.64) L;
the mean FVC was 2.58 (SD, 0.75) L; the mean FEV1/
FVC was 80.00 (SD, 9.31) %; the mean BMI was 22.88
(SD, 3.50); and 35.1% of population had ever smoked cigarettes. The baseline characteristics of the cohort study
and the cross-sectional study populations were similar,
except for occupational exposure (p < 0.05) (Table 1).
Copyright 2013 Informa Healthcare USA, Inc

Association between BMI and COPD in Guangzhou, China

Table 1. Baseline characteristics of the participants in the cross-sectional

study and subsequent cohort study
Cross-sectional
study
Subjects
Age (years)

1818 (100.0)

Cohort study
759 (100.0)

59.11 (11.82) *

59.27 (11.31) *

40-49 yrs

517 (28.4)

198 (26.1)

50-59 yrs

384 (21.1)

176 (23.2)

60-69 yrs

521 (28.7)

231 (30.4)

70 yrs or over

396 (21.8)

154 (20.3)

Gender
Male

730 (40.2)

316 (41.6)

1088 (59.8)

443 (58.4)

0 yrs

175 (9.6)

70 (9.2)

1-5 yrs

585 (32.2)

269 (35.4)

6-8 yrs

455 (25.0)

184 (24.2)

9-11 yrs

485 (26.7)

196 (25.8)

12 yrs

118 (6.5)

40 (5.3)

Yes

354 (19.5)

144 (19.0)

No

1464 (80.5)

615 (81.0)

Female

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Education, yrs

Family history of respiratory

disease

BMI, kg/m2
Low (<18.5)

22.88 (3.50) *

23.09 (3.50) *

166 (9.1)

57 (7.5)

1008 (55.4)

414 (54.5)

Preobese (24.0-27.9)

524 (28.8)

235 (31.0)

Obese (28.0)

120 (6.6)

53 (7.0)

Yes

384 (21.1)

354 (46.6)

No

1434 (78.9)

405 (53.4)

Normal (18.5-23.9)

Occupational exposure

Smoking index, pack-yrs

<15pack-yrs

10.01 (19.27) *
1370 (75.4)

11.90 (20.36) *
529 (69.7)

15-29 pack-yrs

196 (10.8)

97 (12.8)

30-44 pack-yrs

124 (6.8)

72 (9.5)

45 pack-yrs

128 (7.0)

61 (8.0)

Smoking status
Never smoked

1179 (64.9)

446 (58.8)

Former smoker

227 (12.5)

106 (14.0)

Current smoker

412 (22.7)

207 (27.3)

Pre-bronchodilator FEV1, L

2.06 (0.64) *

2.11 (0.58) *

Pre-bronchodilator FVC, L

2.58 (0.75) *

2.60 (0.70) *

Pre-bronchodilator FEV1/FVC, %
Post-bronchodilator FEV1, L
Post-bronchodilator FVC, L
Post-bronchodilator FEV1/FVC, %

80.00 (9.31) *
1.32 (0.60) *

81.44 (6.92) *
-

2.15 (0.81) *

59.99 (11.17) *

All data are shown as n (%), unless otherwise specied.

*
Data are shown as the mean (SD).
Only data for patients with COPD were shown because subjects without COPD did not
receive post-bronchodilator spirometry testing.
p < 0.05 between cross-sectional study and cohort study.

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BMI and COPD

As the cross-sectional study has shown, patients with
low BMI had a higher prevalence of COPD than those
with normal BMI (21.1% vs. 7.5%), with an adjusted OR
of 2.75 (95% CI, 1.69 to 4.47) (Table 2). In addition, it
appeared that the subjects with higher BMI had a lower
likelihood of COPD (Ptrend < 0.001). This association
was further identied in the follow-up cohort study, as
shown in Table 3.
Non-COPD subjects with low BMI at baseline were
more prone to developing COPD than were those without low BMI, with an RR of 2.88 (95% CI, 1.06 to 7.85).
In addition, as shown in Table 2, males, elderly subjects,
smokers and subjects with a family history of respiratory
disease were more likely to develop COPD. Non-COPD
subjects with low FEV1/FVC at baseline and those with
a higher smoking index were also more likely to develop
COPD (Table 3). Finally, we found that patients with
COPD had lower BMIs than those without COPD,
and patients with stage IV COPD had the lowest BMIs
(Figure 1). The baseline survey showed that both low
BMI and obese subjects with or without COPD had
lower FEV1 after adjustment for covariates (Figure 2).

Discussion
The major nding of this study was that low BMI was
associated with an increased incidence of COPD, and
that this association was not merely observed at a later
stage of COPD. A major strength of the present study
compared to previous studies is that it provides comprehensive data about COPD and BMI in the general
population using both cross-sectional and prospective
approaches. With regard to the association between
COPD and low BMI, researchers have previously suggested that low BMI was secondary to COPD (15)
and could be attributed to the systemic inammation,
imbalance of oxidative status and tissue hypoxia present
in COPD patients (1618).
In contrast to this hypothesis, we observed that subjects with low BMI were at a substantially elevated risk
of COPD even after adjusting for other potential risk
factors. Our results were consistent with the reports of
Harik-Khan and Higgins. Harik-Khan (5) has indicated
that men with a low BMI are at increased risk of developing COPD, and Higgins (19) has demonstrated that
the incidence of obstructive airway disease, dened as a
predicted FEV1 < 65%, is highest in lean men and lowest
in overweight men.
The association between low BMI and an excessive
incidence of COPD may be explained by several factors.
First, poor nutritional status at birth or during early
infancy is associated with impaired lung function or the
development of COPD in adulthood (20, 21). Although
we assessed low adulthood BMI rather than low birth
weight, both of these observations suggest that malnutrition reduces respiratory muscle and is likely to increase
the likelihood of chronic lung infections (22, 23). Second,

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Zhou et al.

Table 2. Association between BMI and COPD in a population-based cross-sectional study

Crude

COPD
(n, %)

OR (95% C.I.)

Low (<18.5)

166

35 (21.1)

3.28 (2.11-5.08)

Normal (18.5-23.9)

1008

76 (7.5)

1.00 (Reference)

Overweight (24.0-27.9)

524

22 (4.2)

0.54 (0.33-0.87)

0.012

0.49 (0.30-0.82)

0.006

Obese (28.0)

120

1 (0.8)

0.10 (0.01-0.75)

0.025

0.11 (0.02-0.85)

0.034

40-49 yrs

517

9 (1.7%)

1.00 (Reference)

50-59 yrs

384

13 (3.4%)

1.98 (0.84-4.68)

0.120

2.21 (0.92-5.31)

0.077

60-69 yrs

521

42 (8.1%)

4.95 (2.38-10.28)

<0.001

5.41 (2.56-11.44)

<0.001

70 yrs or over

396

70 (17.7%)

12.12 (5.97-24.60) <0.001

OR (95% C.I.)

<0.001

BMI (kg/m )

Age (years)

<0.001

730

101 (13.8%)

5.13 (3.42-7.70)

Female

1088

33 (3.0%)

1.00 (Reference)

Family history of respiratory disease

<0.001

1.00 (Reference)

<0.001
1.00 (Reference)

12.11 (5.75-25.49) <0.001

<0.001

Male

p
<0.001

2.75 (1.69-4.47)

<0.001

Sex

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Adjusted*

Subjects
(n)

<0.001
3.04 (1.85-5.00)
1.00 (Reference)

0.376

0.046

Yes

354

30 (8.5%)

1.21 (0.79-1.85)

1.61 (1.01-2.58)

No

1464

104 (7.1%)

1.00 (Reference)

1.00 (Reference)

Never smoked

1179

44 (3.7%)

1.00 (Reference)

Current smoker

412

51 (12.4%)

3.64 (2.39-5.55)

<0.001

1.76 (1.05-2.95)

0.031

Former smoker

227

39 (17.2%)

5.35 (3.39-8.46)

<0.001

1.83 (1.06-3.16)

0.029

<15 pack-yrs

1370

60 (4.4%)

1.00 (Reference)

15-29 pack-yrs

196

19 (9.7%)

2.34 (1.37-4.02)

<0.001

1.12 (0.61-2.06)

0.716

30-44 pack-yrs

124

21 (16.9%)

4.45 (2.61-7.61)

<0.001

1.94 (1.05-3.57)

0.033

7.90 (4.94-12.63)

<0.001

2.10 (1.21-3.67)

0.009

Smoking status

<0.001

Smoking index

0.047
1.00 (Reference)

0.002

45 pack-yrs

128

34 (26.6%)

0.027
1.00 (Reference)

*Adjusted for age, sex, education, smoking status and index, occupational exposure to dust, and family history of respiratory disease.

Table 3. Association between BMI and COPD in population-based cohort study

Subjects
(n)

COPD
(n, %)

Crude
RR (95% C.I.)

BMI (kg/m2)
Low (<18.5)
Normal or over (18.5)

Adjusted*
p

RR (95% C.I.)

0.019
57
702

6 (10.5)
26 (3.7)

3.06 (1.20-7.77)

2.88 (1.06-7.85)

1.00 (Reference)

Age (years)

p
0.039

1.00 (Reference)
0.185

0.852

40-49 yrs

198

4 (2.0)

1.00 (Reference)

50-59 yrs

176

6 (3.4)

1.71 (0.48-6.17)

0.411

1.21 (0.32-4.66)

0.781

60-69 yrs

231

12 (5.2)

2.66 (0.84-8.38)

0.095

1.54 (0.46-5.20)

0.485

70 yrs or over

154

10 (6.5)

3.37 (1.04-10.95)

0.044

1.68 (0.46-6.15)

Smoking index
<15pack-yrs

1.00 (Reference)

<0.001
529

11 (2.1)

1.00 (Reference)

15-29 pack-yrs

97

6 (6.2)

3.11 (1.12-8.61)

30-44 pack-yrs

72

8 (11.1)

45 pack-yrs

61

7 (11.5)

1.00 (Reference)
0.029

1.66 (0.52-5.33)

0.396

5.89 (2.28-15.18)

<0.001

2.77 (0.91-8.48)

0.073

6.10 (2.27-16.40)

<0.001

2.45 (0.76-7.91)

Sex

0.133
0.089

Male

316

24 (7.6)

Female

443

8 (1.9)

Baseline FEV1/FVC

0.433
0.036*

4.47 (1.98-10.08)

<0.001

2.25 (0.88-5.75)

<0.001

0.92 (0.85-0.98)

1.00 (Reference)
0.87 (0.81-0.94)

1.00 (Reference)
0.015

*Adjusted for age, sex, education, smoking index, occupational exposure to dust, and family history of respiratory disease.

When BMI was included in the logistic regression model as a continuous variable, the adjusted OR was 1.14 (1.021.26), p = 0.017.

Baseline FEV1/FVC was included into the logistic regression model as a continuous variable.

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Association between BMI and COPD in Guangzhou, China

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Figure 1. BMI stratied by non-COPD and COPD stages in the population-based

cross-sectional study, after adjustment for age, sex, education, co-morbidity,
smoking, occupational exposure to dust, and family history of respiratory disease.

an independent analysis of the female subgroup in the

cohort study. Second, like many other prospective studies, this study has an inevitable survivor bias. However,
the inuence of this eect should be minor because
COPD is typically not a fatal condition.
In addition, the assessment of nutritional status based
on BMI has several inherent limitations, in that the loss
of skeletal muscle mass is the main cause of weight loss
in patients with COPD, and this commonly occurs at an
earlier stage of COPD than does the decrease in BMI.
Recent data have suggested that fat-free mass index
(FFMI) and mid-arm muscle area (MAMA) can provide
information beyond that provided by BMI (2830).
In summary, we have found that low BMI is an important risk factor for development of COPD, independent
of patient age, smoking status, and other potential risk
factors. The source of this relationship is unclear, but it
raises the possibility that early intervention in patients
with low BMI may reduce the occurrence of COPD.

Acknowledgements

Figure 2. Estimated FEV1 for each BMI stage in the population-based crosssectional study, after adjustment for age, sex, education, co-morbidity, smoking
index, occupational exposure to dust, and family history of respiratory disease.

We are grateful to Prof. Shiliang Liu (Health Surveillance and Epidemiology Division, Health Promotion
and Chronic Disease Prevention Branch, Public Health
Agency of Canada, Ministry of Health, Ottawa) for their
assistance in English.

Declaration of Interest Statement

increases in BMI over time provoked greater decreases
in FVC than in FEV1; therefore, the ratios of FEV1/FVC
increased as BMI increased because both FVC and FEV1
decreased (24).
Third, the lower caloric intake by cigarette smokers
may contribute to the nding that low BMI subjects were
more susceptible to COPD. However, smoking-induced
low caloric intake cannot completely account for low
BMI because the association of leanness with a higher
risk of respiratory mortality was also observed in nonsmokers (never smokers) (25, 26). Hence, weight loss in
COPD is unlikely to be due to simple malnutrition. In
addition, decits in cell-mediated immunity and circulating T-lymphocyte numbers caused by protein-energy
malnutrition can lead to an increased susceptibility to
infection (27), which exacerbate declines in pulmonary
function and are considered important risk factors for
COPD (23).
A somewhat surprising result of this study is our
nding that subjects with high baseline BMI had a lower
risk of developing COPD, despite their lower FEV1. We
had initially suspected that the predominantly restrictive eects of central obesity would eventually lead to a
reduction in both FVC and FEV1.
However, this study has several limitations that
must be acknowledged. First, there were insucient
subjects with low BMI and newly developed COPD for
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Supported by Chinese Central Government key

research projects of the 10th national 5-year development plan grants 2001BA703B03(A) (P.R.) and The
National Key Technology R&D Program of the 12th
National Five-year Development Plan 2012BAI05B01
(P.R.).
The researchers were also independent from funders.
The study funders were independent from the study in
design, collection, analysis, interpretation of data, writing of the report, and in the decision to submit the article
for publication. The study protocol was approved by the
Medical Ethics Committee of Guangzhou Institute of
Respiratory Diseases on 20 May 2002.
Yumin Zhou collected the data and monitored data
collection, planned the statistical analysis, analysed
the data, and drafted the manuscript. Dali Wang,
Shengming Liu, and Jiachun Lu implemented the trial.
Jingping Zheng and Nanshan Zhong conducted and
monitored data collection. Pixin Ran initiated and
designed the project, monitored data, and drafted the
paper. Yumin Zhou and Pixin Ran are guarantors.

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