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Andréa Lessard MSc
Nathalie Alméras PhD
Hélène Turcotte MSc
Angelo Tremblay PhD
Jean-Pierre Després PhD, FAHA
Louis-Philippe Boulet MD, FRCPC
Centre de recherche de l’Institut universitaire
de cardiologie et de pneumologie de Québec
(CRIUCPQ), Québec, Canada.
Adiposity and pulmonary function:
Relationship with body fat
distribution and systemic
inammation
Abstract
Purpose: Obesity is associated with changes in pulmonary function and increased systemic
inammation. We explored the relationships among adiposity, body fat distribution indi-
ces, serum inammatory markers and pulmonary function.
Methods: is was a post-hoc cross-sectional analysis that included subjects who had pre-
viously participated in randomized studies on obesity at our centre. Non-smoking seden-
tary men (282 subjects, mean age 42) without respiratory diseases were studied. BMI,
waist circumference (WC), visceral and subcutaneous adipose tissue (AT), lung residual
volume (RV), vital capacity (VC) and expiratory reserve volume (ERV) were measured.
Serum leptin, adiponectin, tumor necrosis factor alpha (TNF-α) and high-sensitive C-
reactive protein (hs-CRP) levels were measured.
Results: In subjects with metabolic syndrome (n=124), percent predicted ERV and RV
were signicantly associated with BMI (ERV: r=-0.19, p=0.02, RV: r=-0.28, p=0.0007),
WC (r=-0.20, p=0.02, r=-0.26, p=0.002), visceral (r=-0.22, p=0.007, r=-0.25, p=0.002)
and subcutaneous AT (r=-0.19, p=0.02, r=-0.28, p=0.0007). Percent predicted VC corre-
lated with visceral (r=-0.20, p=0.02) and subcutaneous AT (r=-0.18, p=0.03). Leptin was
strongly correlated with BMI (MS/no-MS: r=0.52, p=0.0005/r=0.62, p<0.0001), WC
(r=0.41, p=0.008/r=0.49, p<0.0001), visceral (r=0.27,p=0.09/0.43, p<0.0001) and sub-
cutaneous AT (r=0.46, p=0.003/r=0.66, p<0.0001), while adiponectin levels were associ-
ated in subjects with no-MS with WC (r=-0.20, p=0.01), visceral (r=-0.22, p=0.008), and
subcutaneous AT (r=-0.17, p=0.05). When adjusted for anthropometric measures, neither
ERV, RV nor VC was signicantly correlated with serum leptin, adiponectin, TNF-α, or
hs-CRP levels.
Conclusion: ese results suggest that the inuence of obesity on lung function in healthy
subjects is mostly mediated by mechanical factors. Furthermore, not only BMI but also the
pattern of fat distribution should be considered when studying associations between adi-
posity indices and mechanical or inammatory variables potentially associated with
pulmonary function.
ORIGINAL RESEARCH
© 2011 CIM Clin Inv().%"$%&'!" E64
Correspondence to:
Louis-Philippe Boulet, MD
Institut universitaire de cardiologie et de pneumologie de Québec (IUCPQ)
2725 chemin Sainte-Foy, Québec, QC Canada, G1V 4G5
Email: lpboulet@med.ulaval.ca
$*('!&)(*#!))) &)#'
$*('!&)&)) '
Clin Invest Med 2011; 34 (2): E64-E70.
Obesity is associated with an increase in the work of breathing,
reduced respiratory compliance and hypoventilation, and has
been considered to contribute to disorders such as sleep apnea
syndrome, obesity/hyperventilation syndrome and, more re-
cently, asthma [1]. Increased body mass index (BMI) is also
associated with lung mechanical changes such as reduced func-
tional residual capacity (FRC) and expiratory reserve volume
(ERV). It has been suggested that pulmonary function could
be inuenced by body fat distribution as assessed by the ratio of
waist-to-hip circumferences [2,3]; however, waist-to-hip ratio
provides only an index of relative accumulation of abdominal
fat [4]. ere is a need to study the impact of abdominal fat
distribution, assessed by more precise imaging techniques such
as computed tomography, on pulmonary function.
Obesity is an inammatory state. Among others, serum
leptin levels, a pro-inammatory adipokine and serum levels of
TNF-α are increased in obesity [5]. Consistent with this, se-
rum adiponectin level, an anti-inammatory adipokine, is typi-
cally decreased in the obese subject [5]. ese hormones have
been suggested to play a role in the pathogenesis of cardiovas-
cular diseases and diabetes [6]. Plasma IL-6, C-reactive protein
(CRP) and TNF-α are inammatory factors that are also in-
creased in obesity [7-9]. erefore, the systemic inammation
associated with obesity could contribute to the development
and/or the persistence of airway inammatory disorders such
as asthma and Chronic Pulmonary Obstructive Disease
(COPD) [10,11]. e additional impact on pulmonary func-
tion of systemic inammation, and their relationships with
mechanical changes associated with obesity, remains to be de-
termined.
e main objective of this study was to quantify the rela-
tionships among anthropometric markers of adiposity/body fat
distribution and specic variations in pulmonary function in
subjects with and without a metabolic syndrome (MS or no-
MS). As secondary analyses, the relationships between anthro-
pometric markers and systemic inammatory factors were
compared and the links between markers of systemic inam-
mation and pulmonary function were evaluated.
Materials and Methods
is post-hoc cross-sectional analysis was conducted on a data-
base kept in our institution that included male subjects who
had previously taken part in randomized studies on obesity and
for whom data on pulmonary function was available. Various
markers of obesity and systemic inammation were measured
in a sub-group of this cohort, in the context of a research
program on the metabolic eects of obesity. All subjects were
sedentary, doing less than 30 minutes of exercise per week, aged
18 years and over, had no known metabolic disorders or respi-
ratory diseases and were non-smokers at the time of the enrol-
ment. All appropriate subjects were included in the study. e
studies were approved by the Ethics Committee of Laval
Hospital Research Center and all subjects had signed an in-
formed consent form.
Body mass index (BMI) was calculated from measured
height and weight. Obesity, was dened as a BMI >30 kg/m2,
overweight >25 to <30 kg/m2 and normal weight <25 kg/m2.
Waist circumference (WC) was measured at the narrowest part
of the torso while the subject was standing. Abdominal visceral
and subcutaneous adipose tissue (AT) area were measured by
computed tomography (CT) on a Siemens Somatom DRH
scanner (Erlangen, Germany) as previously described [12].
FRC was assessed with the helium dilution technique of
Meneely and Kaltreider [13]. ERV was calculated by subtract-
ing VC from FRC. Residual volume (RV) was obtained in sub-
tracting ERV from FRC. Pulmonary volumes were expressed as
percentage of predicted values. Predicted values were calcu-
lated using reference values of the European Respiratory Soci-
ety [14].
Blood samples were obtained in the morning aer a 12h
overnight fast. Fasting plasma leptin and adiponectin concen-
trations were determined by an enzyme-linked immunosorbent
assay (ELISA) (B-Bridge International, Inc., San Jose, CA,
USA) on whole plasma kept at –80°C until use. Fasting plasma
tumor necrosis factor alpha (TNF-α) concentrations were also
assessed on deeply frozen plasma samples (80°C) and were
measured by a high sensitivity ELISA for human TNF-α
(R&D Systems Inc, Minneapolis, USA). Serum IL-6 levels
were measured using a human IL-6 Elisa kit (R&D Systems
Inc, MN, USA). High sensitive-CRP (hs-CRP) was assessed
using a highly sensitive immunoassay (hs-CRP) that uses a
monoclonal antibody coated to polystyrene particles per-
formed on the Behring BN-Prospect nephelometer (Dade Be-
hring) according to methods described by the manufacturer
[15].
e criteria used to dene metabolic syndrome (MS) were
those of the Diabetes International Federation; that is to have
at least three of the ve following risk factors: high fasting
plasma glucose (>5.6 mmol/L), high blood pressure (≥ 130/85
mmHg), increased waist circumference (≥ 102 cm), increased
triglycerides (≥ 1.7 mmol/L) and reduced HDL-cholesterol (≤
1.0 mmol/l) [16].
Variables were expressed using mean ± standard deviation.
Relationships between variables were measured using univari-
ate linear regression analyses. To take into account possible
confounding factors, such as BMI, WC and AT, adjusted corre-
Lessard et al. Obesity and pulmonary function
© 2011 CIM Clin Inv().%"$%&'!" E65
lations were performed using multivariate regression analyses.
P-value < 0.05 using a two-tailed test was deemed signicant.
Data were analysed using the statistical package SAS (SAS In-
stitute, Inc.,Cary, NC, USA).
Results
Two hundred eighty two men were included in the analy-
sis. A total of 124 subjects responded to the criteria of a MS
while the other 158 had no-MS, with fewer than three meta-
bolic risk factors. Many subjects had measures of systemic
inammatory factors such as leptin (n = 132), adiponectin (n
= 267), TNF-α (n = 228), IL-6 (n = 228), hs-CRP (n = 91)
and white blood cell (WBC) count (n = 205). e subjects’
characteristics are summarized in Table 1. BMI distribution is
presented in Figure 1.
Among the MS and no-MS subjects, mean percent of pre-
dicted ERV was, respectively, 85 ± 47 and 96 ± 33 (p = 0.02),
mean percent of predicted values were, respectively, 90 ± 20
and 91 ± 17 (p = 0.60) for RV, 98 ± 11 and 101 ± 12 (p =
0.009) for VC, and 79 ± 16 and 96 ± 21 (p < 0.0001) for
FRC. Correlations between anthropometric measurements and
specic variations in pulmonary function are presented in Ta-
ble 2. Briey, in subjects with a MS, decreased percent of pre-
dicted ERV and RV were signicantly associated with an in-
creased BMI, WC, visceral and subcutaneous AT. Decreased
percent of predicted VC was only slightly but signicantly cor-
related with visceral and subcutaneous AT although not with
BMI and WC. ere were no signicant correlations between
anthropometric measurements and percent of predicted ERV,
RV or VC in subjects with no-MS.
Mean values for measured inammatory markers are given
in Table 3 for subjects with or without MS. Leptin, adipo-
neptin and hs-CRP levels and WBC counts were signicantly
higher in subjects with MS than in those with no-MS. Among
the subjects with a MS who had systemic inammatory marker
measurements, leptin was signicantly correlated with BMI,
WC, and subcutaneous AT while adiponectin, Il-6 and TNF-α
were not signicantly correlated with any of the anthropomet-
ric markers. Hs-CRP was signicantly correlated with WC and
Lessard et al. Obesity and pulmonary function
© 2011 CIM Clin Inv().%"$%&'!" E66
TABLE 1. Subject’s charac
cteristics
Metabolic
syndrome
(n=124)
No metabolic
syndrome
(n = 158)
p
Age, yr
44± 8
41 ± 10
0.02
BMI (kg/m2) 32 ± 3 26 ± 4 <0.0001
WC (cm)
108 ± 8
91 ± 11
<0.0001
Visceral AT (cm2) 203 ± 59 123 ± 57 <0.0001
Subcutaneous AT(cm2)
326 ± 90
215 ± 109
<0.0001
BMI: body mass index; W
Mean + SD
WC: waist circum
umference; AT:
adipose tissue
FIGURE 1. BMI distribution in the 282 subjects with (n = 124) or without (n = 158) metabolic syndrome
Lessard et al. Obesity and pulmonary function
© 2011 CIM Clin Inv().%"$%&'!" E67
TABLE 2. Correlations between a
anthropometri
ic measuremen
ents and lung v
volumes
BM
MI
W
WC
Viscer
ral AT
Subcuta
aneous AT
r
p
r
p
r
p
r
p
Metabolic syndrome
% of predicted ERV -0.19 0.02 -0.20 0.02 -0.22 0.007 -0.19 0.02
% of predicted RV -0.28 0.0007 -0.26 0.002 -0.25 0.002 -0.28 0.0007
% of predicted VC -0.11 0.19 -0.13 0.11 -0.20 0.02 -0.18 0.03
No metabolic syndrome
% of predicted ERV -0.03 0.77 0.09 0.30 0.13 0.14 0.006 0.95
% of predicted RV -0.002 0.98 0.14 0.12 0.08 0.40 0.07 0.44
% of predicted VC
0.06
0.53
0.02
0.84
-0.15
0.09
-0.02
0.85
BMI: body mass index; WC: wais
sensitive C-reactive protein; WBC
st circumferen
C: white blood
nce; AT: adipo
d cells.
ose tissue; TNF
F-alpha: tumo
or necrosis fac
ctor; IL-6: Inte
terleukine-6; H
Hs-CRP: high-
TABLE 3. Lung volumes and systemic inammatory factors m
measurements
Systemic inammatory factors:
Metabolic syndrome
No metabolic syndrome
p
Leptin (ng/ml)
12.5 ± 9.5
6.6 ± 6.9
<0.0001
Adiponectin (μg/ml) 8.4 ± 3.8 9.9 ± 5.7 0.02
TNF-alpha (pg/ml) 1.4 ± 0.7 1.2 ± 0.6 0.07
IL-6 (pg/ml) 1.3 ± 0.9 1.1 ± 1.1 0.20
Hs-CRP (mg/L) 1.8 ± 1.2 0.9 ± 0.9 0.0005
WBC (X 109/L)
6.0 ± 1.1
5.5 ± 1.3
0.003
ERV: expiratory reserve volume; RV: residual volume; VC: vi
High-sensitive C-reactive protein; WBC: white blood cells.
Mean + SD
vital capacity; TNF-alpha: Tumo
or necrosis factor; IL-6: Interl
leukine-6; Hs-CRP:
TABLE 4. Correlations b
between systemi
ic in
ammatory
y factors and an
nthropometric m
measurements
BM
MI
W
WC
Viscer
ral AT
Subcutan
neous AT
r
p
r
p
r
p
r
p
Metabolic syndrome
Leptin (n = 41) 0.52 0.0005 0.41 0.008 0.27 0.09 0.46 0.003
Adiponectin (n = 121)
0.47
0.61
0.08
0.39
-0.05
0.61
0.15
0.11
TNF-alpha (n = 107) 0.03 0.76 0.04 0.69 0.06 0.57 0.06 0.53
IL-6 (n = 108) 0.14 0.15 0.11 0.24 0.08 0.43 0.09 0.33
Hs-CRP (n = 20) 0.37 0.11 0.52 0.02 0.51 0.02 0.41 0.08
WBC (n = 102) 0.16 0.11 0.26 0.007 0.18 0.08 0.15 0.13
No metabolic syndrome
Leptin (n = 91) 0.62 <0.0001 0.49 <0.0001 0.43 <0.0001 0.66 <0.0001
Adiponectin (n = 146) -0.16 0.06 -0.20 0.01 -0.22 0.008 -0.17 0.05
TNF-alpha (n = 121) 0.05 0.60 0.02 0.82 -0.02 0.87 0.10 0.30
IL-6 (n = 120) 0.21 0.02 0.16 0.07 0.09 0.35 0.23 0.01
Hs-CRP (n = 71) 0.26 0.03 0.26 0.03 0.19 0.12 0.25 0.04
WBC (n = 103)
0.21
0.04
0.24
0.02
0.23
0.02
0.24
0.01
BMI: body mass index; W
sensitive C-reactive prote
WC: waist circu
ein; WBC: whit
umference; AT:
te blood cells.
adipose tissue;
TNF-alpha: tu
umor necrosis f
factor; IL-6: Int
terleukine-6; Hs
Hs-CRP: high-
visceral AT and WBC were signicantly correlated with WC
only (Table 4). In subjects without MS, leptin was strongly
correlated with increased BMI, WC, visceral and subcutaneous
AT, adiponectin was signicantly correlated with WC, visceral
AT and also slightly with subcutaneous AT. IL-6, hs-CRP and
WBC were signicantly but slightly correlated with BMI and
subcutaneous AT, hs-CRP and WBC were also slightly corre-
lated with WC and nally, WBC was slightly correlated with
visceral AT (Table 4).
Finally, when adjusted for BMI, WC, visceral and subcu-
taneous AT, neither ERV, neither RV nor VC were correlated
with leptin, adiponectin, TNF-α or hs-CRP in either subjects
with MS or without MS (Table 5). No signicant correlations
were found between IL-6 or WBC and ERV, RV or VC in sub-
jects with MS. A weak correlation was found in subjects with
no-MS between VC and IL-6 and between VC and WBC.
Discussion
We found that ERV, RV and leptin levels are signicantly asso-
ciated with anthropometric measures in subjects with MS
while there are no signicant associations among ERV, RV or
VC and anthropometric measures subjects without MS. Fur-
thermore, leptin and adiponectin levels are signicantly corre-
lated with anthropometric measures in subjects with no MS.
Markers of systemic inammation were not signicantly asso-
ciated with changes in ERV, RV and VC aer adjustment for
anthropometric characteristics except for a weak correlation of
IL-6 and WBC with changes in VC in subjects with no-MS.
Our study suggests that the obesity phenotype, in terms of
fat distribution, should be taken into consideration when
evaluating the impact of obesity on pulmonary function. As
already reported, increased BMI is associated with a reduction
in ERV oen without change in RV [1]. In agreement with
recent data from Babb ) " correlations among markers of
abdominal obesity and ERV were similar to those with BMI,
suggesting that global obesity rather than abdominal obesity
&'( is associated with breathing near the closing volume [17];
however, a dierent conclusion was reached for VC. While a
study by Ray et al. showed no change in VC among 43 healthy
non-smoking obese subjects [18], VC was reduced to 75% of
the predicted value in 43 morbidly obese subjects [19]. In our
study, the correlation was signicant with visceral and subcuta-
neous AT in subjects with MS, suggesting that body fat distri-
bution may particularly inuence VC in this group. Since ERV
seems to be inuenced by BMI and not only abdominal obe-
sity, these results suggest an impact of abdominal obesity on
inspiratory capacity. It has been suggested that decreased inspi-
ratory capacity in obese subjects may result in impaired inspira-
tory muscle activity during exercise [20] and in reduction of
the bronchoprotection of deep inspiration during induced
bronchoconstriction [21]. e impact of body mass distribu-
tion on inspiratory capacity and its link to dyspnea and respira-
tory diseases such asthma in obese subjects needs to be further
explored.
Lessard et al. Obesity and pulmonary function
© 2011 CIM Clin Inv().%"$%&'!" E68
TABLE 5. Correlations between syste
emic in
ammatory
y factors and lung v
volumes adjusted f
for anthropometri
ic measurements
% of predi
icted ERV
% of pred
dicted RV
% of pred
dicted VC
r
p
r
p
r
p
Metabolic syndrome
Leptin (n = 41) 0.15 0.36 -0.05 0.78 -0.15 0.34
Adiponectin (n = 121) 0.17 0.07 0.12 0.18 0.11 0.22
TNF-alpha (n = 107) -0.11 0.25 0.002 0.99 -0.07 0.50
IL-6 (n = 108) -0.04 0.65 -0.05 0.61 -0.08 0.44
Hs-CRP (n = 20) -0.16 0.49 0.32 0.17 -0.11 0.63
WBC (n = 102) -0.13 0.20 0.11 0.28 -0.18 0.07
No metabolic syndrome
Leptin (n = 91) -0.02 0.83 -0.19 0.08 -0.07 0.07
Adiponectin (n = 146) 0.11 0.20 0.11 0.17 0.06 0.50
TNF-alpha (n = 121) 0.08 0.40 0.04 0.69 0.0006 0.99
IL-6 (n = 120)
-0.17
0.06
0.05
0.62
-0.23
0.01
Hs-CRP (n = 71) -0.10 0.40 -0.06 0.61 0.11 0.38
WBC (n = 103)
-0.12
0.24
-0.16
0.10
-0.20
0.05
ERV: expiratory reserve volume; RV: r
tein; WBC: white blood cells; IL-6: in
residual volume; V
nterleukine-6.
VC: vital capacity;
; TNF: tumor necr
crosis alpha; Hs-CR
RP: high-sensitive
e C-reactive pro-
As already reported in other studies, serum levels of adi-
ponectin seemed to be inuenced by the body mass distribu-
tion. In agreement with Staiger et al. [5], adiponectin levels
were found to be predominantly related to the visceral fat
compartment while serum leptin levels were associated with
overall obesity as estimated by the BMI. Since adipokines have
been proposed to play a role in the physiopathology of respira-
tory diseases in obese subjects [10,11], these results reiterate
the importance of considering body fat distribution when as-
sessing pulmonary function in obese subjects.
Finally, there were no signicant association between most
of the systemic inammatory markers classically associated
with obesity and pulmonary function changes, suggesting that
the impact of obesity on pulmonary function is mainly medi-
ated by mechanical factors. Little is known about the eect of
systemic inammation markers on pulmonary function among
subjects without known respiratory disease and this study pro-
vides additional data on this topic.
is study has some limitations, being a retrospective
analysis performed only on data from male subjects with mark-
ers of inammation assessed only in sub-groups of subjects.
Nevertheless, highly signicant results were obtained, shedding
more light on the combined eects of mechanical and
inammatory markers on pulmonary function of the obese
subject. Our study is also limited to lung volumes and the ef-
fects of the factors evaluated on airway obstruction could not
be evaluated. Such analysis should be performed in subjects
with airway inammatory diseases to determine if similar asso-
ciations would be observed. Sutherland et al. recently suggested
that systemic inammation does not signicantly inuence
airway inammation in obese asthmatic subjects, although this
issue will require more extensive evaluation [22]. Watz et al.
showed that about half of the patients with chronic bronchitis
and COPD had a co-existing metabolic syndrome associated
with increased level of hs-CRP and IL-6 independent of lung
function impairment [23]. An inverse relationship has also
been shown between CRP concentrations and measures of
pulmonary function (FEV1, FVC and PEF) in subjects without
pulmonary diseases and in non-smokers [24]. Kony et al. found
that in adults, increased CRP levels were strongly and inde-
pendently associated with FEV1 and FVC impairment and
more frequent bronchial hyperresponsiveness [25] and that
both female gender and CRP levels were signicantly associ-
ated with airway hyperresponsiveness. Our study included
men only and dierent lung volumes were evaluated; these dif-
ferences could explain some apparent discrepancies between
the results. Rasmussen et al. showed that in young men, higher
levels of CRP at age 20 years predicted the decline in lung
function by age 39 years [26]; however, other studies either on
young or older adults did not demonstrate that CRP levels
predicted a subsequent decline in lung function [27,28].
It is possible that lung function could be altered by other
obesity-associated features such as the metabolic syndrome. In
our study, a signicant inverse correlation was found between
lung function measures (ERV and RV) and BMI, WC, visceral
and subcutaneous tissue only in the group of subject with
metabolic syndrome. Indeed, this last syndrome, usually char-
acterized by abdominal obesity, hyperglycemia, hyperinsuline-
mia, dyslipidemia, and high arterial blood pressure, has been
associated with an increased risk of coronary heart disease in
middle-aged subjects but also to a reduction in pulmonary
function [29]. In this regard, Leone et al. reported that lung
function impairment was associated with metabolic syndrome
independently of age, sex, smoking status, alcohol consump-
tion, educational level, body mass index, leisure-time physical
activity and cardiovascular disease history [29]. Following fac-
tor analysis, three main elements were inversely related to lung
function: low high-density lipoprotein cholesterol/high tri-
glycerides, high fasting glycemia/high blood pressure and ab-
dominal obesity, although this last factor was the strongest
predictor of lung function impairment, for both women and
men.
In conclusion, these results suggest that obesity is associ-
ated with variations in pulmonary function and increases in
systemic inammation although the obesity-related changes in
lung function do not seem to be signicantly related to
systemic inammation.
List of Abbreviations
AT Adipose Tissue
BMI Body Mass Index
CRP C-reactive protein
CT Computed Tomography
ELISA Enzyme-Linked Immunosorbent Assay
ERV Expiratory Reserve Volume
IL-6 Interleukine-6
FRC Functional Residual Capacity
Hs-CRP High-sensitive C-reactive protein
MS metabolic syndrome
No-MS No metabolic syndrome
RV Residual Volume
TNF-α Tumor Necrosis Factor Alpha
VC Vital Capacity
WBC White blood cell counts
WC Waist Circumference
Lessard et al. Obesity and pulmonary function
© 2011 CIM Clin Inv().%"$%&'!" E69
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