Relationship between Lung Function and Metabolic Syndrome
Citation: Chen W-L, Wang C-C, Wu L-W, Kao T-W, Chan JY-H, et al. (
Relationship between Lung Function and Metabolic Syndrome
Wei-Liang Chen 0
Chung-Ching Wang 0
Li-Wei Wu 0
Tung-Wei Kao 0
James Yi-Hsin Chan 0
Ying-Jen Chen 0
Ya-Hui Yang 0
Yaw-Wen Chang 0
Tao-Chun Peng 0
Cordula M. Stover, University of Leicester, United Kingdom
0 1 Division of Family Medicine, Department of Family and Community Medicine, Tri-Service General Hospital and School of Medicine, National Defense Medical Center , Taipei, Taiwan , 2 Division of Geriatric Medicine, Department of Family and Community Medicine, Tri-Service General Hospital and School of Medicine, National Defense Medical Center , Taipei, Taiwan , 3 Graduate Institute of Medical Sciences, National Defense Medical Center , Taipei, Taiwan , 4 Department of Occupational Safety and Hygiene, Fooyin University , Kaohsiung , Taiwan
Although the link between impaired lung function and cardiovascular events and type 2 diabetes mellitus has been recognized, the association between impaired lung function and metabolic syndrome has not been comprehensively assessed in the United States (U.S.) population. The aim of our study was to explore the association between impaired lung function and metabolic syndrome in a nationally representative sample of men and women. This cross-sectional populationbased study included 8602 participants aged 20-65 years in the Third National Health and Nutrition Examination Survey (NHANES III). We examined the relationship between the different features of metabolic syndrome and lung function, including forced vital capacity (FVC) and forced expiratory volume in 1 second (FEV1). After adjusting for potential confounders such as age, body mass index, inflammatory factors, medical condition, and smoking status, participants with more components of metabolic syndrome had lower predicted values of FVC and FEV1 (p for trend ,0.001 for both). Impaired pulmonary function was also associated with individual components of metabolic syndrome, such as abdominal obesity, high blood pressure, high triglycerides, and low high density lipoprotein (HDL) cholesterol (p,0.05 for all parameters). These results from a nationally representative sample of US adults suggest that a greater number of features of metabolic syndrome is strongly associated with poorer FVC and FEV1. In clinical practice, more comprehensive management strategies to address subjects with metabolic syndrome and impaired lung function need to be developed and investigated.
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. Data are available from the National Health
and Nutrition Examination Survey (http://www.cdc.gov/nchs/nhanes.htm).
Funding: The authors received no specific funding for this work.
Competing Interests: The authors have declared that no competing interests exist.
Impaired pulmonary function, which includes measurements of
forced expiratory volume in one second (FEV1) and forced vital
capacity (FVC), is mainly present in individuals with chronic
obstructive pulmonary disease (COPD) and asthma . Previous
studies have shown that reduced FEV1 is a strong predictor of
coronary heart disease, COPD-related mortality, and
cardiovascular mortality . Reduced FVC is also a marker for increased
mortality in asymptomatic adults  or individuals with metabolic
syndrome . Recent years have seen an increased focus on
metabolic syndrome in the prediction of lung function
impairment. Previous data from Asian [7,8] and European [9,10]
patients demonstrated a substantial association between impaired
pulmonary function and metabolic syndrome. However, the
diagnostic criteria and clinical features of metabolic syndrome
varied by race. Few studies have focused on the U.S. general
population to investigate the association between lung capacity
and metabolic syndrome. In addition, important risk factors
[8,11,12], such as gender, smoking status, biomarkers of
inflammation, and C-reactive protein (CRP), were not fully taken into
account in previous studies. The objective of our study was to
investigate the independent relationship between impaired lung
function and metabolic syndrome using by the Third National
Health and Nutrition Examination Survey (NHANES III) sample,
which is a well-designed population-based study with a large
sample size of US adults.
Executed during the period 19881994, NHANES III consisted
of a representative sample of the noninstitutionalized civilian US
population, which was selected by using a multistage, stratified,
and cluster sampling design . All participants were interviewed
for demographic, health, and dietary information within 2 months
of initial enrollment. After a detailed home-based interview,
participants were invited to receive pertinent examination sessions
during which blood specimens were collected. For participants
who were unable to attend the examination for health reasons, a
blood sample was obtained during the home interview. We limited
our analysis to participants aged 2065 years who attended the
medical examination and included the 8602 eligible subjects (4053
men and 4549 women) with complete information. To minimize
confounding effects, participants with a history of asthma, chronic
bronchitis, and emphysema were excluded. The NHANES III
study received National Center for Health Statistics (NCHS)
Institutional Review Board approval, and informed consent was
acquired from participants prior to starting the study.
The NHANES study protocol was approved by the NCHS
Institutional Review Board (IRB). Because our analysis exclusively
used de-identified data, it was exempt from IRB review.
Pulmonary Function Data
Spirometry was conducted using procedures based on the 1987
American Thoracic Society (ATS) recommendations . Values
used in this analysis included FVC and FEV1. The units of
measurement for FVC and FEV1 values were liters. Each eligible
subject performed at least five FVC maneuvers to meet the ATS
acceptability and reproducibility criteria. Forced exhaled volumes
were measured using a dry rolling-seal spirometer. All of the data
were stored on digital tape, allowing the recalculation of all
parameters based on ATS acceptability and reproducibility
criteria . We also used prediction equations to determine
predicted FEV1 and FVC values. Predicted FVC and FEV1
values vary with the characteristics (age, height, gender, and race/
ethnicity) of the specific population. For the United States, the
predicted FVC and FEV1 were calculated using the reference
equations developed by Hankinson et al. . The spirometry
system has been independently tested and found to exceed ATS
spirometry equipment recommendations .
Assessment of co-variates
Serum uric acid was measured using the Hitachi 737 automated
multichannel chemistry analyzer (Boehringer Mannheim
Diagnostics, Indianapolis, IN, USA). Chemical analyses of total
cholesterol, triglycerides and HDL-C cholesterol (Hitachi 704
Analyzer) were performed by the Lipoprotein Analytical
Laboratory at Johns Hopkins University, Baltimore, Maryland. LDL
cholesterol levels were calculated using the Friedewald formula
. Serum glucose was determined by using an enzymatic
reaction (Cobas Mira assay). Serum total bilirubin was measured
by using the Hitachi 737 automated autoanalyzer (Boehringer
Mannheim Diagnostics, Indianapolis, IN, USA). C-reactive
protein was measured using latex-enhanced nephelometry. All
protocols followed standardized methods that had documented
accuracy with respect to Centers for Disease Control and
Prevention (CDC) reference methods .
The participants were interviewed to collect information on sex,
age, race/ethnicity (including non-Hispanic white, non-Hispanic
black, Mexican-American, and other), body measurements
(including height, weight, and waist), blood pressure, and medical
conditions (including self-reported physician-diagnosed heart
disease, and stroke). Body mass index (BMI) was calculated by
dividing the individuals weight in kilograms by the square of their
height in meters. Waist circumference was measured by trained
NHANES staff using standard protocols. A brief questionnaire was
used to determine the patients smoking status. Detailed specimen
collection and processing instructions are presented in the
NHANES Laboratory Procedures Manual and are available on
the NHANES website .
Definition of metabolic syndrome
The revised National Cholesterol Education Programs Adult
Treatment Panel III (NCEP: ATP III) defined metabolic
syndrome as the presence of three or more of the following
characteristics: (1) abdominal obesity: waist circumference .
102 cm in men and .88 cm in women; (2) hypertriglyceridemia:
$150 mg/dL ($1.69 mmol/L);(3) reduced HDL cholesterol: ,
40 mg/dL (,1.03 mmol/L) for men and ,50 mg/dL (,
1.29 mmol/L) for women; (4) elevated blood pressure: systolic
blood pressure $130 mm Hg or diastolic blood pressure $85 mm
Hg; and (5) elevated fasting glucose: $100 mg/dL (5.6 mmol/L)
All statistical analyses were performed using SPSS (Version 18.0
for Windows, SPSS, Inc., Chicago, IL, USA). Due to the complex
survey design used in NHANES III, traditional calculations of
statistical analyses based on the assumption of a simple random
sample provided incorrect variance estimates and are not
appropriate . The Complex Samples procedure was used
to incorporate sample weights and adjust for clusters and strata of
the complex sample design. Predicted values of FEV1 and FVC
were compared by the number of metabolic components or each
individual components of metabolic syndrome. Based on
published articles, influential demographic factors, and clinical
standpoints, an extended-model approach was used for covariate
adjustments. We used 2 models with progressive degrees of
adjustment. Model 1 was adjusted for age and race/ethnicity.
Model 2 was further adjusted for BMI, C-reactive protein, serum
total bilirubin, serum uric acid, smoking, heart disease, and stroke.
The P-values for trend tests were assessed by treating the
components of metabolic syndrome as a continuous variable from
1 to 4 to observe the associations across increasing components
of metabolic syndrome and lung function impairment.
A total of 8,602 participants (4053 males and 4549 females)
were included in the study. The characteristics of the eligible
subjects stratified by gender and the presence of metabolic
syndrome are summarized in Table 1. The overall prevalence of
metabolic syndrome was 26.85%. In our study, participants with
metabolic syndrome were likely to be older and non-Hispanic
white compared with individuals without metabolic syndrome
among both men and women. The BMI, CRP, serum uric acid,
and serum total bilirubin concentration were statistically
significantly higher among those with metabolic syndrome than among
those without the syndrome (p,0.001 for all factors).
Metabolic components and pulmonary function test
Metabolic components such as SBP, DBP, waist circumference,
serum glucose, and serum triglycerides were statistically
significantly increased and HDL-C was significantly lower among those
with metabolic syndrome compared with those without the
syndrome (all of the parameters, p,0.001). In addition,
pulmonary function tests, such as FEV1, FEV1 % predicted, FVC, and
FVC1 % predicted were significantly lower among those with
metabolic syndrome compared with those without the syndrome
(all of the parameters, p,0.001). For the FEV1/FVC ratio, no
statistically significant difference was noted between those with
and without metabolic syndrome for both men and women
(p = 0.588 and p = 0.079, respectively).
Continuous variables, mean (SD)
Waist circumference (cm)
Serum triglycerides (mg/dL)
Serum glucose (mg/dL)
C-reactive protein (mg/dL)
Serum uric acid (mg/dL)
Serum total bilirubin (mg/dL)
FEV1 % predicted
FVC % predicted
Categorical variables, n (%)
Men (n = 4053)
syndrome N = 3164
Women (n = 4549)
syndrome N = 3128
syndrome N = 889
syndrome N = 1421
SD, standard deviation;BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; HDL-C, high-density lipoprotein cholesterol; WBC, white blood
cell; CRP, C-reactive protein; FEV1, forced expiratory volume in 1; FVC, forced vital capacity.
Metabolic components and FVC predicted percentages
Results from models examining the association between
metabolic components and FVC percent predicted values
stratified by gender are presented in Table 2. As shown, there
was a strong linear decrease in FVC percent predicted as the
number of components of metabolic syndrome increased. After
additional adjustment, the b coefficients of FVC percent predicted
(%) for those with 1, 2, 3, and $4 features of metabolic syndrome
were 0.006, 20.004, 20.021, and 20.049 in men and 20.017,
20.024, 20.041, and 20.073 in women, respectively (p for trend
,0.001). In both males and females, abdominal obesity, high
blood pressure, high triglycerides, high glucose, and low HDL-C
were significantly associated with lower FVC percent predicted in
fully adjusted models (all of the parameters, p,0.05).
Metabolic components and FEV1 predicted percentages
Results from models examining the association between
metabolic components and FEV1 percent predicted stratified by
gender are presented in Table 3. There was a significant inverse
relationship between the number of components present and
pulmonary function. After additional adjustment, the b coefficients
of FEV1 percent predicted for those with 1, 2, 3, and $4 features
of metabolic syndrome were 0.001, 20.011,20.027, and 20.045
in men and 0.007, 20.007, 20.018 and 20.040 in women,
respectively (p for trend ,0.001). In both males and females,
abdominal obesity, high blood pressure, high triglycerides, and low
HDL-C were significantly associated with lower FEV1 percent
predicted in fully adjusted models (all of the parameters, p,0.05).
High glucose was significantly associated with lower FEV1 percent
predicted in fully adjusted models in females.
This study used a nationally representative sample of the U.S.
population to examine the relationship between pulmonary
function and metabolic syndrome, defined using revised ATP III
criteria. Our findings indicated that both FEV1 and FVC were
lower in proportion to the number of metabolic syndrome
components the patients had. Notably, individual components of
abdominal obesity, low HDL-C, high triglycerides, and high blood
pressure were significantly associated with decreasing FVC and
FEV1 in both males and females.
Metabolic syndrome is a complex disorder featuring chronic
inflammation characterized by the constellation of abdominal
obesity, hyperglycemia, hypertension, and dyslipidemia. Its
definition varies by organization and expert group. The definition
of the revised NCEP: ATP III is one of the most widely used.
Although previous studies examined the association between
individual components of metabolic syndrome and pulmonary
function, the contribution of each component of metabolic
syndrome to complications and comorbidity seems to differ
between each race group. For instance, insulin resistance is
related to blood pressure in white but not in black Americans .
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Therefore, each component of metabolic syndrome may have a
different influence on pulmonary function across racial groups. In
an Italian study, HDL-C was the main predictor for pulmonary
function impairment . In a Japanese study, this relationship
between lung function impairment and metabolic syndrome was
thought to be due mainly to abdominal obesity and hyperglycemia
in males . In a Korean study, abdominal obesity, blood
pressure, HDL-C, and fasting plasma glucose strongly influenced
pulmonary function . In an Australian study, poorer pulmonary
function was also noted as metabolic syndrome components
accumulated . Our study, which was conducted in a U.S.
population, revealed that metabolic syndrome was associated with
impaired pulmonary function and that abdominal obesity, high
blood pressure, high triglycerides and low HDL-C were
significantly associated with decreasing FVC and FEV1 in both males
Our finding that increased abdominal obesity was significantly
associated with lung function impairment in both men and women
was consistent with previous studies [12,2224]. Abdominal
obesity is considered the core of the pathophysiology of metabolic
syndrome . The available data support a connection between
metabolic syndrome and impaired pulmonary function, mainly via
abdominal obesity. However, the identification of the definitive
pathway and the exact pathophysiological mechanism to explain
this association requires further evaluation. One potential
explanation is that increased abdominal obesity directly affects thoracic
and diaphragm compliance, which impairs lung function .
However, in a previous Japanese study, waist circumference was
only significantly associated with impaired lung function in men
. Moreover, in Korea, sex differences in the association
between waist circumference and pulmonary function were also
recognized. Given that various distributions of abdominal and
visceral fat accumulation were noted in different race populations
and genders , our viewpoint of the varying weight of each
component in different racial groups was confirmed. Another
possible explanation for impaired pulmonary function mediated
by abdominal obesity is that visceral fat may be a more specific
marker . Increased visceral fat was identified as the main
factor that increases CRP concentrations . In addition,
increased serum CRP was positively correlated with each
metabolic component and strongest with abdominal obesity
[11,30]. Serum CRP is also associated with impaired pulmonary
function . However, after considering CRP levels in our study,
the relationship between impaired lung function and abdominal
obesity was still evident.
Another important component, low HDL-C, was correlated
with impaired pulmonary function in our study. In agreement with
this observation, a study with 237 patients found that serum
HDLC had an inverse association with lower FEV1 and FVC . The
pathophysiology underlying this association remains unclear.
Lower HDL-C levels are associated with the development of
coronary heart disease because of the function of HDL-C in
reverse cholesterol transport and anti-inflammation. It is tempting
to speculate that the serum HDL-C level serves as a predictor for
the decline of lung function, mainly due to its pleiotropic
properties, including antioxidative function, inhibition of
cytokine-induced expression of endothelial cell adhesion molecules,
and suppression of the chemotactic activity of monocytes and
lymphocytes [32,33]. Klisic et al. also reported that significantly
higher hs-CRP levels correlated with lower HDL-C levels [34,35].
This observation implied that inflammation might be an early
event in the decline of pulmonary function in individuals with low
The current analysis has a few limitations. First, this study was a
cross-sectional survey that measured lung functions and metabolic
components at a single time rather than recording long-term
repeated observations. Although previous reports and biological
plausibility consistently suggest that metabolic syndrome is
associated with impaired lung capacity, a cross-sectional study
design tends to leave uncertainty regarding the temporal sequence
of exposureoutcome relations. Thus, confirming the relationship
between the two prospective longitudinal data (the relationship
between prior metabolic syndrome and incident impaired
pulmonary function) would be valuable. Second, our samples
were collected from 19881994. These samples may not
accurately reflect todays U.S. population. However, based on a
recent study of the prevalence of metabolic syndrome in the U.S.
, individuals with metabolic syndrome were still likely to be
older and non-Hispanic whites, which is similar to our sample. In
addition, the current most useful FEV1 percent predicted and
FEV percent predicted values were also calculated using the
NHANES III reference equations developed by Hankinson et al.
, which used a population similar to the one used in our study.
Therefore, our sample result is applicable to todays U.S.
Our findings highlight the notion that in the U.S., FVC and
FEV1 are inversely associated with the accumulation of metabolic
syndrome components and also independently associated with
each component of metabolic syndrome. Therefore, this
relationship might receive more attention and even urge action to be taken
on metabolic components in the context of poor pulmonary
function. The results of this study warrant the development and
investigation of comprehensive management strategies.
Conceived and designed the experiments: WLC TCP. Performed the
experiments: WLC CCW LWW TWK JYHC YHY YWC TCP YJC.
Analyzed the data: WLC CCW LWW TWK JYHC YHY YWC TCP
YJC. Contributed reagents/materials/analysis tools: WLC CCW LWW
TWK JYHC YHY YWC TCP YJC. Wrote the paper: WLC TCP.
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