Background
The global prevalence of obesity has doubled during the past three decades [
1]. In 2015, approximately 39% of the world’s population was estimated to be overweight or have obesity [
2]. The condition has been shown to be a risk factor for various lung diseases, especially those associated with the deterioration of pulmonary function [
3]. Consequently, obesity poses a substantial health burden.
Previous studies have explored the longitudinal association between adiposity and lung function using assessment of bodyweight or body mass index (BMI) [
4‐
7]. Nevertheless, the single use of bodyweight or BMI as a measure of obesity can be misleading as weight or BMI are poor measures of adiposity, resulting in inconsistent conclusions [
8]. A few cross-sectional studies have investigated the relationship between lung function and body composition parameters, including body fat mass and its distribution, by employing bio-electrical impedance analysis (BIA) or dual-energy X-ray absorptiometry. Body fat distribution has a stronger association with lung function than bodyweight or BMI [
9,
10]. Further, the effects of body fat on different sites have shown comparable effects on respiratory function [
10,
11].
However, it remains unclear how long-term body composition changes are related to lung function impairment. Few studies have tried to elucidate this long-term association; however, several limitations were observed due to specific age ranges (young/old), small sample size, and measurements at only two timepoints (the beginning and end) [
12‐
14].
In this study, we examined the long-term association between adiposity and lung function changes using BIA in a large community-based cohort. Anthropometric and spirometry data were collected repeatedly during the follow-up period, and we categorized the study population according to changes in the fat mass index (FMI) and waist-to-hip ratio (WHR). To the best of our knowledge, this comprehensive study is the first to use the individual slope of adiposity changes to elucidate the association between adiposity and respiratory function in a middle-aged Asian population.
Discussion
In this study, we sought to determine the association between adiposity and lung function in the Asian general population. The cross-sectional analyses showed that higher adiposity was associated with lower lung function. During follow-up, an increase in the FMI was associated with a decline in FVC and FEV1 in both sexes, and an increased WHR was associated with a decline in FVC and FEV1 in men. Notably, participants in the WHR-increased group had a steeper decline in FVC and FEV1 than those in the WHR-decreased group, in both the fat-gain and fat-loss groups. Our findings suggest that changes in adiposity, especially central adiposity, strongly affect lung function in the middle-aged Asian general population.
Lung function impairment is associated with an increase in the incidence of chronic obstructive pulmonary disease [
26,
27], cerebrovascular disease [
28,
29], insulin resistance, diabetes [
30], and all-cause mortality [
31]. Obesity and being overweight are not only huge health burdens, but also affect lung function. Numerous cross-sectional studies [
10,
11,
32] and a few longitudinal studies [
12‐
14] have investigated the association between adiposity and lung function using BIA or dual-energy X-ray absorptiometry. However, previous studies have had some limitations, such as a small study population (47 women and 30 men) [
12], narrow age range (32–38 years) [
14], being limited to Western countries [
12‐
14], and most importantly, having only two measurements, at the beginning and end of the study period [
12‐
14]. In contrast to these studies, we grounded our analyses on a large-scale community-based cohort. More than 70% of the study population was followed up for 8 years, with ≥ 4 spirometry and anthropometric analyses. We used linear regression analysis to calculate the individual slopes of FMI and WHR changes. Through these comprehensive data analyses and linear mixed regression analyses, we demonstrated that increased adiposity was associated with decline in lung function. Moreover, this study excluded those with chronic lung diseases, such as chronic obstructive pulmonary disease or asthma. Therefore, our findings provide evident insights into the impact of central adiposity on lung function.
Central obesity is characterized by fat accumulation in the thorax, abdomen, and visceral organs. Fat deposition in the mediastinum and abdominal cavity reduces compliance of the respiratory system and changes the breathing pattern, resulting in a reduction in lung volumes, which is proportional to the severity of obesity [
3]. In fact, expiratory flow velocity is determined by the degree of previous lung inflation through the elasticity of the lungs [
33]. Therefore, decrease in lung volumes subsequently result in decrease in expiratory flow, which leads to a reduction in FEV
1. Fat deposition also causes narrowing, closure, and hyperresponsiveness of the airway, thereby leading to gas trapping and ventilation inhomogeneity [
3]. Accordingly, FMI and WHR were negatively associated with FVC and FEV
1 in men in this study. Lung function decline was more prominent in the WHR-increased group, especially in the fat-gain group. Although the mechanism underlying the relationship between obesity and airway hyperresponsiveness remains to be established, the adipose tissue in individuals with obesity is infiltrated with activated macrophages interacting with adipocytes to induce systemic inflammation. Changes in adipose-derived inflammatory cytokines such as tumor necrosis factor-α, leptin, and adiponectin have the capacity to promote airway hyperresponsiveness [
34].
In a study by Sutherland et al
., no longitudinal association was observed between body fat distribution and lung function in a 6-year follow-up in non-smoking, non-asthmatic young adults aged 32 and 38 years in New Zealand [
14]. However, in our study, participants in the WHR-increased group tended to have more severe lung function impairment than those in the WHR-decreased group, in both the fat-loss and fat-gain groups. The older age of the participants in our study (40–69 years) might contribute to the difference. Age-related decline in FEV
1 is estimated to be 25–30 mL/yr beginning at the age of 35–40 years, which increases to 60 mL/yr after the age of 70 years [
35]. The age-adjusted decrease in lung function was greater in the WHR-increased group than in the WHR-decreased group, in both the fat-gain and fat-loss groups, suggesting that central obesity might have a more significant effect on lung function in the middle-aged population.
Additionally, although previous studies have reported improvements in lung function after weight loss in patients with obesity [
36,
37], the fat-loss group with an increased WHR showed a more rapid lung function decline than those with a decreased WHR in this study. Therefore, our study clearly indicates that central obesity, not merely total adiposity, is the main driver for lung function impairment. Furthermore, in the South Korean general population, healthy never-smokers showed an FEV
1 decline of 31.8 mL/yr and 27.0 mL/yr in men and women, respectively [
38]. In comparison, the fat-gain group with an increased WHR showed the highest decline in FEV
1 in both men (56.1 mL/yr) and women (41.4 mL/yr) in this study.
We noted sex-associated differences in this study as well; the annual rate of lung function decline was more prominent in men than in women. Consistent with our findings, Fenger et al. [
13] and Sutherland et al. [
14] also observed that the rate of lung function decline was more pronounced in men. A greater decline in lung function in men may suggest that lung function decline is directly proportional to lung size, due to the differences in airway caliber between males and females [
13,
38].
According to our multiple linear mixed regression analysis (Table
2), FMI and WHR were both associated with lung function change in men, although FMI alone was associated with lung function change in women. Previous studies also have reported the different effects of fat and abdominal obesity on lung function decline between both sexes. The increase in waist circumference was related more prominently to FEV
1 decline in men than in women [
39]. In men, loss of fat mass over time was more closely associated with attenuated FEV
1 reduction than the change in muscle mass [
40]. Two possible mechanisms need to be considered. First, the mechanical effect of abdominal obesity affects differently to lung between the sexes. Abdominal and thoracic fat mass reduce the room for lung expansion, reducing vital capacity and limiting expiratory flow. As men have more abdominal fat than women when they have the same degree of adiposity, the mechanical aspect of central obesity in the respiratory system might be responsible for the sex-associated difference [
13,
41]. Second, gain of adipose tissue may accentuate inflammatory processes, which can damage the alveolus and airway.
Additionally, the heavy smoking history in men compared with that in women might have been another reason. Different thresholds for detrimental effects of pulmonary irritants are expected between sexes [
13]. Moreover, hormonal differences, mainly affected by menopause or hormonal replacement therapy, might have also contributed to the sex-associated difference [
42]. Further comprehensive studies are needed to elucidate the sex-associated difference in lung function decline.
A few limitations of this study should be considered. First, BIA might not be as accurate as dual-energy X-ray absorptiometry since the former is influenced by hydration status and body morphology [
43]. However, multiple studies have substantiated that the former is still a useful approach for assessing body composition with minimal errors in large epidemiological studies [
11,
14,
44]. Second, pre-bronchodilator spirometry measurements alone were performed. However, these spirometry data were obtained under strict quality control. Third, we did not consider physical activities, aerobic fitness, dietary patterns, or chronic medical conditions such as diabetes, hypothyroidism, sleep apnea, neurological diseases, and long-term corticosteroid use, which could be possible confounders. Fourth, we divided participants into only two (fat loss and fat gain) or three (WHR-decreased, -stable, and -increased) groups, which could oversimplify the intensity of adiposity change. Finally, the cross-sectional analyses between adiposity and lung function at baseline showed a small correlation coefficient (Figs.
2 and
3). However, these are unadjusted results, and the longitudinal analyses after adjustment supported the importance of central adiposity change.
In conclusion, our study demonstrated that increased adiposity, especially central obesity, was associated with long-term impairment of lung function. An increase in FMI was associated with a significant decline in FVC and FEV1 in both sexes, whereas it was positively related to FEV1/FVC in women. However, an increase in the WHR was inversely associated with a decrease in FVC and FEV1 in men only. Moreover, the WHR-increased group showed a faster decline in FVC and FEV1 in both the fat-loss and fat-gain groups, suggesting that central obesity markedly reduces respiratory function in the middle-aged Asian general population.
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