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Original Research: PULMONARY FUNCTION TESTING |

Fat Distribution and End-Expiratory Lung Volume in Lean and Obese Men and Women FREE TO VIEW

Tony G. Babb, PhD; Brenda L. Wyrick, BSN; Darren S. DeLorey, PhD; Paul J. Chase, MEd; Mabel Y. Feng, MS
Author and Funding Information

*From the Institute for Exercise and Environmental Medicine (Dr. Babb, Ms. Wyrick, Mr. Chase, and Ms. Feng), University of Texas Southwestern Medical Center/Presbyterian Hospital of Dallas, Dallas, TX; and Faculty of Physical Education and Recreation (Dr. DeLorey), University of Alberta, Edmonton, AB, Canada.

Correspondence to: Tony G. Babb, PhD, Institute for Exercise and Environmental Medicine, 7232 Greenville Ave, Suite 435, Dallas, TX 75231; e-mail: TonyBabb@TexasHealth.org


This research was supported by an American Lung Association Career Investigator Award, AHA, TX Affiliate Grant, and the King Charitable Foundation Trust.

The authors have reported to the ACCP that no significant conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (www.chestjournal.org/misc/reprints.shtml).


Chest. 2008;134(4):704-711. doi:10.1378/chest.07-1728
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Background:  Although obesity significantly reduces end-expiratory lung volume (EELV), the relationship between EELV and detailed measures of fat distribution has not been studied in obese men and women. To investigate, EELV and chest wall fat distribution (ie, rib cage, anterior subcutaneous abdominal fat, posterior subcutaneous fat, and visceral fat) were measured in lean men and women (ie, < 25% body fat) and obese men and women (ie, > 30% body fat).

Methods:  All subjects underwent pulmonary function testing, hydrostatic weighing, and MRI scans. Data were analyzed for the men and women separately by independent t test, and the relationships between variables were determined by regression analysis.

Results:  All body composition measurements were significantly different among the lean and obese men and women (p < 0.001). However, with only a few exceptions, fat distribution was similar among the lean and obese men and women (p > 0.05). The mean EELV was significantly lower in the obese men (39 ± 6% vs 46 ± 4% total lung capacity [TLC], respectively; p < 0.0005) and women (40 ± 4% vs 53 ± 4% TLC, respectively; p < 0.0001) compared with lean control subjects. Many estimates of body fat were significantly correlated with EELV for both men and women.

Conclusions:  In both men and women, the decrease in EELV with obesity appears to be related to the cumulative effect of increased chest wall fat rather than to any specific regional chest wall fat distribution. Also, with only a few exceptions, relative fat distribution is markedly similar between lean and obese subjects.

Figures in this Article

In general, obesity decreases end-expiratory lung volume (EELV),14 which is one of the earliest and most prominent changes in pulmonary function with obesity.2,5 However, the magnitude of the reduction in lung function is not always directly proportional to the degree of obesity2,6 and appears to be different in men and women, possibly due to gender differences in fat distribution.68 For these reasons, there has been an increased interest in the influence of fat distribution on lung function in obese men and women.

It has been suggested that lung function may be reduced more with central fat distribution (as indicated by a waist/hip ratio [WHR] of > 0.95) than with overall body fatness (as indicated by body mass index [BMI]).6,7,912 However, WHR provides only a gross estimate of the body weight above and below the waist, and BMI is only an overall estimate of body fatness. The specific effects of fat distribution on lung function in obese patients have not been addressed by actually measuring the percentage of body fat and/or fat distribution, especially the amount of fat distributed on the chest wall, which includes the rib cage (ie, ribs and sternum), diaphragm, and abdominal contents displaced by the diaphragm (ie, subcutaneous abdominal fat and muscle, and visceral contents including fat). In fact, relatively little is known about the distribution of fat between lean and obese individuals.1316 Therefore, these potentially important relationships between fat distribution and lung function require further investigation with direct estimates of the percentage of body fat and chest wall fat distribution in otherwise healthy obese adults. Furthermore, because of potential sexual dimorphisms in fat distribution, it is important to examine these relationships in men and women separately.68

At rest, under static conditions, the EELV, like functional residual capacity, is dependent on the balance of elastic forces of the lungs (ie, inward recoil) and chest wall (ie, outward recoil).17 Adipose tissue on the rib cage pushes in on the ribs, and subsequently the lungs, while increased abdominal fat (ie, anterior subcutaneous abdominal fat and/or visceral fat) pushes in and upward on the diaphragm.1,18 Thus, the EELV, of all measures of lung function, is very sensitive to changes in the static compliance of the lungs and chest wall, and is specifically altered by deposits of adipose tissue on the chest wall.1921 This effect has also been demonstrated by simulated chest wall loading.22 The EELV is also significant because it represents the absolute lung volume at which we normally initiate a breath, and it has the potential to influence gas exchange, distribution of ventilation, work of breathing, airway resistance, and expiratory flow limitation, especially during exercise and in the supine body position where many obese individuals experience difficulty breathing.2329 Thus, the EELV is a sensitive, accurate, and easily measured indicator with which to examine the effects of chest wall fat distribution on lung function in contrast with other measures of lung function.30 However, it is currently unknown whether fat distributed on the rib cage will cause greater changes in EELV than fat distributed on the abdomen (eg, subcutaneously or viscerally), and this question cannot be addressed accurately until the percentage of body fat and chest wall fat distribution are measured.

To investigate the effects of obesity and chest wall fat distribution on lung function, we measured the percentage of body fat, resting EELV, chest wall fat distribution (ie, rib cage or chest fat, and abdominal fat including anterior subcutaneous abdominal fat, posterior subcutaneous fat, and visceral fat) by MRI in lean and obese men and women. The unique and novel aspects of this study were to measure the percentage of body fat by hydrostatic weighing and to estimate the distribution of fat on the chest wall (ie, rib cage and abdomen) via multiple MRI slices. We hypothesized that abdominal fat distribution (ie, visceral fat in the men7 and anterior subcutaneous abdominal fat in the women) would better predict the change in EELV with obesity than overall percentage of body fat.

Subjects

Nine lean men (< 25% body fat) and 10 obese men (> 30% body fat), and 11 lean women and 10 obese women were recruited through local advertisements (ie, BMI ranges were used for recruitment purposes, and the percentage of body fat was confirmed after written consent was obtained). The lean and obese men also participated in another study,18 which focused on the effects of obesity on respiratory mechanics during exercise. The lean and obese women exclusively participated in this prospective study to investigate fat distribution and lung function. Thus, the direct comparison of obese men and women was not deemed appropriate. In accordance with the institutional review board, all details of the study were discussed with the volunteers and written informed consent was obtained. No subject had a history of asthma, cardiovascular disease, or musculoskeletal abnormalities, or had participated in regular vigorous exercise for the last 6 months. All the subjects were nonsmokers. All qualified participants were instructed to avoid exercise, food, and caffeine for at least 2 h prior to testing. All subjects underwent lung function measurements, hydrostatic weighing, and MRI. Pulmonary function tests, resting ECG, and body composition measurements were performed as an initial screening. MRI scans were performed on a separate day.

Pulmonary Function

All subjects underwent standard spirometry and lung volume determinations (model 6200 body plethysmograph; SensorMedics; Yorba Linda, CA) according to the guidelines of the American Thoracic Society.31 Predicted values for spirometry and lung volumes were based on the norms of Knudson and colleagues,32,33 and Goldman and Becklake,34 respectively.

In the lean and obese men, EELV was measured with subjects at rest while in the upright position and seated on a cycle ergometer18 using a pneumotachograph system that has been described previously.35 EELV was estimated from the measurement of inspiratory capacity while the subject was seated on the cycle, and total lung capacity (TLC) was measured with the body plethysmograph with the subject in the same seated position (EELV = TLC − inspiratory capacity) and was reported as a percentage of TLC ([EELV/TLC] × 100).36 In the lean and obese women, EELV (percent of TLC) was measured by the body plethysmograph with the subject in the upright posture because these subjects did not participate in any exercise studies. However, the method by which EELV is determined should not have any effect on the measurement or the results. Also, we never directly compared the men and women in regard to EELV.

Body Composition

Standard measures of height and weight were made at the initial screening of the subjects. Waist, hip, and chest circumferences were also measured. Hydrostatic weighing was performed to determine the percentage of body fat, fat mass (ie, body weight × percentage of body fat/100), and lean body mass (ie, body weight − fat mass). Rib cage fat (ie, chest fat), abdominal fat distribution (visceral and abdominal anterior subcutaneous fat), and posterior subcutaneous fat estimates were calculated based on analysis of the MRI scans.

MRI

MRI data were obtained in all volunteers using a whole-body magnet. A supine position with arms above the head was maintained throughout the examination. All images (10-mm slice thickness) were acquired using quadrature body coil (antennae) 1.5-T magnet systems (ACS-NT unit [version 6.1.2 software] and Intera unit [version 7.1.2 software]; Philips Medical Systems; Best, the Netherlands). For the assessment of fat in the upper torso (chest), three axial images were obtained through the upper rib cage (one through the sternal notch, one through the xiphoid process, and one halfway between the two). For the assessment of fat in the abdominal region of the torso, nine axial views were obtained through the abdomen and pelvis (one at the xiphoid process, one at the T12 vertebra, one at each lumbar level, one at the S1 vertebra, and one at the symphysis pubis).

Image Analysis

The images were manually analyzed with the use of specific software (Scion Image, version β 4.0.2; Scion Corporation; Frederick, MD) with which the adipose tissue was easily identified. Abdominal area fat was estimated by evaluating the slices obtained from the set of nine images obtained between the xiphoid process (roughly at the T10 vertebra) and the symphysis pubis.16 Subcutaneous fat area was equal to the difference between the outer edge of the adipose tissue (skin) and the inner visceral area (abdominal muscles and back muscles).37 Subcutaneous fat was then divided, using a horizontal midline between the inner abdominal wall and the spine, into anterior subcutaneous abdominal fat and posterior subcutaneous fat. Visceral fat area was equal to the sum of the individual fat deposit areas outlined within the inner visceral area. Abdominal fat was equal to the sum of the visceral and anterior subcutaneous abdominal fat. Rib cage adipose tissue (ie, chest fat) was determined in a similar manner, except that the fat mass was not divided into inner and outer fat, or anterior and posterior fat. For each slice, areas were converted into volumes by multiplying the measured area by the slice thickness. Subcutaneous and visceral adipose tissue masses were calculated in kilograms for each 10-mm slice by multiplying volumes by the estimated density of the adipose tissue (0.9196 kg/L). These procedures have been described previously,15,3840 and the data were similar to those produced by comparable MRI techniques.13,14,16

Data Analysis

Differences between lean and obese subjects were determined by an independent t test, separately by gender (ie, the obese men and women were not directly compared). Relationships among variables were determined with Pearson correlation coefficients. A p value of ≤ 0.05 was considered to be significant.

Subjects

Subject characteristics are shown in Table 1. All body circumferences, ratios and BMIs were significantly different between the lean and obese subjects for both men and women (p < 0.001). Both total body fat and lean body mass were significantly greater (p < 0.001) in the obese men compared with the lean men (Fig 1, top, A). The same was true for the lean and obese women (Fig 1, bottom, B). Among the men, all subjects were currently nonsmokers, while two of the lean men were ex-smokers (smoking history, 1.5 and 2.5 pack-years) and six of the obese men were ex-smokers (mean [± SD] history of smoking, 6.78 ± 7.41 pack-years). All of the women were never-smokers.

Table Graphic Jump Location
Table 1 Subject Characteristics in Lean and Obese Men and Women*

*Values are given as the mean ± SD, unless otherwise indicated. NS = nonsignificant.

Figure Jump LinkFigure 1 Top, A: body composition for lean and obese men. Bottom, B: body composition for lean and obese womenGrahic Jump Location
Pulmonary Function

Pulmonary function data are presented in Table 2. All subjects had normal spirometry findings compared with predicted norms. Spirometry data were not significantly different between the lean and obese men or women. In the men, EELV (ie, percentage of TLC measured on the cycle ergometer) was significantly lower in the obese men compared with the lean men (p < 0.001). In the women, EELV (ie, percentage of TLC) was significantly lower in the obese women than in the lean women (p < 0.001).

Table Graphic Jump Location
Table 2 Pulmonary Function in Lean and Obese Men and Women*

*Values are given as the mean ± SD, unless otherwise indicated. PEF = peak expiratory flow; MVV = measured maximal voluntary ventilation; RV = residual volume. See Table 1 for abbreviation not used in the text.

Fat Distribution

Fat distribution was similar between the lean and obese men when reported as a percentage of total fat weight (Fig 2, top, A) despite a significantly greater WHR in the obese men. However, the absolute amount of fat (in kilograms) in each chest wall location was significantly increased (p < 0.05) in the obese men. Roughly 48% of body fat was distributed on the chest wall, while 52% was distributed peripherally in the obese men (ie, arms, legs, and buttocks). Abdominal fat (ie, the sum of anterior subcutaneous and visceral fat) accounted for 22 ± 4% of mean fat weight in the obese men, of which 55% was distributed subcutaneously.

Figure Jump LinkFigure 2 Top, A: fat distribution for lean and obese men. Bottom, B: fat distribution for lean and obese women. Ant SubQ = anterior subcutaneous abdominal fat; Post SubQ = posterior subcutaneous fat; Peripheral = total fat − rib cage fat − anterior subcutaneous abdominal fat − visceral fat − posterior subcutaneous fatGrahic Jump Location

The absolute amount of fat (in kilograms) in each chest wall location was significantly increased (p < 0.05) in the obese women compared with the lean women (Fig 2, bottom, B). However, the distribution of fat was remarkably similar between the lean and obese women with only a few, but statistically significant, exceptions. The relative distributions of rib cage fat (chest) and anterior subcutaneous abdominal fat were significantly greater (p < 0.05) in the obese women; in turn, peripheral fat distribution was significantly lower compared with lean women (p < 0.05). Thus, the obese women had relatively more fat on the chest wall than the lean women (52% vs 46% of fat weight, respectively), which is in agreement with the WHRs for the two groups. However, visceral fat distribution was the same in the lean and obese women. Abdominal fat accounted for approximately 21 ± 2% of mean fat weight in the obese women, of which only 24% was visceral. Thus, subcutaneous fat accounted for > 60% of the chest wall fat in both groups of women.

Fat Distribution and EELV

While all the correlation coefficients between EELV and the fat distribution measures reported in Table 3 for the lean and obese men were significant (p < 0.05), the correlation between visceral fat and EELV is shown in Figure 3, top, A. The correlation coefficient between EELV and anterior subcutaneous abdominal fat was the lowest of all the fat distribution correlation coefficients. In subsequent stepwise regression analyses of EELV and all the measures of fatness and fat distribution, the predictive model was not significantly improved by the addition of any other variable besides visceral fat. Note in Figure 3, top, A, that one of the obese subjects had a visceral fat content that was similar to that of the lean subjects. This man had undergone gastric bypass surgery, which may have influenced his visceral fat content.

Table Graphic Jump Location
Table 3 Correlation Coefficients Between End-Expiratory Lung Volume (Percentage of TLC) and Measures of Body Composition and Fat Distribution in Lean and Obese Men and Women*

*PBF = percentage of body fat; Ant SubQ = anterior subcutaneous abdominal fat; Abdominal = visceral fat plus anterior subcutaneous abdominal fat; Post SubQ = posterior subcutaneous fat; Peripheral = total fat less the sum of rib cage, Ant SubQ, and Post SubQ fat.

†Lean men, n = 9; obese men, n = 10.

‡Lean women, n = 11; obese women, n = 10.

Figure Jump LinkFigure 3 Top, A: EELV plotted against visceral fat for lean and obese men. Bottom, B: EELV plotted against visceral fat for lean and obese womenGrahic Jump Location

In the lean and obese women, all of the correlation coefficients between EELV and the fat distribution measures reported in Table 3 were significant (p < 0.0001). The relationship between EELV and anterior subcutaneous abdominal fat for both the lean and obese women is shown in Figure 3, bottom, B. In subsequent stepwise regression analyses of EELV and all of the measures of fatness and chest wall fat distribution, the predictive model was not significantly improved by the addition of any other variable besides anterior subcutaneous abdominal fat.

We have reported for the first time the associations between direct measures of chest wall fat distribution and measures of lung function in lean and obese men and women. We also have reported that the chest wall fat distribution was closely similar between lean and obese men and women, which means that the increase in chest wall fat distribution was proportional to the overall increase in obesity. Therefore, almost all measurements of overall obesity (eg, BMI and percentage of body fat) and all measures of regional obesity (eg, anterior subcutaneous abdominal fat and visceral fat) were significantly associated with the decrease in EELV in obese men and women. Thus, the decrease in EELV appears to be related to the cumulative effect of increased chest wall fat rather than to any specific regional chest wall fat distribution (ie, visceral fat or anterior subcutaneous abdominal fat). This study also confirmed earlier findings that while other measures of lung function are changed little with class I and II obesity, EELV is markedly reduced in otherwise healthy obese men1,2,4,5,9,41 and women,1,2,4,5,9,41 which could predispose obese men or women to breathing constraints during exercise, sleep, altitude exposure, and respiratory disease.23,24,42,43

Fat Distribution and EELV

In contrast to our hypothesis, the reduction in EELV was significantly correlated with all measures of body fatness and chest wall fat distribution, since there was no meaningful difference between the lean and obese men and women in relative overall fat distribution (Table 3). These data suggest that it is the cumulative effect of chest wall fat that decreases EELV in obesity, supposedly by compressing the rib cage inward and abdomen upward. Prior studies would suggest that the increased chest wall fat contributes to lower transpulmonary end-expiratory pressures (less negative) and increased gastric end-expiratory pressures in obese men and women at rest and during exercise compared with lean subjects.1,44 In other words, adipose tissue on the rib cage pushes in on the rib cage and lungs while abdominal weight pushes up on the diaphragm or opposes the downward motion of the contracted diaphragm.17 This agrees with findings that simulated anterior abdominal obesity results in significant decreases in EELV.22 Our data show that, in terms of absolute weight, visceral, rib cage, and anterior subcutaneous abdominal fat were more than three times larger in the obese men than in the lean men, which produced a significant decrease in EELV in the obese men. Most of the past studies2,711 addressing the relationship between obesity and lung function have focused on spirometry variables and have used only BMI or anthropometric measurements to grade obesity; thus, they were not able to specifically address the effect of chest wall fat distribution on lung function. Nonetheless, detailed measures of fat distribution do not appear to be terribly enlightening regarding changes in lung function with obesity, at least in the obesity subjects employed in these studies.

Fat Distribution

These data on chest wall fat distribution suggest that fat weight is added evenly, with only a few exceptions, all over the body with obesity. This is despite the finding that the obese men had a significantly higher WHR, which is suggestive of a greater relative central fat distribution. Nevertheless, the obese men did have a greater absolute fat mass on the rib cage and abdomen, with a large amount of visceral fat.

In the obese women, we found that visceral fat distribution as a percentage of total fat weight was similar in the lean and obese women, despite the fact that absolute visceral fat was four times greater in the obese women (Fig 2, bottom, B). In contrast to conventional thinking, the obese women had large absolute amounts of chest wall fat, despite a WHR that was well below 0.95 (Table 1). Furthermore, anterior subcutaneous abdominal fat was more than three times greater than visceral fat. These data suggest that absolute visceral fat is a relatively low percentage of chest wall fat in obese women, while anterior subcutaneous abdominal fat, rib cage fat, and posterior subcutaneous fat were quite high in these obese women, despite a WHR < 0.95. Because fat distribution was fairly similar between the lean and obese women we studied, almost any measure of overall obesity (eg, BMI and percentage of body fat) and/or almost any measurement of chest wall fat distribution (eg, anterior subcutaneous abdominal fat and visceral fat) adequately represented the magnitude of obesity. However, our subjects were mostly mild-to-moderately obese with a limited range in WHR, and the associations could be different in a larger sample of obese subjects.

BMI

body mass index

EELV

end-expiratory lung volume

TLC

total lung capacity

WHR

waist/hip ratio

The authors wish to express their appreciation to P.T. Weatherall, MD, Tommy Tillery, RT (R) (MR)(CT), Brian Fox, RT (R)(MR), and Jerri Payne, PA-C, of the Rogers NMR Center at University of Texas Southwestern Medical Center; and Judy L. Barron and R. Michael Collins of the Institute for Exercise and Environmental Medicine for their assistance with this project. The authors also acknowledge the editorial contributions of Helen E. Wood, PhD.

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Figures

Figure Jump LinkFigure 1 Top, A: body composition for lean and obese men. Bottom, B: body composition for lean and obese womenGrahic Jump Location
Figure Jump LinkFigure 2 Top, A: fat distribution for lean and obese men. Bottom, B: fat distribution for lean and obese women. Ant SubQ = anterior subcutaneous abdominal fat; Post SubQ = posterior subcutaneous fat; Peripheral = total fat − rib cage fat − anterior subcutaneous abdominal fat − visceral fat − posterior subcutaneous fatGrahic Jump Location
Figure Jump LinkFigure 3 Top, A: EELV plotted against visceral fat for lean and obese men. Bottom, B: EELV plotted against visceral fat for lean and obese womenGrahic Jump Location

Tables

Table Graphic Jump Location
Table 1 Subject Characteristics in Lean and Obese Men and Women*

*Values are given as the mean ± SD, unless otherwise indicated. NS = nonsignificant.

Table Graphic Jump Location
Table 2 Pulmonary Function in Lean and Obese Men and Women*

*Values are given as the mean ± SD, unless otherwise indicated. PEF = peak expiratory flow; MVV = measured maximal voluntary ventilation; RV = residual volume. See Table 1 for abbreviation not used in the text.

Table Graphic Jump Location
Table 3 Correlation Coefficients Between End-Expiratory Lung Volume (Percentage of TLC) and Measures of Body Composition and Fat Distribution in Lean and Obese Men and Women*

*PBF = percentage of body fat; Ant SubQ = anterior subcutaneous abdominal fat; Abdominal = visceral fat plus anterior subcutaneous abdominal fat; Post SubQ = posterior subcutaneous fat; Peripheral = total fat less the sum of rib cage, Ant SubQ, and Post SubQ fat.

†Lean men, n = 9; obese men, n = 10.

‡Lean women, n = 11; obese women, n = 10.

References

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