Fat Distribution and End Expiratory Lung Volume in Lean and Obese Men and Women

7/27/2019 Fat Distribution and End Expiratory Lung Volume in Lean and Obese Men and Women

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Fat Distribution and End-ExpiratoryLung Volume in Lean and Obese Menand Women*

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

Background: Although obesity significantly reduces end-expiratory lung volume (EELV), therelationship between EELV and detailed measures of fat distribution has not been studied inobese men and women. To investigate, EELV and chest wall fat distribution (ie, rib cage, anteriorsubcutaneous abdominal fat, posterior subcutaneous fat, and visceral fat) were measured in leanmen 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 MRIscans. Data were analyzed for the men and women separately by independent t test, and therelationships between variables were determined by regression analysis.Results: All body composition measurements were significantly different among the lean andobese men and women (p < 0.001). However, with only a few exceptions, fat distribution wassimilar among the lean and obese men and women (p> 0.05). The mean EELV was significantlylower 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 controlsubjects. 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 relatedto the cumulative effect of increased chest wall fat rather than to any specific regional chest wallfat distribution. Also, with only a few exceptions, relative fat distribution is markedly similar

between lean and obese subjects. (CHEST 2008; 134:704711)

Key words: abdominal fat; body composition; lung volumes; obesity; pulmonary function; visceral fat

Abbreviations: BMI body mass index; EELV end-expiratory lung volume; TLC total lung capacity; WHRwaist/hip ratio

In general, obesity decreases end-expiratory lungvolume (EELV),14 which is one of the earliest

and most prominent changes in pulmonary function

with obesity.2,5 However, the magnitude of the re-duction in lung function is not always directly pro-portional to the degree of obesity2,6 and appears tobe different in men and women, possibly due togender differences in fat distribution.68 For thesereasons, there has been an increased interest in theinfluence of fat distribution on lung function inobese men and women.

It has been suggested that lung function may bereduced more with central fat distribution (as indi-cated by a waist/hip ratio [WHR] of 0.95) thanwith overall body fatness (as indicated by body mass

index [BMI]).6,7,912 However, WHR provides only agross estimate of the body weight above and belowthe waist, and BMI is only an overall estimate of

body fatness. The specific effects of fat distributionon lung function in obese patients have not beenaddressed by actually measuring the percentage ofbody fat and/or fat distribution, especially the amountof fat distributed on the chest wall, which includes therib cage (ie, ribs and sternum), diaphragm, and ab-dominal contents displaced by the diaphragm (ie,subcutaneous abdominal fat and muscle, and visceralcontents including fat). In fact, relatively little isknown about the distribution of fat between lean andobese individuals.1316 Therefore, these potentiallyimportant relationships between fat distribution and

Original ResearchPULMONARY FUNCTION TESTING

704 Original Research

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lung function require further investigation with di-rect estimates of the percentage of body fat andchest wall fat distribution in otherwise healthy obeseadults. Furthermore, because of potential sexualdimorphisms in fat distribution, it is important toexamine these relationships in men and womenseparately.68

At rest, under static conditions, the EELV, likefunctional residual capacity, is dependent on thebalance of elastic forces of the lungs (ie, inwardrecoil) and chest wall (ie, outward recoil).17 Adiposetissue on the rib cage pushes in on the ribs, andsubsequently the lungs, while increased abdominalfat (ie, anterior subcutaneous abdominal fat and/orvisceral fat) pushes in and upward on the dia-phragm.1,18 Thus, the EELV, of all measures of lungfunction, is very sensitive to changes in the staticcompliance of the lungs and chest wall, and isspecifically altered by deposits of adipose tissue onthe chest wall.1921 This effect has also been demon-strated by simulated chest wall loading.22 The EELVis also significant because it represents the absolutelung volume at which we normally initiate a breath,and it has the potential to influence gas exchange,distribution of ventilation, work of breathing, airwayresistance, and expiratory flow limitation, especiallyduring exercise and in the supine body positionwhere many obese individuals experience difficultybreathing.2329 Thus, the EELV is a sensitive, accu-rate, and easily measured indicator with which toexamine the effects of chest wall fat distribution onlung function in contrast with other measures of lungfunction.30 However, it is currently unknownwhether fat distributed on the rib cage will causegreater changes in EELV than fat distributed on theabdomen (eg, subcutaneously or viscerally), and thisquestion cannot be addressed accurately until thepercentage of body fat and chest wall fat distributionare measured.

To investigate the effects of obesity and chest wallfat distribution on lung function, we measured thepercentage of body fat, resting EELV, chest wall fatdistribution (ie, rib cage or chest fat, and abdominalfat including anterior subcutaneous abdominal fat,posterior subcutaneous fat, and visceral fat) by MRIin lean and obese men and women. The unique andnovel aspects of this study were to measure the

percentage of body fat by hydrostatic weighing andto 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 subcutaneousabdominal fat in the women) would better predictthe change in EELV with obesity than overall per-centage of body fat.

Materials and Methods

Subjects

Nine lean men ( 25% body fat) and 10 obese men ( 30%body fat), and 11 lean women and 10 obese women wererecruited through local advertisements (ie, BMI ranges wereused for recruitment purposes, and the percentage of body fat

was confirmed after written consent was obtained). The lean andobese men also participated in another study,18which focused onthe effects of obesity on respiratory mechanics during exercise.The lean and obese women exclusively participated in thisprospective study to investigate fat distribution and lung function.Thus, the direct comparison of obese men and women was notdeemed appropriate. In accordance with the institutional reviewboard, all details of the study were discussed with the volunteers

and written informed consent was obtained. No subject had ahistory of asthma, cardiovascular disease, or musculoskeletalabnormalities, or had participated in regular vigorous exercise forthe last 6 months. All the subjects were nonsmokers. All qualifiedparticipants were instructed to avoid exercise, food, and caffeinefor at least 2 h prior to testing. All subjects underwent lungfunction measurements, hydrostatic weighing, and MRI. Pulmo-nary function tests, resting ECG, and body composition measure-ments were performed as an initial screening. MRI scans wereperformed on a separate day.

Pulmonary Function

All subjects underwent standard spirometry and lung volume

determinations (model 6200 body plethysmograph; SensorMed-ics; Yorba Linda, CA) according to the guidelines of the AmericanThoracic Society.31 Predicted values for spirometry and lung

volumes were based on the norms of Knudson and col-leagues,32,33 and Goldman and Becklake,34 respectively.

In the lean and obese men, EELV was measured with subjectsat rest while in the upright position and seated on a cycleergometer18 using a pneumotachograph system that has beendescribed previously.35 EELV was estimated from the measure-ment of inspiratory capacity while the subject was seated on thecycle, and total lung capacity (TLC) was measured with the bodyplethysmograph with the subject in the same seated position(EELV TLC inspiratory capacity) and was reported as apercentage of TLC ([EELV/TLC] 100).36 In the lean andobese women, EELV (percent of TLC) was measured by the

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

Canada.This research was supported by an American Lung AssociationCareer Investigator Award, AHA, TX Affiliate Grant, and theKing Charitable Foundation Trust.The authors have reported to the ACCP that no significantconflicts of interest exist with any companies/organizations whoseproducts or services may be discussed in this article.Manuscript received July 16, 2007; revision accepted April 22,2008.Reproduction of this article is prohibited without written permissionfrom the American College of Chest Physicians (www.chestjournal.org/misc/reprints.shtml).Correspondence to: Tony G. Babb, PhD, Institute for Exerciseand Environmental Medicine, 7232 Greenville Ave, Suite 435,Dallas, TX 75231; e-mail: [email protected]: 10.1378/chest.07-1728

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body plethysmograph with the subject in the upright posturebecause these subjects did not participate in any exercise studies.However, the method by which EELV is determined should nothave any effect on the measurement or the results. Also, we neverdirectly 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 circumfer-ences were also measured. Hydrostatic weighing was performedto 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), abdominalfat distribution (visceral and abdominal anterior subcutaneousfat), and posterior subcutaneous fat estimates were calculatedbased on analysis of the MRI scans.

MRI

MRI data were obtained in all volunteers using a whole-bodymagnet. A supine position with arms above the head wasmaintained 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 andIntera unit version 7.1.2 software ; Philips Medical Systems;Best, the Netherlands). For the assessment of fat in the uppertorso (chest), three axial images were obtained through the upperrib cage (one through the sternal notch, one through the xiphoidprocess, and one halfway between the two). For the assessmentof fat in the abdominal region of the torso, nine axial views wereobtained through the abdomen and pelvis (one at the xiphoidprocess, one at the T12 vertebra, one at each lumbar level, one atthe S1 vertebra, and one at the symphysis pubis).

Image Analysis

The images were manually analyzed with the use of specificsoftware (Scion Image, version 4.0.2; Scion Corporation;Frederick, MD) with which the adipose tissue was easily identi-fied. Abdominal area fat was estimated by evaluating the slicesobtained from the set of nine images obtained between thexiphoid process (roughly at the T10 vertebra) and the symphysispubis.16 Subcutaneous fat area was equal to the differencebetween the outer edge of the adipose tissue (skin) and the inner

visceral area (abdominal muscles and back muscles).37 Subcuta-neous fat was then divided, using a horizontal midline betweenthe inner abdominal wall and the spine, into anterior subcutane-ous abdominal fat and posterior subcutaneous fat. Visceral fat

area was equal to the sum of the individual fat deposit areasoutlined within the inner visceral area. Abdominal fat was equalto the sum of the visceral and anterior subcutaneous abdominalfat. Rib cage adipose tissue (ie, chest fat) was determined in asimilar manner, except that the fat mass was not divided intoinner and outer fat, or anterior and posterior fat. For each slice,areas were converted into volumes by multiplying the measuredarea by the slice thickness. Subcutaneous and visceral adiposetissue masses were calculated in kilograms for each 10-mm slice

by multiplying volumes by the estimated density of the adiposetissue (0.9196 kg/L). These procedures have been describedpreviously,15,3840 and the data were similar to those produced bycomparable MRI techniques.13,14,16

Data Analysis

Differences between lean and obese subjects were determinedby an independent t test, separately by gender (ie, the obese menand 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.

Results

Subjects

Subject characteristics are shown in Table 1. Allbody circumferences, ratios and BMIs were signifi-cantly different between the lean and obese subjectsfor both men and women (p 0.001). Both totalbody fat and lean body mass were significantlygreater (p 0.001) in the obese men compared withthe lean men (Fig 1, top, A). The same was true forthe lean and obese women (Fig 1, bottom, B).Among the men, all subjects were currently non-

smokers, while two of the lean men were ex-smokers(smoking history, 1.5 and 2.5 pack-years) and sixof the obese men were ex-smokers (mean [ SD]history of smoking, 6.78 7.41 pack-years). All ofthe women were never-smokers.

Pulmonary Function

Pulmonary function data are presented in Table 2.All subjects had normal spirometry findings com-

Table 1Subject Characteristics in Lean and Obese Men and Women*

CharacteristicsAge,yr

Height,cm

Weight,kg

BMI,kg/m2

Chest,cm

Waist,cm

Hip,cm WHR

Weight/HeightRatio

MenLean (n 9) 30 7 176 6 73 6 23 3 37 3 33 2 38 1 0.86 0.04 0.41 0.03Obese (n 10) 37 6 180 4 113 13 35 4 46 2 46 4 47 3 0.97 0.06 0.63 0.07p Value NS NS 0.0001 0.0001 0.0001 0.0001 0.0001 0.0002 0.0001

WomenLean (n 11) 30 6 165 5 58 4 21 1 34 1 27 1 37 1 0.73 0.03 0.35 0.02Obese (n 10) 33 5 166 8 102 14 37 2 44 1 42 4 50 3 0.84 0.06 0.61 0.05p Value NS NS 0.0001 0.0001 0.0001 0.0001 0.0001 0.0002 0.0001

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




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pared with predicted norms. Spirometry data werenot significantly different between the lean andobese men or women. In the men, EELV (ie,percentage of TLC measured on the cycle ergome-ter) was significantly lower in the obese men com-pared with the lean men (p 0.001). In the women,EELV (ie, percentage of TLC) was significantlylower in the obese women than in the lean women

(p 0.001).

Fat Distribution

Fat distribution was similar between the lean andobese men when reported as a percentage of total fatweight (Fig 2, top, A) despite a significantly greaterWHR in the obese men. However, the absoluteamount of fat (in kilograms) in each chest walllocation was significantly increased (p 0.05) in theobese men. Roughly 48% of body fat was distributedon the chest wall, while 52% was distributed periph-erally in the obese men (ie, arms, legs, and buttocks).

Abdominal fat (ie, the sum of anterior subcutaneousand visceral fat) accounted for 22 4% of mean fatweight in the obese men, of which 55% was distrib-uted subcutaneously.

The absolute amount of fat (in kilograms) in eachchest wall location was significantly increased(p 0.05) in the obese women compared with thelean women (Fig 2, bottom, B). However, the distri-bution of fat was remarkably similar between thelean and obese women with only a few, but statisti-cally significant, exceptions. The relative distribu-tions of rib cage fat (chest) and anterior subcut-

Figure 1. Top, A: body composition for lean and obese men.

Bottom, B: body composition for lean and obese women.

Table2PulmonaryF

unctioninLeanandObeseMenandWomen*

Characteristics

FVC,

L

(%predicted)

FEV

1,

L

(%predicted)

FEV

1/FVC

Ratio,%

PEF,

L/s

(%predicted)

MVV,

L/min

(%

predicted)

TLC,

L

(%predicted)

EELV,

%

TLC

RV/TLC

Ratio,

%

MenL

ean(n

9)

5.3

0.5

(105

10)

4.2

0.4

(100

5)

84

2

10.1

1.2

(107

11)

172

18(98

8)

6.6

0.8

(95

7)

46

4

20

2

Obese(n

10)

5.3

0.5

(102

10)

4.2

0.5

(96

10)

82

2

10.4

1.6

(108

15)

165

22(94

9)

6.8

0.5

(94

8)

39

6

21

6

pValue

NS(NS)

NS(NS)

NS

NS(NS)

NS(NS)

NS(NS)

0.0

055

NS

Women

Lean(n

11)

4.2

0.6

(113

14)

3.4

0.5

(108

13)

86

1

7.4

0.9

(111

13)

125

17(109

16)

5.5

0.7

(102

11)

53

4

24

2

Obese(n

10)

3.9

0.5

(108

10)

3.1

0.4

(100

11)

85

1

7.3

0.7

(111

12)

123

16(109

14)

5.0

0.5

(93

8)

40

4

21

4

pValue

NS(NS)

NS(NS)

NS

NS(NS)

NS(NS)

NS(0.0

5)

0.0

001

0.0

705

*Valuesaregivenasthemean

SD,unle

ssotherwiseindicated.

PEF

peakexpiratoryflow;MVV

measuredmaximalvoluntaryventilation;RV

residualvolume.See

Table1forabbreviationnot

usedinthetext.




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aneous abdominal fat were significantly greater(p 0.05) in the obese women; in turn, peripheralfat distribution was significantly lower comparedwith lean women (p 0.05). Thus, the obese womenhad 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 twogroups. However, visceral fat distribution was thesame in the lean and obese women. Abdominal fataccounted for approximately 21 2% of mean fat

weight in the obese women, of which only 24% wasvisceral. Thus, subcutaneous fat accounted for 60%of the chest wall fat in both groups of women.

Fat Distribution and EELVWhile all the correlation coefficients between

EELV and the fat distribution measures reported inTable 3 for the lean and obese men were significant(p 0.05), the correlation between visceral fat andEELV is shown in Figure 3, top, A. The correlationcoefficient between EELV and anterior subcutane-ous abdominal fat was the lowest of all the fatdistribution correlation coefficients. In subsequentstepwise regression analyses of EELV and all themeasures of fatness and fat distribution, the predic-

tive model was not significantly improved by theaddition of any other variable besides visceral fat.Note in Figure 3, top, A, that one of the obesesubjects had a visceral fat content that was similar tothat of the lean subjects. This man had undergonegastric bypass surgery, which may have influencedhis visceral fat content.

In the lean and obese women, all of the correlationcoefficients between EELV and the fat distributionmeasures reported in Table 3 were significant(p 0.0001). The relationship between EELV andanterior subcutaneous abdominal fat for both the

lean and obese women is shown in Figure 3, bottom,

Figure 2. Top, A: fat distribution for lean and obese men. Bottom,B: fat distribution for lean and obese women. Ant SubQ anteriorsubcutaneous abdominal fat; Post SubQ posterior subcutaneousfat; Peripheral total fat rib cage fat anterior subcutaneousabdominal fatvisceral fat posterior subcutaneous fat.

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

Variables Units

Men Women

Correlation Coefficients p Value Correlation Coefficients p Value

Wt kg 0.66 0.0022 0.77 0.0001Weight/height ratio 0.65 0.0024 0.82 0.0001Chest circumference cm 0.59 0.0078 0.85 0.0001Waist cm 0.68 0.0014 0.83 0.0001Hip cm 0.59 0.0081 0.79 0.0001

WHR ratio 0.59 0.0071 0.80 0.0001BMI kg/m2 0.63 0.0035 0.84 0.0001PBF % 0.56 0.0122 0.86 0.0001Total fat kg 0.61 0.0051 0.84 0.0001Rib cage kg 0.56 0.0116 0.85 0.0001Ant SubQ kg 0.49 0.0328 0.86 0.0001Visceral fat kg 0.70 0.0009 0.78 0.0001Abdominal kg 0.62 0.0047 0.86 0.0001Post SubQ kg 0.58 0.0096 0.76 0.0001Peripheral kg 0.58 0.0094 0.80 0.0001

*PBF percentage of body fat; Ant SubQ anterior subcutaneous abdominal fat; Abdominalvisceral fat plus anterior subcutaneousabdominal 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.




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B. In subsequent stepwise regression analyses of EELVand all of the measures of fatness and chest wall fatdistribution, the predictive model was not significantly

improved by the addition of any other variable besidesanterior subcutaneous abdominal fat.

Discussion

We have reported for the first time the associa-tions between direct measures of chest wall fatdistribution and measures of lung function in leanand obese men and women. We also have reportedthat the chest wall fat distribution was closely similarbetween lean and obese men and women, whichmeans that the increase in chest wall fat distribution

was proportional to the overall increase in obesity.Therefore, almost all measurements of overall obe-sity (eg, BMI and percentage of body fat) and allmeasures of regional obesity (eg, anterior subcuta-neous abdominal fat and visceral fat) were signifi-cantly associated with the decrease in EELV inobese men and women. Thus, the decrease in EELVappears to be related to the cumulative effect ofincreased chest wall fat rather than to any specificregional chest wall fat distribution (ie, visceral fat oranterior subcutaneous abdominal fat). This study alsoconfirmed earlier findings that while other measures of

lung function are changed little with class I and IIobesity, EELV is markedly reduced in otherwisehealthy obese men1,2,4,5,9,41 and women,1,2,4,5,9,41 whichcould predispose obese men or women to breathingconstraints during exercise, sleep, altitude exposure,and respiratory disease.23,24,42,43

Fat Distribution and EELVIn contrast to our hypothesis, the reduction in

EELV was significantly correlated with all measuresof body fatness and chest wall fat distribution, sincethere was no meaningful difference between the leanand obese men and women in relative overall fatdistribution (Table 3). These data suggest that it isthe cumulative effect of chest wall fat that decreasesEELV in obesity, supposedly by compressing the ribcage inward and abdomen upward. Prior studieswould suggest that the increased chest wall fatcontributes to lower transpulmonary end-expiratorypressures (less negative) and increased gastric end-expiratory pressures in obese men and women at restand during exercise compared with lean subjects.1,44

In other words, adipose tissue on the rib cage pushesin on the rib cage and lungs while abdominal weightpushes up on the diaphragm or opposes the down-ward motion of the contracted diaphragm.17 Thisagrees with findings that simulated anterior abdom-inal obesity results in significant decreases inEELV.22 Our data show that, in terms of absoluteweight, visceral, rib cage, and anterior subcutaneousabdominal fat were more than three times larger inthe obese men than in the lean men, which produceda significant decrease in EELV in the obese men.Most of the past studies2,711 addressing the relation-ship between obesity and lung function have focusedon spirometry variables and have used only BMI oranthropometric measurements to grade obesity;thus, they were not able to specifically address theeffect of chest wall fat distribution on lung function.Nonetheless, detailed measures of fat distribution donot appear to be terribly enlightening regardingchanges in lung function with obesity, at least in theobesity subjects employed in these studies.

Fat Distribution

These data on chest wall fat distribution suggestthat fat weight is added evenly, with only a fewexceptions, all over the body with obesity. This isdespite the finding that the obese men had a signif-icantly higher WHR, which is suggestive of a greaterrelative central fat distribution. Nevertheless, theobese men did have a greater absolute fat mass onthe rib cage and abdomen, with a large amount ofvisceral fat.

Figure 3. Top, A: EELV plotted against visceral fat for lean andobese men. Bottom, B: EELV plotted against visceral fat for leanand obese women.




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In the obese women, we found that visceral fatdistribution as a percentage of total fat weight wassimilar in the lean and obese women, despite the factthat absolute visceral fat was four times greater in theobese women (Fig 2, bottom, B). In contrast toconventional thinking, the obese women had largeabsolute amounts of chest wall fat, despite a WHRthat was well below 0.95 (Table 1). Furthermore,

anterior subcutaneous abdominal fat was more thanthree times greater than visceral fat. These datasuggest that absolute visceral fat is a relatively lowpercentage of chest wall fat in obese women, whileanterior subcutaneous abdominal fat, rib cage fat,and posterior subcutaneous fat were quite high inthese obese women, despite a WHR 0.95. Be-cause fat distribution was fairly similar between thelean and obese women we studied, almost anymeasure of overall obesity (eg, BMI and percentageof body fat) and/or almost any measurement of chestwall fat distribution (eg, anterior subcutaneous ab-

dominal fat and visceral fat) adequately representedthe magnitude of obesity. However, our subjectswere mostly mild-to-moderately obese with a limitedrange in WHR, and the associations could be differ-ent in a larger sample of obese subjects.

ACKNOWLEDGMENT: The authors wish to express theirappreciation to P.T. Weatherall, MD, Tommy Tillery, RT (R)(MR)(CT), Brian Fox, RT (R)(MR), and Jerri Payne, PA-C, of theRogers NMR Center at University of Texas Southwestern Med-ical Center; and Judy L. Barron and R. Michael Collins of theInstitute for Exercise and Environmental Medicine for theirassistance with this project. The authors also acknowledge theeditorial contributions of Helen E. Wood, PhD.

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Fat Distribution and End Expiratory Lung Volume in Lean and Obese Men and Women