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O2 max
Division of Gerontology, Department of Medicine, University of Maryland School of Medicine, and Geriatric Research Education and Clinical Center, Baltimore Veterans Affairs Medical Center, Baltimore, Maryland 21201
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ABSTRACT |
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The accumulation of
visceral fat is independently associated with an increased risk for
cardiovascular disease. The aim of this study was to determine whether
the loss of visceral adipose tissue area (VAT; computed tomography) is
related to improvements in maximal O2 uptake
(
O2 max) during a weight loss
(250-350 kcal/day deficit) and walking (3 days/wk, 30-40 min)
intervention. Forty obese [body fat 47 ± 1 (SE) %], sedentary
(
O2 max 19 ± 1 ml · kg
1 · min
1)
postmenopausal women (age 62 ± 1 yr) participated in the study. The intervention resulted in significant declines in body weight (
8%), total fat mass (dual-energy X-ray absorptiometry;
17%), VAT
(
17%), and subcutaneous adipose tissue area (
17%) with no change
in lean body mass (all P < 0.001). Women with an
average 10% increase in
O2 max reduced
VAT by an average of 20%, whereas those who did not increase
O2 max decreased VAT by only 10%,
despite comparable reductions in body fat, fat mass, and subcutaneous
adipose tissue area. The decrease in VAT was independently related to
the change in
O2 max
(r2 = 0.22; P < 0.01) and
fat mass (r2 = 0.08; P = 0.05). These data indicate that greater improvements in
O2 max with weight loss and walking are
associated with greater reductions in visceral adiposity in obese
postmenopausal women.
obesity; postmenopausal women; exercise; intra-abdominal fat; maximal oxygen uptake
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INTRODUCTION |
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THE ACCUMULATION OF FAT IN visceral depots, independent of total body obesity, is associated with the development of dyslipidemia, hypertension, glucose intolerance, and hyperinsulinemia in women (10, 13, 36). These metabolic abnormalities increase the risk for cardiovascular disease (19) and diabetes (25), which are the leading causes of death among older women (16, 31).
Several studies show that lifestyle interventions, including
hypocaloric dieting for weight loss (WL) and/or aerobic exercise training (AEx), reduce abdominal obesity and cardiovascular disease risk factors (4, 14, 33, 37). However, only a few studies use computed tomography (CT) or magnetic resonance imaging to document
whether these interventions preferentially decrease visceral adipose
tissue area (VAT). In the hypocaloric WL studies, there was a
preferential loss of VAT compared with abdominal subcutaneous adipose
tissue area (SAT) in premenopausal women (20, 39), postmenopausal women (32), and men (20, 27,
29). However, hypocaloric WL often reduced lean body mass (LBM)
(20, 32), which resulted in a decline in resting metabolic
rate (20). Other studies have shown that AEx training
blunts the loss of LBM (10, 30). The effects of AEx on the
preferential loss of VAT are variable and may be affected by the
magnitude of the improvement in maximal oxygen uptake
(
O2 max). Schwartz et al.
(30) showed a 25% reduction in VAT with a 22% increase in
O2 max during AEx in old men,
whereas a 17% decrease in VAT was associated with a 18% increase in
O2 max in young men. This
suggests that the reduction in VAT may be more pronounced with
greater improvements in
O2 max.
However, Despres et al. (9) reported an 11%
decrease in SAT and no change in VAT after an AEx program that
increased
O2 max by 15% in
premenopausal women. Thus, although AEx seems to reduce VAT and
preserve LBM in some studies, the best treatment for visceral and total
body obesity may be a combined program of hypocaloric WL and AEx.
The few studies that examined the effects of a combination of
hypocaloric WL and AEx showed that the loss of VAT and body weight was
similar to that observed with hypocaloric dieting alone and that LBM
was preserved (1, 28, 29). There are no studies examining
the effect of changes in
O2 max during
a hypocaloric WL and walking program on changes in VAT and SAT in
postmenopausal women. We hypothesized that postmenopausal women who
show the greatest improvement in
O2 max
during a 6-mo hypocaloric WL and walking intervention would lose the
most VAT.
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METHODS |
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Subject selection. All subjects were healthy, obese (body mass index >27 kg/m2) postmenopausal women (no menstruation for at least 1 yr, with follicle-stimulating hormone >30 IU/l). The women were sedentary (<20 min of AEx, 2 times/wk), weight stable (<2.0-kg weight change in past year), and had not smoked for at least 5 yr. None of the women was on estrogen or hormone replacement therapy in the previous year or medications affecting lipids, glucose metabolism, or blood pressure. All women provided informed consent to participate in the study according to the guidelines of the University of Maryland Institutional Review Board for Human Research.
Initial screening evaluations included a medical history, physical examination, fasting blood profile, 2-h oral glucose tolerance test, 12-lead resting electrocardiogram, and a treadmill exercise test according to the Bruce protocol (6a). Subjects with evidence of diabetes (2), hypertension (blood pressure >140/90 mmHg), hyperlipidemia (triglyceride >400 mg/dl), heart disease, liver disease, renal or hematologic disease, cancer, other medical disorders, or orthopedic limitations that would affect physical activity were excluded. Sixty-four women met the criteria and were enrolled in the study.Dietary control. Before beginning the intervention, the women completed an initial 7-day food record to provide information about their dietary habits. All women met weekly with a registered dietitian for 8-10 wk and were instructed in the principles of the American Heart Association Step 1 diet to establish dietary control before research testing. Subjects were weight stable (<0.50-kg weight change) on this diet for at least 2 wk before research testing. The dietitian monitored compliance by weekly review of 7-day food-exchange records and 24-h dietary recalls.
Research testing. Measurements of body composition and aerobic fitness were performed before and after a 6-mo WL and walking program. Waist-to-hip ratio was measured in duplicate and calculated as the ratio of the minimal waist circumference to the circumference at the maximal gluteal protuberance. A total body scan was performed using dual-energy X-ray absorptiometry (model DPX-L, Lunar Radiation, Madison, WI) to determine percent body fat, nonosseous LBM, and fat mass. A single-slice CT scan taken midway between L4 and L5 was performed using a GE Hi-Light CT scanner to measure VAT and SAT, as previously described (22).
O2 max was measured during a modified
Balke protocol (3a). Treadmill speed remained
constant at the speed that elicited 70% of heart rate maximum with 0%
grade. The elevation was increased by 2% every 2 min for the first 4 min and then by 2% every minute until maximal exhaustion. Oxygen
uptake (
O2), carbon dioxide production,
and minute ventilation were obtained every 20 s using a
Sensormedics metabolic measurement cart (model 2900, Yorba Linda, CA).
Heart rate was determined electrocardiographically throughout the
tests. Two of three criteria had to be met for achievement of
O2 max: 1) maximal heart
rate ± 10 beats/min of age-predicted maximal heart rate (heart
rate = 220
age), 2) respiratory exchange ratio
of at least 1.10, and 3) plateau in
O2 (<2.0
ml · kg
1 · min
1).
O2 max was calculated from the average
of the three highest 20-s collections.
Hypocaloric WL and walking intervention. During the 6-mo WL intervention, women met weekly with a registered dietitian for instruction in the principles of a hypocaloric diet (250-350 kcal/day deficit) that followed the American Heart Association Step 1 guidelines. The program focused on eating behavior, stress management, control of portion sizes, modification of binge eating, and other adverse habits. The dietitian monitored compliance by weekly review of 7-day food exchange records. In addition, women were instructed to walk 3 days/wk at a target heart rate of 50-60% of heart rate reserve for 30-45 min. The women walked 1 day/wk on a treadmill at our exercise facility under the supervision of an exercise physiologist, during which time heart rate was determined with a heart rate monitor, and they walked the other 2 days on their own. After the 6-mo intervention, the women continued the walking program but were weight stabilized (<0.5-kg change) on a eucaloric diet for a period of 2 wk before retesting.
Statistics.
Standardized residual plots and standardized residual vs.
predicted value plots for all variables were used to examine the assumption of independence. No violations of regression or ANOVA assumptions were identified, and all data analyses were completed using
SPSS for Windows. Analysis of covariance (ANCOVA) was used to adjust
O2 max for LBM at baseline and after
the intervention (34). Change values were defined as the
difference between the postintervention values and the baseline values,
and relative change (%) was calculated by expressing the change value
as a function of the baseline value. The absolute change in
O2 max was adjusted for baseline
O2 max using ANCOVA. Correlations between response variables and their respective baseline values were
determined using Pearson correlation analysis. Response variables that
significantly correlated with their baseline value were adjusted using
ANCOVA. One-way ANOVA was used to determine differences between
variables before and after intervention and to determine statistically
significant differences between women who improved
O2 max (highest 3 quartiles) and women
who did not improve
O2 max
(lowest quartile). Statistically significant relationships between
change in
O2 max and body composition
were determined using Pearson correlational analysis.
Multiple-regression analysis was used to determine independent
predictors of the change in VAT. Data are presented as means ± SE, and the level of significance was set at P < 0.05 for all analyses.
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RESULTS |
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Dropout rate and adherence to the walking intervention. We report data on the 40 women who completed the WL and walking intervention. Reasons for dropout included illness, relocation, personal reasons, and/or time constraints of participation. All women had follicle-stimulating hormone values >30 IU/l, and baseline physical characteristics of the 24 women who dropped out were not different from those of the 40 women who completed the study (data not shown). Exercise attendance to the supervised exercise session was 78% (range 36-100%), and average exercise intensity was 73% of the maximum predicted heart rate reserve.
Effects of the intervention
(Table 1). These obese (body mass
index = 31 ± 1 kg/m2) and sedentary
(
O2 max 19 ± 1 ml · kg
1 · min
1) women were
age 62 ± 1 yr and postmenopausal (12 ± 2 yr since last
menstrual period) at baseline. Body weight, percent body fat,
fat mass, waist circumference, hip circumference, VAT, and SAT
decreased significantly (P < 0.01) after the 6-mo
intervention. Because both waist and hip circumference decreased to the
same magnitude, the waist-to-hip ratio did not change. On average, nonosseous LBM did not change during the intervention, but there was a
wide range of individual changes (LBM
2.6-2.5 kg). Therefore, all analyses using
O2 max were
covaried for LBM.
O2 max increased an
average of 7%, expressed as liters per minute adjusted for LBM;
however, the response to the intervention was variable (range
6-20%).
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Effects of changes in
O2 max on
VAT.
VAT and SAT response to the intervention significantly correlated
with their respective baseline values. Thus VAT and SAT absolute
response variables were adjusted for the baseline value using ANCOVA.
To examine the effects of the change in
O2 max on the change in VAT, we divided
participants into quartiles on the basis of their absolute change in
O2 max covaried for the initial value
(Fig. 1). The 10 women in the quartile
with the smallest improvement in
O2 max
(
0.01 ± 0.01 l/min) were compared with the 30 women in the
upper three quartiles who showed a combined improvement in
O2 max of 10 ± 1% (0.15 ± 0.01 l/min; P < 0.001). Absolute and relative change
in body weight, percent body fat, total fat mass, and SAT did not
differ between groups. However, the absolute and relative change in VAT was significantly greater (P < 0.01 and
P < 0.02, respectively) in women who improved
O2 max (VAT =
31 ± 3 cm2;
20 ± 2%) compared with women who did not
improve
O2 max (VAT =
13 ± 4 cm2;
10 ± 3%) (Fig.
2).
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O2 max (r =
0.47;
P < 0.01 and r =
0.38; P < 0.02, respectively) but were not related to
changes in body weight (r = 0.22; P = not significant) or total fat mass (r = 0.29;
P = 0.08). In multiple-regression analysis with the
change in
O2 max and fat mass in the
analysis, both the change in
O2 max (r2 = 0.22; P < 0.01) and in fat mass
(r2 = 0.08; P = 0.05)
independently predicted the change in VAT (Fig. 3, A and B,
respectively). Furthermore, 30% of the variance in the decline in VAT
was explained by the change in
O2 max and fat mass. There was no relationship between change in
O2 max and change in other indexes of
obesity. Thus the relationship between change in VAT and
O2 max was independent of the magnitude
of total weight or fat lost.
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DISCUSSION |
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The results of this study show that a 6-mo WL and walking program
in obese postmenopausal women results in reductions in VAT that are
related to the magnitude of the increase in
O2 max. Women who had an average 10%
increase in
O2 max reduced VAT by an
average of 20%, whereas those who did not increase
O2 max decreased VAT by only 10%,
despite comparable reductions in fat mass. In addition, the combined
increase in
O2 max and the decrease in
fat mass explained 30% of the variance in the decrease of VAT with WL
and walking. This suggests that women who raise
O2 max the most during a WL and walking
program will lose the greatest amount of VAT.
Previous studies have not addressed the relationship between the change
in VAT and the change in
O2 max during
a WL and walking program, but our findings are in agreement with the
four studies that report data on the combined influence of WL and AEx
on VAT. Ross et al. showed significant reductions in VAT, SAT, and body
weight and increases in
O2 max during WL and AEx programs in obese women (28) and men
(29). In these studies, there was a 10- to 12-kg loss of
body weight in both men and women. Men decreased VAT by 39% and
improved
O2 max by 14%, and women
decreased VAT by 34% with an 8% increase in
O2 max. Although the difference in
response between groups is quite small, the group that lost the most
VAT had the greatest improvement in
O2 max. Two other studies showed a
reduction in VAT with hypocaloric WL and AEx, but neither study
measured
O2 max (1, 7).
Conway et al. (7) reported a 30 and 34% VAT reduction in
obese black and white women, respectively. Abe et al. (1)
reported a 38% reduction in VAT in young women instructed to exercise
one to two times per week.
A likely explanation for the association between the change in
O2 max and VAT is the role of
O2 max response as an indicator of
free-living physical activity. Broachu et al. (6) reported
a positive association between higher levels of peak
O2 and greater volitional and
nonvolitional (i.e., fidgeting) physical activity energy expenditure.
Thus free-living daily physical activity most likely contributed to the
increase in
O2 max measured during the
6-mo intervention in this population of obese sedentary women.
Furthermore, this increase in daily free-living activity also may
elevate catecholamine levels during activity for a long period of time,
which could affect regional fat cell metabolism and be one mechanism
for the decrease in VAT.
There are other potential mechanisms by which the improvement in
O2 max is associated with a greater
reduction in VAT. Several studies show that exercise training increases
circulating catecholamine levels (3) and in vitro
catecholamine-stimulated lipolysis in isolated adipocytes from SAT
(8, 22). Also, exercise blunts the reduction in lipolysis
of SAT typically seen with weight loss (24). In addition,
VAT is more lipolytically sensitive than SAT at rest (12, 21,
26), which may be due to the combined effects of greater
3-adrenergic receptor affinity and binding and a reduced
action of
2-adrenoceptor sensitivity (18,
35). Thus, because exercise stimulates lipolysis in
SAT, and VAT is more lipolytically active than SAT, lipolysis may be more pronounced in VAT with walking in those women who improve
O2 max the most. In addition, there is
a decline in circulating levels of insulin during acute exercise
(11), as well as after exercise training
(17). Therefore, the reduction of the antilipolytic action
of insulin on VAT (5) may also contribute to the effect of
walking on VAT area. Finally, in vivo studies show that the reesterification of free fatty acids by adipose tissue declines during
exercise (15, 38), and, therefore, free fatty acid mobilization from VAT may be increased in women who improved
O2 max with the walking program. Thus
the lower antilipolytic effect of insulin and increased free fatty acid
mobilization after walking, combined with a rise in catecholamines as a
result of regular physical activity, might explain, at least in part,
the larger reductions in VAT area observed in women who increased
O2 max by walking.
There are several limitations to this study that warrant comment. The
exercise sessions were supervised only 1 day/wk; hence, although
participants were instructed to exercise a total of 3 days/wk, we did
not accurately monitor compliance or intensity of exercise on the
nonsupervised days. Because of the varied degrees of compliance to
walking and variations in walking intensity among the women in this
study, there was a large interindividual variation in
O2 max response. This afforded us the
opportunity to test our hypothesis. However, to determine whether some
biological mechanism related to increases in
O2 max mediate the preferential loss of
VAT, it would be necessary to rigorously control the frequency,
intensity, and duration of exercise during the intervention period so
that all subjects performed similar amounts of work. Well-controlled
studies will need to be designed to determine the optimal dose of
exercise necessary to reduce upper body fat in obese postmenopausal
women. Another limitation of this study is that the results may only be
applicable to obese postmenopausal women. Finally, because the
relationship between the increase in
O2 max and the decrease in VAT is a
correlation, it does not prove cause and effect. We do not know whether
women lost more VAT because they improved
O2 max more or whether the greater loss
in VAT during WL and walking resulted in greater improvements in
O2 max.
The results of this study indicate that postmenopausal women who
manifest greater improvements in
O2 max during a 6-mo walking
and WL program show greater reductions in VAT, despite a similar
reduction in body weight, fat mass, and SAT. This has potential health
benefits for obese postmenopausal women because VAT is independently
correlated with Type 2 diabetes, hypertension, and hyperlipidemia,
which are major risk factors for cardiovascular disease in this
population (9, 13). Future studies will need to control
the frequency, intensity, and duration of the AEx program during WL to
determine the optimal exercise prescription needed to promote the
greatest health benefits.
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ACKNOWLEDGEMENTS |
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We appreciate the assistance of our dietitians, exercise physiologists, and nursing staff in the Division of Gerontology with the WL program, exercise supervision, and research testing. We especially thank all of the women who participated in this research study.
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FOOTNOTES |
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The study was supported by National Institutes on Aging Grants T32 AG-002109, R29 AG-14066, K01 AG-00685, and K07 AG-00608; National Institute of Nursing Research Grant R01 NR-03514; and the Department of Veterans Affairs Geriatric Research, Education, and Clinical Center (Baltimore, MD).
Address for reprint requests and other correspondence: N. A. Lynch, Baltimore Veterans Affairs Medical Center, VAMC/GRECC BT/18/GR, 10 N. Greene St., Baltimore MD 21201 (E-mail: nicole{at}grecc.umaryland.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 9 November 1999; accepted in final form 8 August 2000.
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