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Journal of Clinical Endocrinology & Metabolism, doi:10.1210/jc.2006-2113
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The Journal of Clinical Endocrinology & Metabolism Vol. 92, No. 3 880-886
Copyright © 2007 by The Endocrine Society

Reduction in Midthigh Low-Density Muscle with Aerobic Exercise Training and Weight Loss Impacts Glucose Tolerance in Older Men

Steven J. Prior, Lyndon J. Joseph, Josef Brandauer, Leslie I. Katzel, James M. Hagberg and Alice S. Ryan

Division of Gerontology, University of Maryland School of Medicine and Baltimore Geriatric Research, Education and Clinical Center (S.J.P., L.J.J., L.I.K., J.M.H., A.S.R.), Veterans Administration Maryland Health Care System, Baltimore, Maryland; and Department of Kinesiology (S.J.P., J.B., J.M.H.), University of Maryland, College Park, Maryland

Address all correspondence and requests for reprints to: Steven J. Prior, Ph.D., Baltimore Veterans Administration Medical Center, Geriatrics (18), Room 4B-205, 10 North Greene Street, Baltimore, Maryland 21201. E-mail: sprior{at}grecc.umaryland.edu.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: Intramuscular lipid content increases with aging and obesity and is directly related to impaired glucose tolerance and insulin resistance.

Objective: Our purpose was to determine the effects of aerobic exercise training (AEX) with and without weight loss (WL) on midthigh low-density muscle (LDM; a measure of im lipid) and whether changes in LDM impact glucose tolerance in sedentary older men.

Design: Forty-six men (60.4 ± 1.1 yr) completed 6 months of AEX (n = 34) or AEX + WL (n = 12) and had oral glucose tolerance tests (OGTTs) and computed tomography measures of LDM and regional abdominal and thigh fat depot areas.

Results: At baseline, LDM area directly correlated with fasting plasma glucose (FPG), 120-min glucose (G120), and glucose area under the curve (GAUC) during an OGTT (r = 0.44, r = 0.51, and r = 0.54, respectively, P < 0.01). After the interventions, the AEX + WL group had greater decreases in LDM (–13.5 vs. +1.3%, respectively), FPG (–8.3 vs. +2.1%, respectively), G120 (–22.5 vs. –3.6%, respectively), and GAUC (–17.3 vs. – 3.1%, respectively) than the AEX group. In the entire sample, the decreases in LDM correlated with reductions in FPG, G120, and GAUC during an OGTT (r = 0.31, r = 0.34, and r = 0.41, P < 0.05). Changes in other regional fat depots did not independently correlate with glucose tolerance or insulin responses.

Conclusion: AEX + WL is more efficacious than AEX for reducing LDM and glucose tolerance. The improvement in glucose tolerance may be partially mediated by decreases in LDM in older men.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
AGING IS ASSOCIATED with an increased risk of developing impaired glucose tolerance (1), but evidence suggests that age-related decreases in physical activity and increases in obesity may be underlying insulin resistance (IR) and impaired glucose tolerance. Physical inactivity and obesity may promote the accumulation of lipid in skeletal muscle in older individuals because im lipid increases with aging in sedentary individuals (2, 3) and is higher in obese individuals than in lean individuals (4, 5, 6). This accumulation of im lipid is considered a key metabolic abnormality in the pathogenesis of IR (7). The technique of computed tomography (CT) is used to quantify im lipid by determining muscle attenuation [expressed as mean attenuation or low-density muscle (LDM) vs. normal-density muscle (NDM)] (8). These measures correlate well with measures of im lipid obtained from muscle biopsies (9) and are used as surrogates for im lipid.

Aerobic exercise training with weight loss (AEX + WL) improves insulin sensitivity (10), glucose disposal (11), and glucose tolerance (10, 12), and one potential mechanism is through the reduction of im lipid. The depletion of im lipid reduces IR in obese individuals (13), so strategies to reduce im lipid such as WL and AEX may reduce IR observed in older individuals, improve glucose tolerance, and prevent the development of type 2 diabetes. AEX alone does not appear to decrease im lipid (6, 14), and the effect of AEX may be paradoxical because highly trained athletes exhibit high levels of im lipid similar to individuals with type 2 diabetes (15). WL alone seems to decrease im lipid in older women (16), but results are mixed in younger men and women (17, 18, 19, 20). When AEX and WL are combined, there are no effects on im lipid in young to middle-aged men and women (~25–50 yr old) (17, 18, 19), but a reduction occurs in older women (50–70 yr old) (16, 21). Either an AEX or a WL intervention alone is sufficient to improve the insulin response to an oral glucose tolerance test (OGTT), but the combination of AEX + WL appears necessary to improve the glucose response (10, 12). In the present study, we hypothesized that AEX + WL would decrease im lipid (measured as midthigh LDM) in sedentary older men and improve fasting plasma glucose (FPG) and glucose tolerance to a greater extent than AEX alone. We analyzed CT scans from previous aerobic exercise and WL studies (22, 23) to compare the effects of 6 months of AEX and AEX + WL on LDM and glucose and insulin responses to an OGTT in sedentary older men.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

Subjects were initially recruited to participate in studies examining the effects of gene polymorphisms on metabolic responses to aerobic exercise and WL. Subjects were required to: 1) be sedentary (exercise less than 20 min, 2x/wk for at least 6 months), 2) be 50–75 yr of age, 3) not be taking lipid- or glucose-lowering medication, 4) have no recent history of smoking tobacco, 5) have no previous diagnosis of diabetes mellitus or cardiovascular disease, and 6) not have any other medical condition that would preclude aerobic exercise. A total of 63 men enrolled in these studies and participated in body composition and metabolic testing. Forty-six subjects completed the 6-month intervention: 34 subjects in the AEX group and 12 subjects in the AEX + WL group. The research protocols were approved by the Institutional Review Boards at the University of Maryland College Park and the University of Maryland School of Medicine. All subjects provided written informed consent.

Measures of body composition

CT (General Electric Hi-Light Scanner, Fairfield, CT) was used to measure the midthigh cross-sectional areas of low-density lean muscle, sc fat, and NDM in each limb as previously described (2). Briefly, LDM and NDM were defined as the cross-sectional area of midthigh tissue with Hounsfield units of 0–29 and 30–80, respectively. CT was also used to measure the cross-sectional areas of intraabdominal fat (IAF) and SAF at L4–L5. Dual-energy x-ray absorptiometry (DPX-IQ, LUNAR Radiation Corp., Madison, WI) was used to measure whole-body fat mass and percent body fat.

Maximal oxygen consumption (VO2max)

Subjects underwent a graded exercise test on a treadmill to determine VO2max. Briefly, speed was kept constant while the grade was increased 2% every 1–2 min until the subject was unable to continue. Attainment of true VO2max was determined by standard physiological criteria [i.e. respiratory exchange ratio at maximal exercise > 1.10 and/or a plateau in VO2 (<200 ml/min change in the VO2)] with an increase in workload.

OGTT

Subjects underwent a 2-h OGTT after a 12-h overnight fast. Subjects were weight stable on the American Heart Association (AHA) Step I diet and consumed more than 250 g carbohydrates/d for 3 d before the OGTT. Dietary records were examined to ensure adequate carbohydrate intake. A catheter was placed in an antecubital vein, and blood samples were drawn before and 30, 60, 90, and 120 min after the ingestion of a 75-gram glucose solution for measurement of plasma glucose and insulin. Blood samples were centrifuged, and plasma was separated and stored at –80 C until samples from before and after the intervention could be analyzed in the same assay. Plasma glucose levels were analyzed with a glucose analyzer (2300 STAT Plus, YSI, Yellow Springs, OH). Plasma insulin levels were determined by RIA (Linco Research, St. Charles, MO). Glucose and insulin total area under the curve (GAUC and IAUC, respectively) were calculated using the trapezoidal method. The insulin sensitivity index was calculated using the method of Matsuda and DeFronzo (ISIM) (24), and the homeostasis model assessment for IR (HOMA-IR) and the homeostasis model assessment for ß-cell function (HOMA-B) were calculated as described by Matthews et al. (25).

AEX with and without WL

All subjects underwent 6 months of AEX, beginning at a training volume of 3 sessions/wk of approximately 20 min at ~50% of VO2max and gradually increasing to 3 sessions/wk of 40–45 min at 60–70% of VO2max, a level maintained for more than 4 months. For inclusion in our analyses, subjects were required to have completed more than 80% of scheduled exercise sessions. All subjects maintained a diet consistent with the AHA Step 1 guidelines, and diets were monitored by a registered dietician throughout the intervention. Subjects enrolled in the AEX + WL study met weekly with the registered dietician and were counseled to reduce their body weight (>5% reduction) through caloric deficit (~250 kcal/d). Subjects enrolled in the AEX study with weight maintenance were counseled to maintain their body weight throughout the study with caloric intake increased to match the energy expended during AEX.

Statistical analyses

The primary study outcomes were body weight, LDM, FPG, 120-min glucose (G120), and GAUC; secondary study outcomes were body mass index (BMI), fat mass, percent body fat, IAF, SAF, thigh sc fat (TSF), NDM, fasting insulin (FI), 120-min insulin (I120), IAUC, ISIM, HOMA-IR, and HOMA-B. Data are presented as means ± SEM with the exception of plasma insulin data, which were log-transformed to result in a normal distribution. Geometric mean and 95% confidence intervals are reported for insulin data. Values of LDM, TSF, and NDM are presented as the total cross-sectional area in both lower limbs. Paired Student’s t tests were used to test for differences in body composition and responses to an OGTT before and after the intervention. ANOVA was used to test for differences in body composition, regional fat distribution, and responses to the OGTT between the AEX and AEX + WL groups. Bivariate and multivariate linear regression analyses were used to investigate relationships between changes in body composition and changes in glucose metabolism. For multivariate regression analyses, partial correlation coefficients are reported. Variables in the multivariate regression models at baseline included age, weight, percent body fat, IAF, SAF, TSF, and LDM. Variables in the multivariate regression models after 6 months of AEX included the changes in weight, IAF, SAF, TSF, and LDM, as well as the percent change in fat mass. Two-tailed probabilities are reported for all analyses.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
At baseline, subjects in the AEX and AEX + WL groups were similar in age (62 ± 1 vs. 60 ± 1 yr, respectively), VO2max (27.3 ± 0.9 vs. 26.4 ± 1.7 ml/kg·min, respectively), BMI, and other physical characteristics (Table 1Go). There were no significant differences in glucose or insulin responses to an OGTT between groups at baseline (Table 2Go). The relationship of glucose tolerance to LDM was examined in all subjects at baseline. In bivariate regression analyses, LDM correlated with FPG, G120, and GAUC at baseline (Fig. 1Go, P < 0.01). This was confirmed by multivariate regression models, where only LDM remained an independent, significant correlate of FPG, G120, and GAUC (r = 0.37, r = 0.46, and r = 0.36, respectively, P < 0.05) among all body composition variables. At baseline, LDM also correlated with I120 (r = 0.36, P = 0.02) and with ISIM (r = 0.38, P = 0.02) in bivariate analysis but not with FI [r = 0.14, not significant (NS)], IAUC (r = 0.25, NS), HOMA-IR (r = 0.27, NS), or HOMA-B (r = 0.26, NS). The correlations of LDM with I120 and ISIM were not significant in multivariate analysis (r = 0.12 and r = 0.08, respectively, NS). In bivariate analyses, the cross-sectional area of IAF correlated with FI (r = 0.37, P < 0.05), I120 (r = 0.45, P < 0.01), and IAUC (r = 0.46, P < 0.01). The SAF cross-sectional area also correlated with FI (r = 0.43, P < 0.01), I120 (r = 0.36, P < 0.05), and IAUC (r = 0.44, P < 0.01). The cross-sectional area of TSF correlated only with IAUC (r = 0.36, P < 0.05). In multivariate analyses, these three fat depots did not independently correlate with insulin or glucose (data not shown).


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  		TABLE 1. Body composition of subjects at baseline

 

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  		TABLE 2. Glucose and insulin responses of subjects to an OGTT at baseline

 

Figure 1
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  		FIG. 1. Scatter plots depicting the correlation between LDM and FPG (top), G120 (middle), and GAUC (bottom) during an OGTT at baseline in all subjects.

 
Effects of interventions

The AEX + WL group significantly decreased FPG, G120, GAUC, I120, IAUC, and all body composition measures (Figs. 2Go and 3Go, P < 0.01). The AEX group significantly decreased FI, I120, IAUC, IAF, and SAF (Figs. 2Go and 3Go, P < 0.01) but did not decrease FPG, G120, GAUC, LDM, or TSF (Figs. 2Go and 3Go). There were significant differences in changes in body composition between the AEX and AEX + WL groups after the intervention (Fig. 2Go) but not in VO2max (5.6 ± 0.9 vs. 4.6 ± 1.9 ml/kg fat-free mass·min). The AEX + WL group had greater reductions in body weight (–8.5 vs. –1.6%, respectively), fat mass (–20.6 vs. –8.1%, respectively), IAF (–29.5 vs. –10.2%, respectively), SAF (–25.1 vs. –4.8%, respectively), and LDM (–13.5 vs. +1.3%, respectively) when compared with the AEX group (Fig. 2Go, P < 0.01 for all). Men in the AEX + WL group also had greater reductions in FPG (–8.3 vs. +2.1%, respectively), G120 (–22.5 vs. –3.6%, respectively), and GAUC (–17.3 vs. –3.1%, respectively) than men in the AEX group (Fig. 3Go, P < 0.01 for all). The AEX + WL group also showed a significantly greater improvement than the AEX group in I120 (Fig. 3Go, P < 0.05), ISIM (2.3 ± 0.4 vs. 0.7 ± 0.3, respectively, P < 0.01), and HOMA-B (23 ± 27 vs. –25 ± 10, respectively, P < 0.05), although the change in HOMA-B was not statistically significant in the AEX + WL group. There were no differences between the AEX + WL and AEX groups in the change of HOMA-IR (–0.51 ± 0.23 vs. –0.41 ± 0.17, NS).


Figure 2
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  		FIG. 2. Changes in body composition after AEX vs. AEX + WL. Within-group changes were significant for all variables (P < 0.01) with the exception of LDM in the AEX group. *, Significant difference between AEX and AEX + WL, P < 0.01.

 

Figure 3
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  		FIG. 3. Changes in glucose and insulin responses to an OGTT after AEX vs. AEX + WL. Within-group changes were significant for FPG, G120, and GAUC in the AEX + WL group and for I120 and IAUC in both groups (P < 0.01). *, Significant difference between AEX and AEX + WL, P < 0.01.

 
The relationship between changes in LDM and changes in glucose tolerance was then assessed in all subjects. There was a direct relationship between the changes in LDM and the changes in FPG, G120, and GAUC in the overall group of older men (Fig. 4Go; P < 0.05). In multivariate regression models, {Delta}LDM was the only independent correlate of {Delta}FPG, {Delta}G120, and {Delta}GAUC (r = 0.35 for all, P < 0.05) among all body composition variables. The changes in FI, I120, IAUC, ISIM, HOMA-IR, and HOMA-B did not correlate with {Delta}LDM (r = –0.12–0.22, NS). The changes in IAF, SAF, and TSF were not related to the changes in FPG, G120, or GAUC in multivariate analyses, nor with FI, I120, or IAUC in bivariate analyses (data not shown).


Figure 4
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  		FIG. 4. Scatter plots depicting the correlation between changes in LDM and changes in FPG (top), G120 (middle), and GAUC (bottom) during an OGTT after the interventions in all subjects.

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
We report the finding that AEX alone does not decrease midthigh LDM, but the addition of WL to AEX results in significant reductions in midthigh LDM and plasma glucose response to an OGTT in previously sedentary older men. Furthermore, the change in midthigh LDM was an independent predictor of changes in FPG and glucose tolerance in our subjects. In addition to the different changes of LDM and plasma glucose between the AEX and AEX + WL groups, there were differences in the changes of the cross-sectional areas of IAF and SAF. However, after accounting for the change in LDM in our regression models, the changes in the other regional fat depots did not independently add to the prediction of changes in glucose tolerance.

At baseline, we find that there is a direct and independent relationship between midthigh LDM and plasma glucose response to an OGTT. Previous reports show that LDM (or muscle attenuation) correlates with glucose disposal during a hyperinsulinemic-euglycemic clamp (4, 20, 26, 27). Together, these results suggest that LDM influences glucose homeostasis. Given this relationship, interventions targeted to reduce LDM should be considered to improve glucose tolerance. The findings from our AEX group indicate that AEX alone is inadequate to reduce LDM and improve glucose tolerance. Our results are consistent with evidence that aerobic exercise alone does not change or may increase im lipid (6, 14). Caloric deficit-induced WL may also reduce LDM, but results are mixed. Two studies have shown that caloric deficit-induced WL does not result in decreased im lipid in young to middle-aged men and women (17, 18). Conversely, one study in older women (16) and one in younger men and women (20) show decreased LDM with WL alone. Even when caloric deficit-induced WL did result in reduced LDM, the reduction did not correlate with increases in glucose disposal during a hyperinsulinemic-euglycemic clamp (16, 20). These results suggest that neither intervention alone is sufficient to decrease LDM with effects on glucose tolerance. Previous research demonstrates that WL should be added to AEX to improve glucose response to an OGTT in older men, but either intervention alone is sufficient to improve the insulin response to an OGTT (10, 12). The data from the present study confirms these findings and indicates that LDM may mediate the improvement in glucose response but not an improvement in insulin response to an OGTT.

The paradoxical effect of AEX training on im lipid should also be considered. Endurance-trained athletes who are highly insulin sensitive exhibit levels of im fat that are similar to the higher levels observed in individuals with type 2 diabetes (15). Because highly trained athletes have an increased ability to oxidize fat compared to sedentary individuals (14, 19), it is likely that high levels of im fat are healthy in highly trained individuals but unhealthy in sedentary individuals. Our data suggest that LDM negatively impacts glucose metabolism in sedentary and moderately trained older men, which, when combined with observations of highly trained athletes, leads to the speculation that this relationship may become uncoupled with further increases in training status and the associated changes in the metabolic characteristics of skeletal muscle. Long-term longitudinal studies will be required to determine whether such a pattern might exist.

In contrast with our results, three previous investigations of AEX with WL report no reduction in im lipid (17, 18, 19). Three factors likely contribute to the different findings in these reports and the present study: the age of subjects, the inclusion of women, and the different measurement techniques used. The age of the subjects may contribute to the discordant results because the mean age of subjects in the aforementioned studies was ~40 yr and im lipid content is higher in sedentary and overweight older individuals. For example, men and women that fall within our age range exhibit higher im lipid content and higher plasma glucose responses to an OGTT than their younger counterparts (2, 3). Significant decreases in LDM with AEX and WL may not occur in younger and middle-aged subjects, in part due to their lower initial levels of LDM and higher fitness. The relationship between LDM and glucose homeostasis may also differ between men and women. A previous report from our laboratory shows that in older women, AEX with WL results in decreased LDM, but the changes in glucose utilization during a hyperinsulinemic-euglycemic clamp correlated with IAF, not LDM (16). Although we did not directly compare relationships between LDM and glucose tolerance between men and women, our previous findings and the present findings suggest that changes in glucose homeostasis may be mediated by changes in different regional fat depots in older men and women. Finally, different measurement techniques (i.e. histochemistry, midthigh CT, and proton magnetic resonance spectroscopy of the soleus) may affect study outcomes, particularly when comparing im lipid of the soleus to CT measures of the midthigh because muscle attenuation of the midthigh and soleus does not correlate strongly (28).

Several mechanisms may contribute to the impaired glucose tolerance associated with a sedentary lifestyle, obesity, and the accumulation of ectopic body fat with aging. Decreases in proadipogenic transcription factor expression (29) and increases in antiadipogenic factor expression (30) may impair the inability to expand adipose tissue and result in aberrant storage of lipid in muscle and other tissue depots (31). Although WL (particularly the reduction of fat mass) may allow for a return to more normal lipid storage in adipose tissue and reduce aberrant lipid disposal into muscle (i.e. reduce LDM), the failure of weight loss-induced changes in LDM to correlate with changes in glucose tolerance suggests that WL alone is inadequate to improve glucose tolerance. Insufficient oxidation of lipid by skeletal muscle may also lead to chronic lipid accumulation and lipotoxicity that contributes to IR. Older subjects with lower rates of mitochondrial oxidative phosphorylation activity (~40% lower than young counterparts) have higher im lipid (~45%) and lower glucose disposal (~40%) during a hyperinsulinemic-euglycemic clamp (32). Decreased expression of transcription factors related to mitochondrial volume and fat oxidation such as peroxisome proliferator-activated receptor {gamma} coactivator-1 {alpha} (33) and carnitine palmitoyltransferase (34) could contribute to the increase in im lipid in sedentary, overweight older individuals. AEX increases the expression of enzymes and factors such as carnitine palmitoyltransferase I (35) and peroxisome proliferator-activated receptor {gamma} coactivator-1{alpha} (36), which could help promote a decrease in lipid accumulation in skeletal muscle. However, even with the AEX-induced increase in fat oxidation, AEX alone does not independently reduce LDM. We speculate that the reversal of a sedentary lifestyle with a corresponding reduction of obesity may promote a return to normal lipid storage (through WL) and metabolism (through AEX), resulting in the reduction in LDM and improvement in glucose tolerance that we observed in the current study. Further experiments are needed to clarify the mechanisms underlying this and the specific cellular and molecular effects of WL and AEX in older men.

Although we have identified a direct relationship between changes in LDM and glucose tolerance in a large number of previously sedentary older men, the strengths and limitations of this study require discussion. First, a major strength of this study is the selection of older men in good health. This minimized the potential confounding effects of medications and diseases on metabolic function. Furthermore, all subjects received instruction on the AHA Step I diet and diets were monitored throughout the study, minimizing dietary influences on metabolic function. The inclusion of only older men does limit our ability to generalize our results and prevents the determination of true aging or sex effects on changes in LDM and glucose tolerance, but does allow us to eliminate sex and minimize age as confounding factors. One limitation of this study is that single cross-sectional CT images of the midthigh were used to quantify LDM, rather than measurement of LDM at several sites throughout the thigh. At the time of this study, only midthigh CT images were available for these subjects. Lastly, ectopic fat depots other than LDM (e.g. hepatic fat content) may exert independent effects on IR and glucose tolerance (37). We did not measure hepatic fat content in the present study.

In summary, the current study shows that midthigh LDM is an independent predictor of glucose tolerance in sedentary older men and that WL should be added to AEX to decrease LDM and improve glucose tolerance in older men. Our results suggest that WL is an integral component of interventions to offset the negative health effects of a sedentary lifestyle and obesity in older men and that improvements in glucose tolerance induced by AEX + WL are mediated in part by decreases in im lipid.


   Acknowledgments
 
Our appreciation is extended to the men who participated in this study. We are grateful to Andrew P. Goldberg, M.D. for his guidance with this project and to the students, nurses, laboratory technicians, and exercise physiologists who assisted with this study.


   Footnotes
 
This work was supported by the Department of Veterans Affairs (Veterans Affairs Merit Review Grant to L.I.K. and A.S.R. and Veterans Affairs Career Scientist to A.S.R.); by the Baltimore Veterans Affairs Medical Center Geriatric Research, Education, and Clinical Center; by the University of Maryland Claude D. Pepper Center (Grant AG-12583 to Dr. Andrew P. Goldberg); and by the National Institutes of Health (Grants AG-15389 to J.M.H., AG-17474 to J.M.H., AG-019310 to A.S.R., NIH T32-AG-000219 support for S.J.P., and NIH K01-AG-021457 to L.J.J.).

The authors have nothing to disclose.

First Published Online January 2, 2007

Abbreviations: AEX, Aerobic exercise training; AHA, American Heart Association; BMI, body mass index; CT, computed tomography; FI, fasting insulin; FPG, fasting plasma glucose; G120, 120-min glucose; GAUC, glucose area under the curve; HOMA-B, homeostasis model assessment for ß-cell; HOMA-IR, homeostasis model assessment for insulin resistance; I120, 120-min insulin; IAF, intraabdominal fat; IAUC, insulin area under the curve; IR, insulin resistance; ISIM, insulin sensitivity index calculated using the method of Matsuda and DeFronzo; LDM, low-density muscle; NDM, normal-density muscle; NS, not significant; OGTT, oral glucose tolerance test; SAF, sc abdominal fat; VO2max, maximal oxygen consumption; TSF, thigh sc fat; WL, weight loss.

Received September 27, 2006.

Accepted December 21, 2006.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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