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Cardiorespiratory Fitness is Associated with Lower Abdominal Fat Independent of Body Mass Index


Medicine & Science in Sports & Exercise: February 2004 - Volume 36 - Issue 2 - p 286-291
doi: 10.1249/01.MSS.0000113665.40775.35
APPLIED SCIENCES: Physical Fitness and Performance

WONG, S. L., P. T. KATZMARZYK, M. Z. NICHAMAN, T. S. CHURCH, S. N. BLAIR, and R. ROSS. Cardiorespiratory Fitness is Associated with Lower Abdominal Fat Independent of Body Mass Index. Med. Sci. Sports Exerc., Vol. 36, No. 2, pp. 286–291, 2004.

Purpose To determine whether, for a given body mass index (BMI), men with high cardiorespiratory fitness (CRF) have lower waist circumference (WC) and less total abdominal, abdominal subcutaneous, and visceral adipose tissue (AT) compared with men with low CRF.

Methods Subjects were categorized into HIGH CRF (N = 169) and LOW CRF (N = 124) groups based on age and CRF measured using a maximal treadmill test. Total abdominal, abdominal subcutaneous and visceral AT were measured by computerized tomography.

Results For a given BMI, men in the HIGH CRF group had significantly lower WC (P < 0.001), total abdominal (P < 0.001), visceral AT (P < 0.001), and abdominal subcutaneous AT (P < 0.001) compared with men in the LOW CRF group.

Conclusion These findings suggest that the ability of CRF to attenuate the health risks associated with BMI may be partially mediated through a reduction in abdominal AT. Accordingly, our observations reinforce the importance of regular physical activity in the prevention and reduction of obesity-related health risk independent of a corresponding reduction in body weight.

1School of Physical and Health Education,

2Department of Community Health and Epidemiology,

3Department of Medicine, Division of Endocrinology and Metabolism, Queen’s University, Kingston, Ontario, CANADA; and

4Centers for Integrated Health Research, The Cooper Institute, Dallas, TX

Address for correspondence: Robert Ross, Ph.D., School of Physical and Health Education, Queen’s University, Kingston, Ontario, Canada, K7 L 3N6; E-mail:

Submitted for publication June 2003.

Accepted for publication September 2003.

It is generally accepted that waist circumference (WC) is positively associated with increased morbidity and mortality from Type 2 diabetes and cardiovascular disease (CVD) independent of body mass index (BMI) (12,18). It is also established that cardiorespiratory fitness (CRF) is associated with reductions in all-cause and CVD mortality rates (4). Further, evidence from large observational studies suggests that CRF attenuates obesity-related health risk (30,32). Indeed, it has been reported that low CRF is associated with premature mortality in individuals classified as normal-weight, overweight, or obese, independent of other mortality predictors, including smoking, hypertension, and Type 2 diabetes (32).

The observation that CRF attenuates obesity-related health risk as measured by BMI (14,32) may be explained by differences in abdominal adiposity. Abdominal obesity as measured by WC is a strong marker of metabolic risk and disease independent of BMI (12), and recent evidence suggests that exercise training is associated with a reduction in WC, independent of changes in BMI (26). Further, in a large cohort representative of the Canadian population, it was shown that high CRF is associated with significantly lower levels of WC for a given BMI by comparison with those with low CRF, independent of gender (28). Together, these findings suggest that reductions in abdominal obesity may be a mechanism by which exercise attenuates obesity-related health risk as measured by BMI. However, currently it is not known whether the reduction in abdominal obesity is a consequence of reductions in visceral and/or abdominal subcutaneous adipose tissue (AT). Some researchers report that visceral AT is an independent predictor of metabolic risk (7,25), whereas others report that abdominal subcutaneous AT (1,10) or a subdivision of abdominal subcutaneous AT, such as deep AT (16), is of primary importance. Thus, the extent to which the attenuation of obesity-related health risk by CRF may be explained by a corresponding reduction in subcutaneous and/visceral obesity independent of BMI would add valuable insight into plausible mechanisms.

The purpose of this study was to test the hypothesis that, for a given BMI, men with high CRF have a lower WC and less total abdominal, abdominal subcutaneous, and visceral AT by comparison with men with low CRF.

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Subjects consisted of a subset of 397 Caucasian men selected from a larger cohort who received a medical examination at the Cooper Clinic in Dallas, TX, between 1995 and 2002. Inclusion criteria required that the subjects were nonsmokers and had received a computerized tomography (CT) scan of the abdominal region. Exclusion criteria included self-reported history of diabetes, heart attack, stroke, and/or cancer. Subjects were from middle to upper socioeconomic background. All subjects gave their informed written consent before participation in the examination according to the ethical guidelines of The Cooper Institute Institutional Review Board, and the study was reviewed and approved annually.

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Clinical examination.

In the morning after an overnight fast of at least 12 h, study participants completed a comprehensive medical examination. This evaluation included a physical examination, a questionnaire on demographic factors and health habits (alcohol consumption, cigarette smoking, physical activity, family history, and medication), anthropometric measurements, standardized maximal treadmill test, and a CT scan of the abdominal region. Body weight and height were measured using a standard physician’s scale and stadiometer and were used to calculate body mass index (weight in kg per height in m2). Waist circumference was measured at the level of the umbilicus using a plastic tape measure.

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Maximal treadmill test.

Cardiorespiratory fitness was evaluated using a modified Balke maximal exercise test protocol performed on a treadmill (2). The initial treadmill speed was 88 m·min−1. The grade was 0% for the first minute and was raised to 2% the second minute. Each subsequent minute the grade was further increased by 1%. After 25 min, the incline remained at 25% while the speed was increased 5.4 m·min−1 every minute until fatigue ensued, and the test was terminated. Total treadmill time was converted to maximal oxygen uptake (V̇O2max) using a standard prediction equation as it has been shown to correlate very well with V̇O2max (r = 0.94) (22).

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Measurement of abdominal AT distribution.

Axial images of the abdominal region were obtained using an electron beam CT (Imatron, General Electric, Milwaukee, WI) with a standard protocol (24). Subjects were examined while in a supine position with their arms extended above their head. Approximately 40 contiguous images (6-mm thickness) were acquired from the distal iliac crest to the caudal region of the heart. Images were obtained using 130 kV and 630 mA with a 48-cm field of view and a 512 × 512 matrix. The CT data collected in Dallas were electronically transferred to the laboratory in Kingston for analysis using specialized image analysis software (Tomovision, Inc., Montreal, Canada).

For each subject, a continuous series of five to seven CT images bordered by the L4–L5 and L3–L4 vertebral disk spaces was selected for analysis. The volume of AT was obtained by summation of the AT areas from this series of images. Adipose tissue volumes (L) were converted to mass units (kg) by multiplying the volumes by the assumed constant density for fat (0.92 kg·L−1). Adipose tissue areas (cm2) were computed using an attenuation range of −190 to −30 Hounsfield units. Visceral AT was determined by delineating the intra-abdominal cavity at the innermost aspect of the abdominal and oblique wall musculature and the anterior aspect of the vertebral body. Abdominal subcutaneous AT area was defined as the area of AT between the skin and the outermost aspect of the abdominal muscle wall. The deep and superficial depots of the abdominal subcutaneous AT were identified for a single image at the level of L4–L5 using the subcutaneous fascia (13,29).

The interobserver (two observers) error for separation of subcutaneous AT area (cm2) measurements into deep and superficial depots was determined from the analyses of a single image at L4–L5 in a subset of 70 subjects. The interobserver coefficient of variations for the division of the abdominal subcutaneous AT was 6% and 5% for deep and superficial subcutaneous AT, respectively.

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Statistical analyses.

Individuals were assigned to one of five age-specific CRF quintiles based on their age and total time on the treadmill test. These cutpoints were derived from the larger Aerobics Center Longitudinal study cohort and are described elsewhere (3). Because our subsample was restricted to 397 men, the subjects were divided into HIGH and LOW CRF groups using the upper two and lower two quintiles to ensure adequate sample sizes. The middle quintile was omitted to generate a meaningful difference in CRF between groups. Thus, the final sample used in the analysis was 293 men. Subject characteristics between the two groups were compared using independent sample t-tests. Pearson correlations were used to determine the linear association between WC and AT masses. The effect of CRF group on the relationships among BMI, total abdominal AT, visceral AT, abdominal subcutaneous AT, subdivisions of abdominal subcutaneous AT, and WC were determined using general linear models, including age as a covariate. In addition to the main effects for CRF group, an interaction term (BMI*CRF GROUP) was included to test for the equality of slopes. If no interaction effects were detected (i.e., the slopes were not different), the analysis for main effects was repeated excluding the interaction term. Estimated marginal means were calculated for WC and each AT measure. All analyses were conducted with SPSS 11.0.1 software and procedures (SPSS Inc., Chicago, IL).

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Subjects ranged in age from 30 to 76 yr and in BMI from 21.2 to 34.9 kg·m−2. Descriptive characteristics are presented in Table 1. As expected, mean V̇O2max was higher in the HIGH CRF group compared with LOW CRF group (P < 0.01). However, with the exception of superficial subcutaneous AT, there were no statistical differences between groups for age or measures of adiposity (P > 0.10). Pearson correlation coefficients between WC and visceral, abdominal subcutaneous, and total abdominal AT masses were 0.68, 0.74, and 0.82, respectively.



The general linear model analyses for WC and abdominal AT masses indicated no significant BMI × CRF group interactions, indicating that the slopes were not different in the HIGH versus LOW CRF groups (P > 0.10). Men with HIGH CRF had a lower WC for a given BMI and age (main effect, P < 0.001) than men with LOW CRF (Fig. 1).



For a given BMI, total abdominal AT mass was lower in the HIGH CRF group compared with the LOW CRF group (main effect, P < 0.001) (Fig. 2). Examination of the specific abdominal AT depots revealed that men with HIGH CRF had less visceral and abdominal subcutaneous AT mass (main effect, P < 0.001) compared to men with LOW CRF (Fig. 3). A significant (P < 0.001) main effect for CRF group was also observed for both deep and superficial subcutaneous AT (data not shown).





The mean age- and BMI-adjusted values for WC, total abdominal, visceral, and abdominal subcutaneous AT in the HIGH and LOW CRF groups are provided in Figure 4.



The results based on AT areas measured at L4–L5 and L3–L4 were similar to those for the corresponding AT mass values. There were no significant BMI × CRF group interactions, indicating that the slopes were not different in the HIGH versus LOW CRF groups (P > 0.10). Significant main effects (P < 0.001) were obtained for total abdominal, subcutaneous, and visceral AT area (e.g., cm2) at both the L3–L4 and L4–L5 levels. The mean visceral AT areas at L4–L5, adjusted for age and BMI, were 157.1 cm2 for the LOW CRF group and 138.6 cm2 for the HIGH CRF group.

All general linear models included age as a covariate. Significant main effects for age were observed for WC, total abdominal and visceral AT mass, and area values (P < 0.001) but not for subcutaneous AT. The increase in WC, and total abdominal and visceral AT with age was observed independent of BMI and CRF group.

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The primary finding of this study is that for a given BMI, men with high CRF levels have significantly lower levels of abdominal AT, by comparison with those with low CRF. The differences in abdominal adiposity between CRF groups provide insight into the plausible mechanisms by which CRF attenuates the health risks attributed to obesity. Further, they reinforce the importance of regular physical activity in the prevention and treatment of obesity-related disease independent of a reduction in body weight. Accordingly, dependence on BMI alone to determine health risk may be misleading because potential differences in abdominal adiposity as a consequence of increased CRF is ignored. Although the measurement of abdominal AT is not practical in clinical practice, the results of this and previous studies (28) show that WC is also lower in association with high CRF. Consequently, it is suggested that WC and CRF be routinely measured to assess health risk.

The results of this study support the hypothesis that men with moderate to high CRF levels have lower WC than men with low CRF independent of BMI. Although our sample consisted of Caucasian men from middle to upper socioeconomic class, the results agree with Ross and Katzmarzyk (28), who report similar observations for WC in a large sample of the Canadian population, which included men and women varying in socioeconomic class. However, whether this observation holds true independent of race is unknown.

The novel finding of this study was that men with high CRF had significantly less total abdominal, subcutaneous, and visceral AT by comparison with men in the low CRF group. This finding agrees with our observations based on WC and is consistent with numerous reports indicating that WC is a strong correlate of radiographically measured visceral and subcutaneous AT (11,15,23). Others report that exercise per se is associated with substantial reduction in subcutaneous (26) and visceral AT (17,26) in the absence of any change in BMI. Given the established association between both abdominal subcutaneous AT (13,29) and visceral AT (7,19,27) with metabolic risk, these observations suggest that a robust mobilization of abdominal fat may be a mechanism by which CRF attenuates health risk without a concomitant decrease in BMI. Because our findings are derived from a sample of Caucasian men, extrapolation to other races and women requires confirmation by further study.

In this study, the physical activity patterns of the participants were not measured, and thus, we were unable to categorically state that routine physically activity is associated with diminished abdominal fat independent of BMI. However, in a previous study, we report that the mean V̇O2max values for the LOW and HIGH CRF men were 33.9 mL·kg−1·min−1 and 49.7 mL·kg−1·min−1, respectively (28). In that study, the mean energy expenditure values from leisure time physical activity for the LOW and HIGH CRF men were 146.0 kcal·d−1 and 236.2 kcal·d−1, respectively. Because the V̇O2max values reported here (33.2 mL·kg−1·min−1 and 42.9 mL·kg−1·min−1, respectively) are similar to those previously reported for a similar group of men, we speculate that the physical activity patterns of the LOW and HIGH CRF men in the present study were also similar to those reported previously. If this is true, it suggests that the physical activity levels required to achieve the CRF levels of those within the HIGH CRF group in this study are not extraordinary. Indeed, assuming that the recommended 30 min of daily physical activity translates to approximately 200 kcal (e.g., walking 3.2 km in 30 min), the physical activity patterns for individuals in the high CRF group would be consistent with current recommendations regarding physical activity and public health (21).

Whether the combination of higher CRF and lower abdominal AT conveys a metabolic benefit by comparison with those with lower CRF and higher visceral AT for a given BMI is unknown. It has been reported that visceral AT remains a significant predictor of Type 2 diabetes after controlling for the disease risk predicted by BMI (5), and visceral AT has been implicated in the etiology of numerous metabolic risk factors for Type 2 diabetes and CVD (19,25). Further, it is consistently reported that lower visceral AT is associated with corresponding reduction in metabolic risk factors independent of obesity (6,17). Therefore, it seems reasonable to suggest that the combination of high CRF and low abdominal AT, in particular visceral AT, would be associated with reductions in metabolic risk compared with those with the same BMI, but low CRF and high visceral AT.

The observation that total abdominal and visceral AT, but not subcutaneous AT, increased with age independent of BMI and CRF extends previous reports wherein the age-associated increase in abdominal adipose tissue for a given fat mass in women is reportedly a consequence of an increase in visceral and not abdominal subcutaneous AT (8,20). Of particular interest in this study was that the CRF effect persisted throughout the age range. In other words, for a given age those in the HIGH CRF group had lower levels of abdominal and visceral fat than those in the LOW CRF group. The lower abdominal and visceral fat in the HIGH CRF group in the absence of a difference in BMI is likely explained by correspondingly lower lean mass. This notion is consistent with Gallagher et al. (9), who report that aging is associated with a progressive decrease in lean mass, and increase in fat mass, despite no change in BMI. Together, these observations reinforce once more the limitations inherent to the use of BMI alone to detect important age- and health-related changes in body composition.

The findings of this study should not be interpreted to suggest that improvement in CRF requires a concomitant change in abdominal obesity to observe a reduction in health risk. To the contrary, it is well established that regular physical activity is associated with numerous physiological effects that are beneficial to health independent of reduction in abdominal AT (3). Indeed, a single exercise session has been shown to reduce triglyceride levels, increase high-density lipoprotein levels, reduce resting blood pressure, increase glucose tolerance, and reduce insulin resistance (31). Thus, it is clear that physical activity (acute and/or chronic) conveys health benefits independent of concomitant improvement in either CRF and reductions in body weight and/or adiposity.

In summary, moderate to high CRF was associated with lower levels of abdominal AT, both subcutaneous and visceral AT depots, for a given BMI by comparison with those with low CRF in men. To the extent that these AT depots convey an increased health risk, this finding suggests a mechanism by which CRF attenuates the health risks attributed to obesity as measured by BMI. Accordingly, they suggest that assessment of health risk by BMI alone may be misleading and that the measurement of WC and CRF would substantially improve the ability to identify those at increased health risk. Further, our findings reinforce the importance of CRF in the reduction of obesity-related health risk, independent of a reduction in body weight. Clinicians unfamiliar with the measurement of CRF are encouraged to seek the expertise of appropriately certified health and fitness professionals for whom the measurement of CRF is routine. Finally, additional research is required to determine whether CRF is associated with lower abdominal AT, independent of BMI, in populations that vary by gender, ethnicity, and socioeconomic class.

Sincere appreciation is extended to Thanh-Binh Nguyen-Duy and Elisa Priest for their contributions to this research.

This research was supported in part by research grants from the National Institutes of Health to Steven N. Blair (AG06945) and Milton Z. Nichaman (HL62508), and from the Canadian Institutes of Health Research to Robert Ross (MT13448). Suzy L. Wong was supported by an Ontario Graduate Scholarship.

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