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Cardiorespiratory Fitness Attenuates Metabolic Risk Independent of Abdominal Subcutaneous and Visceral Fat in Men

¹ School of Physical and Health Education, Queen’s University, Kingston, Ontario, Canada
² Department of Community Health and Epidemiology, Queen’s University, Kingston, Ontario, Canada
³ Centers for Integrated Health Research, The Cooper Institute, Dallas, Texas
⁴ Division of Endocrinology and Metabolism, Department of Medicine; Queen’s University, Kingston, Ontario, Canada

Address correspondence and reprint requests to Robert Ross, PhD, School of Physical and Health Education, Queen’s University, Kingston, Ontario, Canada, K7L 3N6. E-mail: rossr{at}post.queensu.ca

	ABSTRACT

TOP ABSTRACT INTRODUCTION RESEARCH DESIGN AND METHODS RESULTS CONCLUSIONS References

 
OBJECTIVE—Moderate to high levels of cardiorespiratory fitness (CRF) are associated with a lower risk of the metabolic syndrome and all-cause mortality. Unknown is whether CRF attenuates health risk for a given level of abdominal visceral fat, subcutaneous fat, and/or waist circumference.

RESEARCH DESIGN AND METHODS—The sample studied comprised 297 apparently healthy men with available computed tomography or magnetic resonance imaging scans of the abdomen, metabolic data, and maximal treadmill exercise test results. Men were categorized into low-CRF (20%, n = 56), moderate-CRF (40%, n = 94), and high-CRF (40%, n = 147) groups based on age and exercise test results. All analyses were adjusted for age.

RESULTS—For a given level of waist circumference, visceral fat, or subcutaneous fat, the high-CRF group had lower triglyceride levels (P < 0.05) and higher HDL cholesterol levels than the low- or moderate-CRF groups. There was a significant group interaction (P < 0.01) for blood pressure, indicating that the increase in blood pressure per unit increase in visceral fat or waist circumference was greater in men in the low-CRF group compared with the high-CRF group. The relative risks of having the metabolic syndrome were 1.8 (95% CI 1.0–3.1) and 1.6 (0.9–2.7) times higher in the low- and moderate-CRF groups, respectively, compared with the high-CRF group after adjusting for age, visceral fat, and subcutaneous fat (P for trend = 0.06).

CONCLUSIONS—High levels of CRF are associated with a substantial reduction in health risk for a given level of visceral and subcutaneous fat.

Abbreviations: CRF, cardiorespiratory fitness

	INTRODUCTION

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It is well established that abdominal adiposity is a strong predictor of morbidity and mortality independent of BMI (1,2). It is also reported that high levels of cardiorespiratory fitness (CRF) are associated with lower risk of metabolic syndrome (3) and all-cause mortality (4–6). Although both abdominal fat and low CRF are significant predictors of health risk, the independent contribution of these two factors is not firmly established. Recently, Ross and Katzmarzyk (7) reported that for a given BMI, individuals with high CRF had lower abdominal skinfold thickness and waist circumference compared with individuals with lower CRF, independent of sex. Similarly, Wong et al. (8) report that for a given BMI, men with high CRF have lower total abdominal, visceral, and abdominal subcutaneous fat levels compared with men with low CRF, a finding that remains true for African-American men and women (9). Although it is clear that high CRF is associated with lower levels of abdominal adiposity, the association between CRF and measures of metabolic health for a given level of abdominal subcutaneous and/or visceral adiposity remains largely unknown.

Regular physical activity is an effective means of improving CRF and reducing waist circumference, visceral fat, and subcutaneous fat independent of a corresponding change in BMI (10,11). Furthermore, regular physical activity is also associated with favorable changes in blood lipid profiles, blood pressure, and glucose metabolism; these improvements often occur with little or no improvement in BMI (12). Recently, Nagano et al. (13) reported that high CRF is associated with a lower risk of hyperinsulinemia and increased HDL cholesterol levels after controlling for visceral fat in Japanese individuals with glucose intolerance and type 2 diabetes. In that study, the authors combined men and women in their analyses and did not simultaneously control for subcutaneous abdominal fat and/or waist circumference. Both abdominal subcutaneous fat (14) and waist circumference (15) are reported to be strong, independent correlates of metabolic risk.

The primary purpose of this study was, therefore, to determine whether higher levels of CRF are associated with lower levels of selected metabolic risk factors for a given level of abdominal subcutaneous fat, visceral fat, and waist circumference. To examine this question, we studied a sample of Caucasian men varying widely in abdominal adiposity and CRF.

	RESEARCH DESIGN AND METHODS

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At Queen’s University (Kingston, Canada), subjects comprised 95 men who had participated in body composition studies and were recruited via the general media. At the Cooper Clinic (Dallas, TX), subjects comprised 202 white men who voluntarily received a comprehensive medical examination including computed tomography, maximal exercise test, and clinical examination. Inclusion criteria required that the subjects were white, were nonsmokers, and were not taking medications known to affect the primary outcome variables. Exclusion criteria were a history of diabetes, cardiovascular disease, or cancer. All participants gave informed consent in accordance with the ethical guidelines of the respective institutional review boards.

Venous blood samples were obtained from the antecubital vein after a 12-h overnight fast. Measurements included total cholesterol, HDL cholesterol, triglyceride, and glucose levels using standard analytical techniques. Blood pressure was measured with a mercury sphygmomanometer using auscultatory methods. Body mass was measured on a balance scale with the subjects dressed in standard T-shirts and shorts. Barefoot standing height was measured to the nearest 0.1 cm using a stadiometer. Waist circumference was obtained at the level of the umbilicus. Metabolic syndrome was defined according to the criteria established by Adult Treatment Panel III (16). Participants were classified as having the metabolic syndrome if they had three or more of the following risk factors: 1) high blood pressure (130 mmHg systolic); 2) central obesity (waist circumference >102 cm); 3) high triglyceride level (150 mg/ml); 4) low HDL cholesterol level (<40 mg/ml); and 5) high fasting plasma glucose level (110 mg/ml).

Measurement of visceral and subcutaneous fat
A single axial image of the abdomen (L4–L5) was obtained using a 1.5-Tesla magnetic resonance imaging scanner (General Electric, Milwaukee, WI) at Queen’s University, and with an electron beam computed tomography scanner (Imatron; General Electric, Milwaukee, WI) at the Cooper Clinic using established protocols (17,18). For magnetic resonance imaging, images were obtained using a T1-weighted, spin-echo sequence (TR = 210 ms, TE = 17 ms) with a 480-mm field of view and a 256-squared matrix. For computed tomography, images (L4–L5) were obtained using 130 kV and 630 mA with a 480-mm field of view and a 512 x 512 matrix.

Maximal treadmill test
At Queen’s University, CRF was determined by VO_2max using a graded maximal treadmill test. For all subjects, the treadmill speed, predetermined during a practice session, was held constant. The initial grade was set at 0% for the 1st and 2nd min, was 2% for the 3rd min, and was increased by 1% every 2 min thereafter. All tests used standard open-circuit spirometry techniques (SensorMedics, Yorba Linda, CA). VO_2max was attained when at least two of the following three criteria were achieved: no increase in VO_2max despite further increases in treadmill grade, a heart rate at or above age-predicted maximum (220 – age), and/or a respiratory exchange ratio in excess of 1.0. At the Cooper Clinic, CRF was evaluated with a maximal exercise test performed on a treadmill according to a modified Balke procedure (19). Initial treadmill speed was 88 m/min. The grade was 0% for the 1st min, was 2% for the 2nd min, and then was increased by 1% every minute until 25 min. For participants able to continue beyond 25 min, the grade remained constant, and the speed was increased 5.4 m/min each minute until test termination. Total treadmill endurance time with this protocol has been shown to highly correlate with VO_2max (r = 0.94) (20). Total treadmill time was converted to VO_2max using a standard prediction equation (20).

Statistical analyses
Participants were categorized as low CRF (lowest, 20%), moderate CRF (middle, 40%), or high CRF (highest, 40%) based on age-specific VO_2max cutoff points derived from the Aerobics Center Longitudinal Study cohort (6). A one-way ANOVA was used to examine differences in subject characteristics across fitness groups. When the ANOVA result was significant (P < 0.05), a Tukey’s post hoc comparison test was used to identify specific between-group differences. General linear models were used to determine the influence of CRF on the relationship between abdominal obesity and metabolic risk. CRF and abdominal measures (waist circumference, visceral fat, and subcutaneous fat) were the independent variables and metabolic risk factors were the dependent variables. Both abdominal measures and metabolic risk factors were entered as continuous variables, whereas CRF groups were entered as categorical variables in the general linear models. Both the main effects for CRF group and interaction effects (e.g., visceral fat x CRF group) were included in each of the models to test for the equality of slopes. If the interaction effects were not significant (e.g., the slopes were not different), the analyses for main effects were repeated excluding the interaction term. All analyses were adjusted for age.

All general linear models were tested for institutional differences in the relationships between waist circumference, visceral fat, and subcutaneous fat and metabolic risk. An institution term was added to the models to examine the influence of institutions on the relationships between all the independent variables. Because no institutional interactions were found in any model, subjects from the two institutions were pooled for all analyses. To facilitate comparisons, all figures were standardized to a 40-year-old individual.

Proc GENMOD was used to determine the relative risk (RR) and 95% CI estimates for the metabolic syndrome between the CRF groups. For these analyses, tertiles of age, visceral fat, and abdominal subcutaneous fat were used as the independent variables in the models. The presence of the metabolic syndrome was coded as a categorical variable and was used as the dependent variable in the models. The high-CRF group was used as the reference category (RR 1.0). All analyses were performed using SAS software and procedures (version 8; SAS Institute, Cary, NC).

	RESULTS

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The subject characteristics in Table 1 show that the subjects varied widely in age, all measures of abdominal adiposity, and CRF.

View larger version (23K): [in this window] [in a new window]   Figure 1— Relationship between waist circumference (WC) and metabolic risk, standardized to 40 years of age. A: Low CRF, y = –14.60 – 0.17 (age) + 2.20 (WC); moderate CRF, y = –29.81 – 0.17 (age) + 2.20 (WC); high CRF, y = –59.79 – 0.17 (age) + 2.20 (WC). B: Low CRF, y = 57.26 + 0.21 (age) – 0.28 (WC); moderate CRF, y = 61.43 + 0.21 (age) – 0.28 (WC); high CRF, y = 62.64 + 0.21 (age) – 0.28 (WC). C: Low CRF, y = 13.67 + 0.42 (age) + 0.84 (WC); moderate CRF, y = 55.49 + 0.42 (age) + 0.45 (WC); high CRF, y = 93.03 + 0.42 (age) + 0.08 (WC). D: No group or group x WC effect.

View larger version (23K): [in this window] [in a new window]   Figure 2— Relationship between visceral fat (VAT) and metabolic risk, standardized to 40 years of age. A: Low CRF, y = 183.13 – 1.21 (age) + 0.48 (VAT); moderate CRF, y = 156.46 – 1.21 (age) + 0.48 (VAT); high CRF, y = 129.48 – 1.21 (age) + 0.48 (VAT). B: Low CRF, y = 30.13 + 0.33 (age) – 0.06 (VAT); moderate CRF, y = 35.89 + 0.33 (age) – 0.06 (VAT); high CRF, y = 37.36 + 0.33 (age) – 0.06 (VAT). C: Low CRF, y = 85.72 + 0.28 (age) + 0.14 (VAT); moderate CRF, y = 97.26 + 0.28 (age) + 0.07 (VAT); high CRF, y = 105.99 + 0.28 (age) + 0.02 (VAT). D: No group or group x VAT effect.

No group differences were observed in fasting glucose for a given level of waist circumference (Fig. 1D) or visceral fat (Fig. 2D).

Relationship between subcutaneous fat and metabolic risk
For a given level of subcutaneous fat, men with high CRF had lower triglyceride levels (main effect, P < 0.05) than men with low and moderate CRF (data not shown). No significant differences were observed between the low- and moderate-CRF groups (P > 0.05). Men with moderate and high CRF had a higher HDL cholesterol level (main effect, P < 0.05) than men with low CRF. No significant difference between the moderate- and high-CRF groups was observed (P > 0.05). No significant subcutaneous fat x CRF group interactions for triglyceride or HDL cholesterol levels were found, indicating that the slopes were not different between the groups (P > 0.05).

No CRF group differences were observed for systolic blood pressure or fasting glucose for a given level of subcutaneous fat (data not shown).

CRF and RRs for the metabolic syndrome
As depicted in Fig. 3, after adjustment for age, the RRs of having the metabolic syndrome were 4.6 (95% CI 2.7–7.8) and 2.7 (1.5–4.6) times higher in the low- and moderate-CRF groups, respectively, compared with the high-CRF group (P for trend <0.001). After adjustment for age and visceral fat, the RRs of having the metabolic syndrome were 2.5 (1.4–4.4) and 1.8 (1.0–3.1) times higher in the low- and moderate-CRF groups, respectively, than in the high-CRF group (P for trend <0.001). Similarly, after adjusting for age and subcutaneous fat, the RRs of having the metabolic syndrome were 2.7 (1.6–4.6) and 1.8 (1.1–31) times higher in the low- and moderate-CRF groups, respectively, by comparison with the high-CRF group (P for trend <0.001). After adjustment for age, visceral fat, and subcutaneous fat, the RRs of having the metabolic syndrome were 1.8 (1.0–3.1) and 1.6 (0.9–2.7) times higher in the low- and moderate-CRF groups compared with the high-CRF group (P for trend = 0.06).

View larger version (24K): [in this window] [in a new window]   Figure 3— RRs and 95% CIs for the metabolic syndrome after adjusting for age and visceral fat (VAT) or subcutaneous fat (SAT) in men with low, moderate, and high CRF. *Significantly greater than high-CRF group, P < 0.01; significantly greater than high-CRF group, P < 0.05. P values are for tests of linear trend across the CRF groups.

	CONCLUSIONS

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Katzmarzyk et al. (21) reported that moderate and high levels of CRF attenuated the risk of all-cause and cardiovascular disease mortality in men associated with the metabolic syndrome. Furthermore, in men with the metabolic syndrome, there was a significant negative dose-response relationship with mortality across CRF tertiles. Similarly, Blair et al. (6) reported that an improvement in CRF is associated with a 44% lower all-cause mortality independent of changes in BMI. Therefore, our observations are consistent with previous observations suggesting that CRF protects against health risk in men.

It is noteworthy that we observed a stepwise dose-response relationship between CRF and the metabolic syndrome after controlling for age, visceral fat, and subcutaneous fat. This finding extends a previous observation by Nagano et al. (13), who recently reported that the prevalence of hyperinsulinemia and a low HDL cholesterol level is significantly lower in high-fit Japanese men and women compared with the low-fit group after controlling for age and visceral fat in insulin-resistant individuals. The fact that we did not observe a beneficial effect of CRF on fasting glucose is consistent with our previous exercise intervention studies, which failed to demonstrate improvements in fasting glucose in obese men (10) and women (11) despite significant reductions in abdominal fat and insulin sensitivity (10). In this way, insulin data would have been useful because, consistent with the findings of Nagano et al. (13), it is more likely that insulin values would be lower in those with high CRF compared with low CRF for a given glucose level.

Because CRF is a strong correlate of physical activity (22), one might expect that physical activity, like CRF, would be related to health risk independent of abdominal obesity. However, in contrast to this notion, Hunter et al. (23,24) reported that visceral fat remains associated with cardiovascular disease risk factors after controlling for physical activity, whereas physical activity is not associated with cardiovascular disease risk factors after controlling for visceral fat in both men (24) and women (23). The disparate findings may be due to the use of self-report measures of physical activity compared with maximal exercise testing. Self-report physical activity questionnaires are inaccurate, and the inaccuracy increases with the respondent’s weight (25). Use of maximal exercise tests to quantify CRF provides an objective evaluation of an individual’s recent activity patterns and accounts for 70–80% of the variance in detailed activity records (22). CRF is stronger than self-reported physical activity as a predictor of many health outcomes, most likely because fitness measurements are less prone to misclassification and because factors other than activity may influence both fitness and health through related biological factors (26,27). The mechanisms through which CRF would be independently associated with the components of the metabolic syndrome are not firmly established. Assuming that CRF reflects the recent physical activity patterns of our participants, it is reasonable to suggest that the lower levels of insulin resistance (28), blood pressure (29), and blood lipids (30) that are normally associated with routine physical activity are at least partially responsible for our findings.

Limitations of this study warrant mention. The cross-sectional design does not allow us to infer a causal relationship. Therefore, our findings require confirmation from prospective and intervention trials with serial measurements of CRF, abdominal obesity, and metabolic risk factors, which would reinforce the independent relationships between these factors. It is suggested that 40% of the variation in CRF is attributable to genetic factors (31). This does not discount our observed relationship between CRF and health risk; however, it merely suggests that CRF may be a surrogate measure for both physical activity and genotype. The absence of dietary intake data is a limitation because dietary factors are known to influence some components of the metabolic syndrome. Finally, whether our findings remain true for women or other ethnic groups is unknown.

In conclusion, our findings suggest that high CRF is associated with a substantially lower metabolic health risk for a given level of visceral fat, subcutaneous fat, or waist circumference. Furthermore, there was an inverse dose-response relationship between CRF and metabolic syndrome independent of abdominal fat. These findings suggest that moderate CRF levels protect against obesity-related health risk and, therefore, reinforce the recommendation that adults adopt a physically active lifestyle.

	Acknowledgments

 
This research was supported, in part, by research grants from the Canadian Institutes of Health Research (MT13448; to R.R.) and the National Institutes of Health (AG06945; to S.N.B. and T.S.C.).

	Footnotes

 
A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

Received for publication September 8, 2004. Accepted for publication January 2, 2005.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Lee, S. Articles by Ross, R. Search for Related Content PubMed PubMed Citation Articles by Lee, S. Articles by Ross, R. Social Bookmarking                What's this?