0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Original Investigation |

Visceral Adipose Tissue Accumulation, Cardiorespiratory Fitness, and Features of the Metabolic Syndrome FREE

Benoit J. Arsenault, MSc; Dominique Lachance, BSc; Isabelle Lemieux, PhD; Natalie Alméras, PhD; Angelo Tremblay, PhD; Claude Bouchard, PhD; Louis Pérusse, PhD; Jean-Pierre Després, PhD, FAHA
[+] Author Affiliations

Author Affiliations: Hôpital Laval Research Centre, Hôpital Laval (Mr Arsenault, Ms Lachance, and Drs Lemieux, Alméras, Tremblay, and Després), and Department of Anatomy and Physiology (Mr Arsenault) and Division of Kinesiology, Department of Social and Preventive Medicine (Drs Tremblay, Pérusse, and Després), Faculty of Medicine, Université Laval, Québec, Québec; and Pennington Biomedical Research Center, Louisiana State University, Baton Rouge (Dr Bouchard).


Arch Intern Med. 2007;167(14):1518-1525. doi:10.1001/archinte.167.14.1518.
Text Size: A A A
Published online

Background  It has been suggested that overweight and obese individuals with an adequate level of cardiorespiratory fitness (CRF), the so-called fat and fit, are at reduced risk of coronary heart disease and type 2 diabetes mellitus.

Methods  To determine whether individuals with low CRF have more visceral adipose tissue (AT) accumulation compared with individuals with high CRF and to verify whether low CRF is associated with a poorer metabolic profile, we performed a cross-sectional study of 169 asymptomatic men without diabetes mellitus (mean ± SD body mass index [calculated as weight in kilograms divided by height in meters squared], 25.9 ± 4.4; and mean ± SD age, 37.1 ± 14.0 years). Abdominal AT accumulation, CRF, and indexes of plasma glucose-insulin homeostasis and of the lipoprotein-lipid profile were measured.

Results  More visceral AT accumulation was observed among men in the lowest tertile of CRF compared with men in the highest tertile of CRF (mean ± SD, 139.6 ± 70.2 cm2vs 74.7 ± 41.6 cm2; P < .001). Overall, the plasma lipoprotein-lipid profiles were more favorable in men with a high CRF compared with individuals with a low CRF, as men with a low CRF had higher triglyceride (mean ± SD, 161 ± 73 mg/dL vs 99 ±45 mg/dL; P < .001) and apolipoprotein B (mean ± SD, 106 ± 23 mg/dL vs 89 ± 24 mg/dL; P < .009) levels and an increased total cholesterol–high-density lipoprotein cholesterol ratio (mean ± SD, 5.27 ± 1.00 vs 3.96 ± 1.17; P = .002) than men with high CRF. After matching individuals with similar body mass index values but with high or low CRF, men with low CRF were characterized by more visceral AT accumulation than men with high CRF (mean ± SD, 114.4 ± 59.9 cm2vs 87.8 ± 49.1 cm2; P < .007) and by a poorer metabolic profile. However, when matched for visceral AT accumulation, such differences were no longer statistically significant.

Conclusion  This study underlines the importance of visceral AT accumulation in the previously reported association between CRF and metabolic complications predictive of coronary heart disease and type 2 diabetes mellitus.

Figures in this Article

It is well recognized that an excess accumulation of body fat in the abdominal cavity (visceral adipose tissue [AT] accumulation), is associated with a cluster of metabolic abnormalities often referred to as the metabolic syndrome.1,2 To prevent visceral obesity and related metabolic abnormalities, increasing energy expenditure with regular exercise could help reduce risk factors for coronary heart disease (CHD) and type 2 diabetes mellitus.35

The lower CHD risk observed among physically active persons compared with sedentary individuals could be related to the beneficial effects of regular exercise on glucose tolerance, insulin sensitivity, and plasma lipoprotein-lipid levels.6 Regular physical activity has also been shown to induce substantial mobilization of atherogenic visceral AT.7,8 For instance, Ross et al9 reported that an endurance exercise training program, even without weight loss, could cause a selective loss of visceral fat. This preferential loss of visceral AT is usually associated with increased in vivo insulin action, reduced triglyceride and apolipoprotein B levels, larger low-density lipoprotein (LDL) particles (with or without elevated LDL cholesterol levels), and increased high-density lipoprotein cholesterol concentrations.10,11

Studies6,1215 have provided evidence that a low level of cardiorespiratory fitness (CRF), quantified as poor performance on a maximal treadmill exercise test, was a powerful predictor of CHD events and mortality and of the risk of developing type 2 diabetes mellitus in men and women, independent of body weight. The investigators found that overweight and obese subjects with high CRF were at reduced CHD risk compared with subjects with normal body weight and low CRF. Based on these observations, the authors pioneered the theory that one could be “fat and fit” and at reduced CHD risk compared with nonobese unfit individuals. However, little is known about the body fat distribution and visceral AT mass of fat and fit subjects. Therefore, we first tested the hypothesis that individuals with high CRF may have less visceral AT accumulation compared with individuals with low CRF, regardless of body mass index (BMI [calculated as weight in kilograms divided by height in meters squared]). We then examined the contribution of such reduced visceral AT accumulation to the more favorable metabolic risk profile of fit compared with unfit individuals.

POPULATION

Subjects in this study were asymptomatic men without diabetes mellitus who participated in phase 2 of the Québec Family Study. Briefly, the Québec Family Study is a population-based study of French Canadian families living in and around Québec City, Québec. The Québec Family Study was approved by the Medical Ethics Committee of Université Laval, Québec. Subjects were recruited through the media and gave their written informed consent to participate in the study. Only healthy nonsmoking men aged between 18 and 65 years who were not receiving treatment for CHD, diabetes mellitus, dyslipidemias, or endocrine disorders were considered for the present analyses. Further details about the Québec Family Study have been previously reported.16

ANTHROPOMETRIC AND BODY COMPOSITION MEASUREMENTS

Height, body weight,17 and waist circumference18 were measured following standardized procedures. The measurement of cross-sectional areas of abdominal AT accumulation was performed by computed tomography (between L4 and L5 vertebrae) as previously described.19 Fat mass and fat-free mass (FFM) were derived from the measurement of body density assessed by underwater weighing.20

PLASMA LIPOPROTEIN-LIPID PROFILE

Following a 12-hour overnight fast, blood samples were collected from an antecubital vein into vacuum tubes (Vacutainer; Becton, Dickinson and Co, Franklin Lakes, New Jersey) containing EDTA (Miles Pharmaceuticals, Rexdale, Ontario) for the measurement of plasma lipid and lipoprotein levels. Plasma cholesterol and triglyceride levels were analyzed in plasma and lipoprotein fractions (Technicon RA-500; Bayer Corporation, Tarrytown, New York) using enzymatic reagents (Randox Laboratories Ltd, Crumlin, England). Plasma very LDL (density, <1.006 g/mL) was isolated by ultracentrifugation,21 and the high-density lipoprotein fraction was obtained after precipitation of LDL in the infranatant (density, ≥ 1.006 g/mL) with heparin and manganese chloride.21,22 The cholesterol content of the infranatant fraction was measured before and after the precipitation step, allowing the calculation of LDL cholesterol levels. Apolipoprotein B levels were measured in plasma using the rocket immunoelectrophoretic method of Laurell.23 Lyophilized serum standards for apolipoprotein B measurements were prepared in our laboratory and were calibrated using reference standards (Centers for Disease Control and Prevention, Atlanta, Georgia). The LDL peak particle size was measured by 2% to 16% nondenaturing polyacrylamide gradient gel electrophoresis performed on whole plasma as previously described.24

ORAL GLUCOSE TOLERANCE TEST

A 3-hour 75-g oral glucose tolerance test was performed in the morning after an overnight fast. Blood samples were collected in EDTA-containing tubes through a venous catheter placed in an antecubital vein for the determination of plasma glucose and insulin levels. Plasma glucose levels were measured enzymatically, whereas plasma insulin levels were measured by radioimmunoassay with polyethylene glycol separation.25,26 The total glucose and insulin areas under the curve during the oral glucose tolerance test were determined using the trapezoid method.

CARDIORESPIRATORY FITNESS

Cardiorespiratory fitness of each participant was assessed by a progressive submaximal physical working capacity (PWC) test performed on a cycle ergometer (Monark, Vansbro, Sweden). Heart rate was measured through a single electrocardiogram derivation and was recorded during 3 consecutive 6-minute workloads, each separated by a 1-minute rest. The test was designed to reach a target heart rate of 150 beats/min at the end of the last workload. The PWC150, which is the power output at 150 beats/min, was then calculated. To consider the individual differences in body weight, PWC150 was expressed as kilograms of body weight (PWC150/kg).

STATISTICAL ANALYSIS

Data are expressed as mean ± SD in the tables and as mean ± SE in the figures. Unpaired t tests were performed to compare men with high vs low CRF. One-way analyses of covariance using the general linear model with adjustment for age were performed to evaluate the effect of CRF on anthropometric and metabolic risk variables. Stepwise multiple regression analyses were computed to sort out the independent contribution of anthropometric and body composition variables to the variance of CRF. The 50th percentile for PWC150/kg in the present study sample corresponded to a value of 10.7 kiloponds/min (kpm) per kilogram. Therefore, subjects with a PWC150/kg of 10.7 kpm/kg or less were defined as being unfit (low CRF), and subjects with a PWC150/kg of greater than 10.7 kpm/kg were defined as being fit (high CRF). Finally, the logistic regression analysis was performed using CRF and visceral AT accumulation to predict the presence of the atherogenic metabolic triad. All statistical analyses were performed using commercially available software (SAS version 8.02; SAS Institute, Cary, North Carolina).

Anthropometric measurements and metabolic profiles of the sample of 169 men (mean ± SD BMI, 25.9 ± 4.4; and mean ± SD age, 37.1 ± 14.0 years), classified into tertiles of CRF (PWC150/kg), are given in Table 1. Because men in the low tertile tended to be older, the reported P values are those obtained after adjustment for age. Adiposity indexes decreased across tertiles of CRF, with visceral AT accumulation being lowest among men with thehighest CRF (P < .001). Accordingly, men in the high CRF tertile had overall better metabolic risk profiles compared with men in the low CRF tertile. For instance, glucose and insulin areas under the curve determined during the oral glucose tolerance test were smallest among men with high CRF (P < .001). Overall, plasma lipoprotein-lipid profiles were more favorable among men with high CRF compared with men with low CRF. Subjects in the high CRF tertile were also characterized by highest FFM (P < .001). Multiple linear regression analyses were performed and revealed that the best predictors of CRF were age, FFM, and visceral AT accumulation (data not shown). The correlation coefficient between BMI and CRF was −0.22 (P = .004) and was not significant after statistical adjustment for visceral AT accumulation (P = .119), whereas the correlation coefficient between visceral AT accumulation and CRF was −0.42 (P < .001) and was unaffected by controlling for BMI.

Table Graphic Jump LocationTable 1. Anthropometric and Metabolic Characteristics Among 169 Men in the Study a

To control for the decreased adiposity observed in subjects with high CRF, men were then individually matched on the basis of their BMI (within a 1.0 variation) but with high CRF or low CRF. Anthropometric measurements and metabolic profiles of men matched for BMI but with high vs low CRF are given in Table 2 and in Figure 1 and Figure 2. When subjects were matched for BMI, men with low CRF were older and had more visceral AT accumulation than men with high CRF (P < .007) (Table 2). Men with low CRF were characterized by elevated triglyceride and apolipoprotein B levels and by an increased total cholesterol–high-density lipoprotein cholesterol ratio compared with men with high CRF (Figure 1) (P ≤ .02). Figure 2 shows that the plasma glucose (P < .010) and insulin (P = .052) responses to the 75-g oral glucose challenge were higher in subjects with low CRF. Subjects were then matched according to their visceral AT accumulation (within a 5.0-cm2 variation). Results given in Table 2 and in Figures 1 and 2 show that subjects with high vs low CRF matched for visceral AT accumulation no longer differed in their plasma lipoprotein-lipid profile and indexes of plasma glucose-insulin homeostasis. Such lack of difference in the cardiometabolic risk profile was observed despite the fact that men with low CRF had a lower FFM than men with high CRF.

Place holder to copy figure label and caption
Figure 1.

Variables of the plasma lipoprotein-lipid profile among men individually matched for body mass index (BMI) (calculated as weight in kilograms divided by height in meters squared) (A) or for visceral adipose tissue (AT) accumulation (B) with high or low levels of cardiorespiratory fitness (CRF) (> 10.7 or ≤ 10.7 kiloponds/minute/kilogram). When men with high vs low CRF were matched on the basis of BMI, men with low CRF were characterized by elevated triglyceride and apolipoprotein B levels and by an increased total cholesterol–high-density lipoprotein (HDL) cholesterol ratio compared with men with high CRF, but when men with high vs low CRF were matched on the basis of visceral AT accumulation, these differences were no longer observed. To determine the SI conversion factor for apolipoprotein B to grams per liter, multiply by 0.01; for triglycerides to millimoles per liter, multiply by 0.0113. Values in the bars are given as mean ± SE.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Area under the curve (AUC) of plasma glucose and insulin levels measured during a 75-g oral glucose tolerance test among men individually matched for body mass index (BMI) (calculated as weight in kilograms divided by height in meters squared) (A) or for visceral adipose tissue (AT) accumulation (B) with high (open circle) or low (solid circle) levels of cardiorespiratory fitness (CRF) (> 10.7 or ≤ 10.7 kiloponds/minute/kilogram). A, When men with high vs low CRF were matched on the basis of BMI, men with low CRF were characterized by larger glucose and insulin AUCs compared with men with high CRF. B, When men with high vs low CRF were matched on the basis of visceral AT accumulation, these differences were no longer observed. To convert glucose to millimoles per liter, multiply by 0.0555; insulin to picomoles per liter, multiply by 6.945. The open bars indicate the AUC of the open circles; the solid bars, the AUC of the solid circles.

Graphic Jump Location
Table Graphic Jump LocationTable 2. Anthropometric Characteristics of Men Matched on the Basis of Body Mass Index (BMI) or Visceral Adipose Tissue (AT) Accumulation With High vs Low Cardiorespiratory Fitness (CRF) a

Finally, to further explore the respective contributions of visceral AT accumulation and CRF to the metabolic risk profile, subjects were classified according to visceral AT accumulation (≤ 130 or > 130 cm2) as previously suggested27 and CRF (> 10.7 or ≤ 10.7 kpm/kg) (Figure 3). Because the presence of the atherogenic metabolic triad (defined by the simultaneous presence of hyperinsulinemia, hyperapolipoprotein B, and small LDL particles) has been reported to be predictive of increased CHD risk,28 the proportions of carriers of 2 or 3 features of this atherogenic metabolic triad were calculated in the 4 subgroups studied. To identify men carrying the atherogenic metabolic triad, previously published cutoff values for fasting insulin and apolipoprotein B levels and LDL peak particle diameter were used and corresponded to 7.0 μIU/mL, 96 mg/dL, and 255.5 Å, respectively.29 The proportion of carriers of 2 or more features of the atherogenic metabolic triad was largely dependent on visceral AT accumulation irrespective of CRF, with prevalences reaching 37.5% (for high CRF) and 35.0% (for low CRF) among individuals with less visceral AT accumulation, whereas the prevalences were substantially increased among men with more visceral AT accumulation irrespective of their fitness level (80.0% for high CRF and 85.3% low CRF).

Place holder to copy figure label and caption
Figure 3.

Proportion of carriers of 2 to 3 features of the atherogenic metabolic triad among men classified according to more or less visceral adipose tissue (AT) accumulation (> 130 or ≤ 130 cm2) with high or low levels of cardiorespiratory fitness (CRF) (> 10.7 or ≤ 10.7 kiloponds/minute/kilogram). Men with more visceral AT accumulation were more likely to carry 2 to 3 features of the atherogenic metabolic triad compared with men with less visceral AT accumulation, irrespective of their CRF level (high vs low). 1.2 indicates that the corresponding subgroup is significantly different from subgroups 1 and 2.

Graphic Jump Location

Results of the present study are consistent with the established theory that middle-aged men with low CRF are more likely to have a less favorable anthropometric and metabolic risk profile than men with high CRF. However, to the best of our knowledge, this study is the first to show that the poor metabolic risk profile of men with low CRF is associated with more visceral AT accumulation even after controlling for BMI. Although men with low CRF were older, adjustment for age failed to eliminate differences in the metabolic risk profile related to visceral AT accumulation. Moreover, after controlling for visceral AT accumulation, the prevalence of carriers of the atherogenic metabolic triad (predictive of an increased CHD risk28,29) was similar among men with high and low CRF. The presence of the atherogenic metabolic triad of nontraditional risk markers, which includes hyperinsulinemia, hyperapolipoprotein B, and small LDL particles, has been shown to increase the risk of CHD by more than 20-fold even after controlling for traditional risk factors and lipid variables.28

It is recognized that visceral obesity is a better correlate of insulin resistance and of an atherogenic plasma lipoprotein-lipid profile than total body fat.30 Katzmarzyk et al6 suggest that elevated CRF diminishes the risk of all-cause and cardiovascular deaths associated with the metabolic syndrome, regardless of BMI. Accordingly, LaMonte et al31 note that low CRF is an independent predictor of incident metabolic syndrome in men and women, independent of age and BMI, supporting the notion that fat and fit individuals could be protected against the development of metabolic abnormalities that increase CHD risk. Although the present study was cross-sectional in design and had a limited sample size, we observed that low CRF was associated with a poor metabolic risk profile among subjects matched for BMI, which is consistent with the results of Katzmarzyk et al6 and of LaMonte et al.31 However, in the present study, men with low CRF were also characterized by more visceral AT accumulation than men with high CRF, despite no difference in BMI. Because the excess visceral AT accumulation was a condition likely to explain the altered metabolic risk profile of men with low CRF, further analyses were performed to control for this potentially confounding factor. Because differences in the metabolic risk profile were no longer significant after matching men with high vs low CRF for visceral AT accumulation, these results support the idea that the greater amount of visceral AT accumulation observed in men with low CRF (when matched for BMI) could be a key factor associated with the metabolic deteriorations associated with low CRF. However, prospective studies with measurement of CRF, visceral AT accumulation, and hard end points will be needed to further sort out the respective contributions of visceral adiposity and CRF to cardiometabolic risk. Nevertheless, our results suggest that visceral AT accumulation could be a key confounding factor when the relationship of CRF, CHD risk, and metabolic syndrome is examined. Results of the present study are consistent with those of Wong et al,32 who reported differences in visceral AT accumulation among subjects with low vs high CRF in a sample of men slightly older than the men in the present study. In the present study, the fact that subjects with low CRF had almost twice as much visceral fat accumulation as subjects with high CRF supports this theory. Christou et al33 suggest that aerobic fitness is not as important as body fatness in explaining individual differences in the cardiovascular risk profile associated with fitness. In that study, the potential associations between fitness, fatness, and metabolic risk markers were evaluated using multiple linear regression analyses with maximal oxygen uptake and waist circumference as respective indexes of aerobic fitness and abdominal AT accumulation. The authors concluded that body fatness was a stronger predictor of cardiovascular risk markers than aerobic fitness.

The fact that endurance exercise training is associated with a preferential mobilization of visceral AT79 suggests that regular exercise may have metabolic benefits even in the absence of body weight loss. In addition, metabolic (and possibly cardiovascular) benefits can be observed without improvement in CRF because regular exercise is associated with increased energy expenditure that in turn promotes negative energy balance and prevents the development of visceral obesity and the associated “dysmetabolic” profile. Although physical activity intensity is associated with energy expenditure,34 our findings suggest that from a clinical standpoint the emphasis should be placed first on the volume of physical activity, to promote mobilization of visceral AT through increased energy expenditure. In addition to increased visceral adiposity, sedentary older populations are generally characterized by lower FFM. Accordingly, we found that men in the low CRF tertile had significantly lower FFM than subjects in the high CRF tertile. However, when men with low vs high CRF matched for visceral adiposity were compared, differences in the metabolic risk profile were no longer observed, despite the fact that men with low CRF tended to have lower FFM than men with high CRF. These results do not exclude an important role for reduced FFM, especially among older populations. In the present study, which included young to middle-aged adult men, visceral AT accumulation seemed to be a more important correlate of the metabolic risk profile than FFM.

Physical fitness was assessed in our study using a submaximal test rather than by the measurement of maximal oxygen uptake. It has been demonstrated that this submaximal test could discriminate highly fit from poorly fit individuals.35 Submaximal test results are associated with maximal oxygen uptake, and this test has the advantage of not requiring a maximal effort to classify subjects by fitness level, at lower cost and greater safety than maximal oxygen uptake tests.36

Our sample included young to middle-aged men of white race/ethnicity. Therefore, we cannot extend these findings to women or to older men, who tend to have a greater visceral AT accumulation as they advance in age.37,38 In this regard, prospective studies are needed to evaluate the true relationship between sex, age, CRF, body composition, visceral AT accumulation, and the cardiometabolic risk profile. It would also be relevant to verify whether the protective effect of high physical fitness against the development of the metabolic syndrome is mediated by the maintenance of a low level of visceral AT accumulation.

Results of the present study suggest that the presence of excess visceral adiposity observed in men with low CRF is an important factor associated with their diabetogenic and atherogenic metabolic risk profile. This conclusion was reached at any BMI value studied. This finding supports the notion that visceral obesity is a major correlate of a metabolic risk factor profile that predicts the development of cardiovascular disease and type 2 diabetes mellitus resulting from poor CRF. Although CRF was not the best independent predictor of the metabolic risk profile, physical activity should be promoted irrespective of sex, age, and degree of obesity as a measure to reduce adiposity, increase energy expenditure, and potentially decrease atherogenic visceral AT mass.

Correspondence: Jean-Pierre Després, PhD, FAHA, Hôpital Laval Research Centre, Hôpital Laval, 2725 Chemin Ste-Foy, Pavilion Marguerite-D’Youville, Fourth Floor, Québec, QC G1V 4G5, Canada (jean-pierre.despres@crhl.ulaval.ca).

Accepted for Publication: February 24, 2007.

Author Contributions: Mr Arsenault and Drs Lemieux, Bouchard, and Després had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Tremblay, Bouchard, Pérusse, and Després. Acquisition of data: Arsenault, Lemieux, Alméras, and Després. Analysis and interpretation of data: Arsenault, Lachance, Lemieux, and Després. Drafting of the manuscript: Arsenault and Lachance. Critical revision of the manuscript for important intellectual content: Lemieux, Alméras, Tremblay, Bouchard, Pérusse, and Després. Statistical analysis: Arsenault, Lachance, Lemieux, and Després. Obtained funding: Tremblay, Bouchard, Pérusse, and Després. Study supervision: Tremblay, Bouchard, Pérusse, and Després.

Financial Disclosure: Dr Tremblay is supported in part by the Canada Research Chair in Physical Activity, Nutrition and Energy Balance. Dr Bouchard is supported in part by the George A. Bray Chair in Nutrition at Louisiana State University. Dr Després is scientific director of the International Chair on Cardiometabolic Risk, which is supported by an unrestricted grant to Université Laval by Sanofi Aventis.

Funding/Support: The Québec Family Study was supported by multiple grants from the Medical Research Council of Canada (now the Canadian Institutes of Health Research) and by the Canadian Diabetes Association.

Role of the Sponsor: The sponsors did not participate in the design or conduct of the study; collection, management, analysis, or interpretation of the data; or preparation, review, or approval of the manuscript.

Additional Contributions: Guy Fournier, BSc, Lucie Allard, BSc, Germain Thériault, MD, and Claude Leblanc, MSc, provided assistance in the collection of the data and contributed to the study. We thank the subjects for their excellent collaboration and the staff of the Hôpital Laval Research Centre.

Després  JP Is visceral obesity the cause of the metabolic syndrome? Ann Med 2006;38 (1) 52- 63
PubMed Link to Article
Eckel  RHGrundy  SMZimmet  PZ The metabolic syndrome. Lancet 2005;365 (9468) 1415- 1428
PubMed Link to Article
Poirier  PGiles  TDBray  GA  et al.  Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation 2006;113 (6) 898- 918doi: 10.1161/CIRCULATIONAHA.106.171016[published online ahead of print December27 2005;
PubMed Link to Article
Després  JPLamarche  B Low-intensity endurance exercise training, plasma lipoproteins and the risk of coronary heart disease. J Intern Med 1994;236 (1) 7- 22
PubMed Link to Article
Kraus  WEHoumard  JADuscha  BD  et al.  Effects of the amount and intensity of exercise on plasma lipoproteins. N Engl J Med 2002;347 (19) 1483- 1492
PubMed Link to Article
Katzmarzyk  PTChurch  TSBlair  SN Cardiorespiratory fitness attenuates the effects of the metabolic syndrome on all-cause and cardiovascular disease mortality in men. Arch Intern Med 2004;164 (10) 1092- 1097
PubMed Link to Article
Lynch  NANicklas  BJBerman  DMDennis  KEGoldberg  AP Reductions in visceral fat during weight loss and walking are associated with improvements in VO2 maxJ Appl Physiol 2001;90 (1) 99- 104
PubMed
Paré  ADumont  MLemieux  I  et al.  Is the relationship between adipose tissue and waist girth altered by weight loss in obese men? Obes Res 2001;9 (9) 526- 534
PubMed Link to Article
Ross  RDagnone  DJones  PJ  et al.  Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men: a randomized, controlled trial. Ann Intern Med 2000;133 (2) 92- 103
PubMed Link to Article
Major  GCPiché  MEBergeron  JWeisnagel  SJNadeau  ALemieux  S Energy expenditure from physical activity and the metabolic risk profile at menopause. Med Sci Sports Exerc 2005;37 (2) 204- 212
PubMed Link to Article
Lamarche  BDesprés  JPPouliot  MC  et al.  Is body fat loss a determinant factor in the improvement of carbohydrate and lipid metabolism following aerobic exercise training in obese women? Metabolism 1992;41 (11) 1249- 1256
PubMed Link to Article
Lee  CDBlair  SNJackson  AS Cardiorespiratory fitness, body composition, and all-cause and cardiovascular disease mortality in men. Am J Clin Nutr 1999;69 (3) 373- 380
PubMed
Blair  SNKampert  JBKohl  HW  III  et al.  Influences of cardiorespiratory fitness and other precursors on cardiovascular disease and all-cause mortality in men and women. JAMA 1996;276 (3) 205- 210
PubMed Link to Article
Blair  SNKohl  HW  IIIPaffenbarger  RS  JrClark  DGCooper  KHGibbons  LW Physical fitness and all-cause mortality: a prospective study of healthy men and women. JAMA 1989;262 (17) 2395- 2401
PubMed Link to Article
Wei  MGibbons  LWMitchell  TLKampert  JBLee  CDBlair  SN The association between cardiorespiratory fitness and impaired fasting glucose and type 2 diabetes mellitus in men. Ann Intern Med 1999;130 (2) 89- 96[published correction appears in Ann Intern Med. 1999;131 ((5)) 394
PubMed Link to Article
Rice  TPérusse  LBouchard  CRao  DC Familial clustering of abdominal visceral fat and total fat mass: the Québec Family Study. Obes Res 1996;4 (3) 253- 261
PubMed Link to Article
Lohman  TedRoche  AedMartorel  Red The Airlie (VA) Consensus Conference: Standardization of Anthropometric Measurements.  Champaign, IL Human Kinetics Publishers1988;39- 80
van der Kooy  KLeenen  RSeidell  JCDeurenberg  PVisser  M Abdominal diameters as indicators of visceral fat: comparison between magnetic resonance imaging and anthropometry. Br J Nutr 1993;70 (1) 47- 58
PubMed Link to Article
Ferland  MDesprés  JPTremblay  A  et al.  Assessment of adipose tissue distribution by computed axial tomography in obese women: association with body density and anthropometric measurements. Br J Nutr 1989;61 (2) 139- 148
PubMed Link to Article
Siri  WE The gross composition of the body. Adv Biol Med Phys 1956;4239- 280
PubMed
Havel  RJEder  HABragdon  JH The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest 1955;34 (9) 1345- 1353
PubMed Link to Article
Burstein  MSamaille  J On a rapid determination of the cholesterol bound to the serum α- and β-lipoproteins [in French]. Clin Chim Acta 1960;5609
PubMed Link to Article
Laurell  CB Quantitative estimation of proteins by electrophoresis in agarose gel containing antibodies. Anal Biochem 1966;15 (1) 45- 52
PubMed Link to Article
St-Pierre  ACRuel  ILCantin  B  et al.  Comparison of various electrophoretic characteristics of LDL particles and their relationship to the risk of ischemic heart disease. Circulation 2001;104 (19) 2295- 2299
PubMed Link to Article
Richterich  RDauwalder  H Determination of plasma glucose by hexokinase-glucose-6-phosphate dehydrogenase method [in German]. Schweiz Med Wochenschr 1971;101 (17) 615- 618
PubMed
Desbuquois  BAurbach  GD Use of polyethylene glycol to separate free and antibody-bound peptide hormones in radioimmunoassays. J Clin Endocrinol Metab 1971;33 (5) 732- 738
PubMed Link to Article
Després  JPLamarche  B Effects of diet and physical activity on adiposity and body fat distribution: implications for the prevention of cardiovascular disease. Nutr Res Rev 1993;6137- 159
Link to Article
Lamarche  BTchernof  AMauriège  P  et al.  Fasting insulin and apolipoprotein B levels and low-density lipoprotein particle size as risk factors for ischemic heart disease. JAMA 1998;279 (24) 1955- 1961
PubMed Link to Article
Lemieux  IPascot  ACouillard  C  et al.  Hypertriglyceridemic waist: a marker of the atherogenic metabolic triad (hyperinsulinemia; hyperapolipoprotein B; small, dense LDL) in men? Circulation 2000;102 (2) 179- 184
PubMed Link to Article
Després  JP Health consequences of visceral obesity. Ann Med 2001;33 (8) 534- 541
PubMed Link to Article
LaMonte  MJBarlow  CEJurca  RKampert  JBChurch  TSBlair  SN Cardiorespiratory fitness is inversely associated with the incidence of metabolic syndrome: a prospective study of men and women. Circulation 2005;112 (4) 505- 512
PubMed Link to Article
Wong  SLKatzmarzyk  PNichaman  MZChurch  TSBlair  SNRoss  R Cardiorespiratory fitness is associated with lower abdominal fat independent of body mass index. Med Sci Sports Exerc 2004;36 (2) 286- 291
PubMed Link to Article
Christou  DDGentile  CLDeSouza  CASeals  DRGates  PE Fatness is a better predictor of cardiovascular disease risk factor profile than aerobic fitness in healthy men. Circulation 2005;111 (15) 1904- 1914
PubMed Link to Article
Yoshioka  MDoucet  ESt-Pierre  S  et al.  Impact of high-intensity exercise on energy expenditure, lipid oxidation and body fatness. Int J Obes Relat Metab Disord 2001;25 (3) 332- 339
PubMed Link to Article
Shephard  RJBouchard  C Principal components of fitness: relationship to physical activity and lifestyle. Can J Appl Physiol 1994;19 (2) 200- 214
PubMed Link to Article
Gore  CJBooth  MLBauman  AOwen  N Utility of pwc75% as an estimate of aerobic power in epidemiological and population-based studies. Med Sci Sports Exerc 1999;31 (2) 348- 351
PubMed Link to Article
Lemieux  SPrud’homme  DMoorjani  S  et al.  Do elevated levels of abdominal visceral adipose tissue contribute to age-related differences in plasma lipoprotein concentrations in men? Atherosclerosis 1995;118 (1) 155- 164
PubMed Link to Article
Lemieux  SPrud’homme  DBouchard  CTremblay  ADesprés  JP Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr 1993;58 (4) 463- 467
PubMed

Figures

Place holder to copy figure label and caption
Figure 1.

Variables of the plasma lipoprotein-lipid profile among men individually matched for body mass index (BMI) (calculated as weight in kilograms divided by height in meters squared) (A) or for visceral adipose tissue (AT) accumulation (B) with high or low levels of cardiorespiratory fitness (CRF) (> 10.7 or ≤ 10.7 kiloponds/minute/kilogram). When men with high vs low CRF were matched on the basis of BMI, men with low CRF were characterized by elevated triglyceride and apolipoprotein B levels and by an increased total cholesterol–high-density lipoprotein (HDL) cholesterol ratio compared with men with high CRF, but when men with high vs low CRF were matched on the basis of visceral AT accumulation, these differences were no longer observed. To determine the SI conversion factor for apolipoprotein B to grams per liter, multiply by 0.01; for triglycerides to millimoles per liter, multiply by 0.0113. Values in the bars are given as mean ± SE.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Area under the curve (AUC) of plasma glucose and insulin levels measured during a 75-g oral glucose tolerance test among men individually matched for body mass index (BMI) (calculated as weight in kilograms divided by height in meters squared) (A) or for visceral adipose tissue (AT) accumulation (B) with high (open circle) or low (solid circle) levels of cardiorespiratory fitness (CRF) (> 10.7 or ≤ 10.7 kiloponds/minute/kilogram). A, When men with high vs low CRF were matched on the basis of BMI, men with low CRF were characterized by larger glucose and insulin AUCs compared with men with high CRF. B, When men with high vs low CRF were matched on the basis of visceral AT accumulation, these differences were no longer observed. To convert glucose to millimoles per liter, multiply by 0.0555; insulin to picomoles per liter, multiply by 6.945. The open bars indicate the AUC of the open circles; the solid bars, the AUC of the solid circles.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Proportion of carriers of 2 to 3 features of the atherogenic metabolic triad among men classified according to more or less visceral adipose tissue (AT) accumulation (> 130 or ≤ 130 cm2) with high or low levels of cardiorespiratory fitness (CRF) (> 10.7 or ≤ 10.7 kiloponds/minute/kilogram). Men with more visceral AT accumulation were more likely to carry 2 to 3 features of the atherogenic metabolic triad compared with men with less visceral AT accumulation, irrespective of their CRF level (high vs low). 1.2 indicates that the corresponding subgroup is significantly different from subgroups 1 and 2.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Anthropometric and Metabolic Characteristics Among 169 Men in the Study a
Table Graphic Jump LocationTable 2. Anthropometric Characteristics of Men Matched on the Basis of Body Mass Index (BMI) or Visceral Adipose Tissue (AT) Accumulation With High vs Low Cardiorespiratory Fitness (CRF) a

References

Després  JP Is visceral obesity the cause of the metabolic syndrome? Ann Med 2006;38 (1) 52- 63
PubMed Link to Article
Eckel  RHGrundy  SMZimmet  PZ The metabolic syndrome. Lancet 2005;365 (9468) 1415- 1428
PubMed Link to Article
Poirier  PGiles  TDBray  GA  et al.  Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation 2006;113 (6) 898- 918doi: 10.1161/CIRCULATIONAHA.106.171016[published online ahead of print December27 2005;
PubMed Link to Article
Després  JPLamarche  B Low-intensity endurance exercise training, plasma lipoproteins and the risk of coronary heart disease. J Intern Med 1994;236 (1) 7- 22
PubMed Link to Article
Kraus  WEHoumard  JADuscha  BD  et al.  Effects of the amount and intensity of exercise on plasma lipoproteins. N Engl J Med 2002;347 (19) 1483- 1492
PubMed Link to Article
Katzmarzyk  PTChurch  TSBlair  SN Cardiorespiratory fitness attenuates the effects of the metabolic syndrome on all-cause and cardiovascular disease mortality in men. Arch Intern Med 2004;164 (10) 1092- 1097
PubMed Link to Article
Lynch  NANicklas  BJBerman  DMDennis  KEGoldberg  AP Reductions in visceral fat during weight loss and walking are associated with improvements in VO2 maxJ Appl Physiol 2001;90 (1) 99- 104
PubMed
Paré  ADumont  MLemieux  I  et al.  Is the relationship between adipose tissue and waist girth altered by weight loss in obese men? Obes Res 2001;9 (9) 526- 534
PubMed Link to Article
Ross  RDagnone  DJones  PJ  et al.  Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men: a randomized, controlled trial. Ann Intern Med 2000;133 (2) 92- 103
PubMed Link to Article
Major  GCPiché  MEBergeron  JWeisnagel  SJNadeau  ALemieux  S Energy expenditure from physical activity and the metabolic risk profile at menopause. Med Sci Sports Exerc 2005;37 (2) 204- 212
PubMed Link to Article
Lamarche  BDesprés  JPPouliot  MC  et al.  Is body fat loss a determinant factor in the improvement of carbohydrate and lipid metabolism following aerobic exercise training in obese women? Metabolism 1992;41 (11) 1249- 1256
PubMed Link to Article
Lee  CDBlair  SNJackson  AS Cardiorespiratory fitness, body composition, and all-cause and cardiovascular disease mortality in men. Am J Clin Nutr 1999;69 (3) 373- 380
PubMed
Blair  SNKampert  JBKohl  HW  III  et al.  Influences of cardiorespiratory fitness and other precursors on cardiovascular disease and all-cause mortality in men and women. JAMA 1996;276 (3) 205- 210
PubMed Link to Article
Blair  SNKohl  HW  IIIPaffenbarger  RS  JrClark  DGCooper  KHGibbons  LW Physical fitness and all-cause mortality: a prospective study of healthy men and women. JAMA 1989;262 (17) 2395- 2401
PubMed Link to Article
Wei  MGibbons  LWMitchell  TLKampert  JBLee  CDBlair  SN The association between cardiorespiratory fitness and impaired fasting glucose and type 2 diabetes mellitus in men. Ann Intern Med 1999;130 (2) 89- 96[published correction appears in Ann Intern Med. 1999;131 ((5)) 394
PubMed Link to Article
Rice  TPérusse  LBouchard  CRao  DC Familial clustering of abdominal visceral fat and total fat mass: the Québec Family Study. Obes Res 1996;4 (3) 253- 261
PubMed Link to Article
Lohman  TedRoche  AedMartorel  Red The Airlie (VA) Consensus Conference: Standardization of Anthropometric Measurements.  Champaign, IL Human Kinetics Publishers1988;39- 80
van der Kooy  KLeenen  RSeidell  JCDeurenberg  PVisser  M Abdominal diameters as indicators of visceral fat: comparison between magnetic resonance imaging and anthropometry. Br J Nutr 1993;70 (1) 47- 58
PubMed Link to Article
Ferland  MDesprés  JPTremblay  A  et al.  Assessment of adipose tissue distribution by computed axial tomography in obese women: association with body density and anthropometric measurements. Br J Nutr 1989;61 (2) 139- 148
PubMed Link to Article
Siri  WE The gross composition of the body. Adv Biol Med Phys 1956;4239- 280
PubMed
Havel  RJEder  HABragdon  JH The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest 1955;34 (9) 1345- 1353
PubMed Link to Article
Burstein  MSamaille  J On a rapid determination of the cholesterol bound to the serum α- and β-lipoproteins [in French]. Clin Chim Acta 1960;5609
PubMed Link to Article
Laurell  CB Quantitative estimation of proteins by electrophoresis in agarose gel containing antibodies. Anal Biochem 1966;15 (1) 45- 52
PubMed Link to Article
St-Pierre  ACRuel  ILCantin  B  et al.  Comparison of various electrophoretic characteristics of LDL particles and their relationship to the risk of ischemic heart disease. Circulation 2001;104 (19) 2295- 2299
PubMed Link to Article
Richterich  RDauwalder  H Determination of plasma glucose by hexokinase-glucose-6-phosphate dehydrogenase method [in German]. Schweiz Med Wochenschr 1971;101 (17) 615- 618
PubMed
Desbuquois  BAurbach  GD Use of polyethylene glycol to separate free and antibody-bound peptide hormones in radioimmunoassays. J Clin Endocrinol Metab 1971;33 (5) 732- 738
PubMed Link to Article
Després  JPLamarche  B Effects of diet and physical activity on adiposity and body fat distribution: implications for the prevention of cardiovascular disease. Nutr Res Rev 1993;6137- 159
Link to Article
Lamarche  BTchernof  AMauriège  P  et al.  Fasting insulin and apolipoprotein B levels and low-density lipoprotein particle size as risk factors for ischemic heart disease. JAMA 1998;279 (24) 1955- 1961
PubMed Link to Article
Lemieux  IPascot  ACouillard  C  et al.  Hypertriglyceridemic waist: a marker of the atherogenic metabolic triad (hyperinsulinemia; hyperapolipoprotein B; small, dense LDL) in men? Circulation 2000;102 (2) 179- 184
PubMed Link to Article
Després  JP Health consequences of visceral obesity. Ann Med 2001;33 (8) 534- 541
PubMed Link to Article
LaMonte  MJBarlow  CEJurca  RKampert  JBChurch  TSBlair  SN Cardiorespiratory fitness is inversely associated with the incidence of metabolic syndrome: a prospective study of men and women. Circulation 2005;112 (4) 505- 512
PubMed Link to Article
Wong  SLKatzmarzyk  PNichaman  MZChurch  TSBlair  SNRoss  R Cardiorespiratory fitness is associated with lower abdominal fat independent of body mass index. Med Sci Sports Exerc 2004;36 (2) 286- 291
PubMed Link to Article
Christou  DDGentile  CLDeSouza  CASeals  DRGates  PE Fatness is a better predictor of cardiovascular disease risk factor profile than aerobic fitness in healthy men. Circulation 2005;111 (15) 1904- 1914
PubMed Link to Article
Yoshioka  MDoucet  ESt-Pierre  S  et al.  Impact of high-intensity exercise on energy expenditure, lipid oxidation and body fatness. Int J Obes Relat Metab Disord 2001;25 (3) 332- 339
PubMed Link to Article
Shephard  RJBouchard  C Principal components of fitness: relationship to physical activity and lifestyle. Can J Appl Physiol 1994;19 (2) 200- 214
PubMed Link to Article
Gore  CJBooth  MLBauman  AOwen  N Utility of pwc75% as an estimate of aerobic power in epidemiological and population-based studies. Med Sci Sports Exerc 1999;31 (2) 348- 351
PubMed Link to Article
Lemieux  SPrud’homme  DMoorjani  S  et al.  Do elevated levels of abdominal visceral adipose tissue contribute to age-related differences in plasma lipoprotein concentrations in men? Atherosclerosis 1995;118 (1) 155- 164
PubMed Link to Article
Lemieux  SPrud’homme  DBouchard  CTremblay  ADesprés  JP Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr 1993;58 (4) 463- 467
PubMed

Correspondence

CME
Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
Submit a Comment

Multimedia

Some tools below are only available to our subscribers or users with an online account.

Web of Science® Times Cited: 49

Related Content

Customize your page view by dragging & repositioning the boxes below.

Articles Related By Topic
Related Collections
PubMed Articles
JAMAevidence.com

The Rational Clinical Examination EDUCATION GUIDES
Abdominal Aortic Aneurysm