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ARTICLE Interrelationships between changes in anthropometric variables and computed tomography indices of abdominal fat distribution in response to a 1-year physical activity–healthy eating lifestyle modification program in abdominally obese men Nicole Villeneuve, Emilie Pelletier-Beaumont, Julie-Anne Nazare, Isabelle Lemieux, Natalie Alméras, Jean Bergeron, Angelo Tremblay, Paul Poirier, and Jean-Pierre Després

Abstract: The objectives were to (i) measure the effects of a 1-year lifestyle modification program on body fat distribution/ anthropometric variables; (ii) determine the interrelationships between changes in all these variables; and (iii) investigate whether there is a selective reduction in deep (DSAT) vs. superficial subcutaneous adipose tissue (SSAT) at the abdominal level following a 1-year lifestyle modification program. Anthropometric variables, body composition and abdominal and midthigh fat distribution were assessed at baseline and after 1 year in 109 sedentary, dyslipidemic and abdominally obese men. Reductions in anthropometric variables, skinfold thicknesses (except the trunk/extremity ratio) and fat mass as well as an increase in fat-free mass were observed after 1 year (p < 0.0001). Decreases in abdominal adipose tissue volumes were also noted (–23%, –26%, –18%, –19%, –17%, p < 0.0001 for total adipose tissue, visceral adipose tissue, subcutaneous adipose tissue, DSAT and SSAT, respectively). Adipose tissue areas at midthigh also decreased (–18%, –18%, –17%, p < 0.0001 for total, deep, and subcutaneous adipose tissue, respectively). A reduction (–9%, p < 0.0001) in low-attenuation muscle area and an increase (+1%, p < 0.05) in normal-attenuation muscle area were also observed. There was a positive relationship between changes in visceral adipose tissue and changes in DSAT (r = 0.65, p < 0.0001) or SSAT (r = 0.63, p < 0.0001). Although absolute changes in DSAT were greater than changes in SSAT, relative changes in both depots were similar, independent of changes in visceral adipose tissue. The 1-year lifestyle modification program therefore improved the body fat distribution pattern and midthigh muscle quality in abdominally obese men. Key words: anthropometry, exercise, muscle quality, nutrition, subcutaneous adipose tissue, visceral obesity. Résumé : Les objectifs étaient : (i) évaluer les effets d’une modification des habitudes de vie d’une durée d’un an sur différentes variables anthropométriques/de distribution du tissu adipeux; (ii) examiner les interrelations entre ces variables; et (iii) évaluer la possibilité d’observer une réduction sélective du tissu adipeux sous-cutané abdominal profond (TASCP) vs superficiel (TASCS) suite a` l’intervention. Les variables anthropométriques, de composition corporelle et de distribution du tissu adipeux (abdomen et mi-cuisse) ont été mesurées avant et après un an chez 109 hommes sédentaires et dyslipidémiques présentant une obésité abdominale. Des diminutions des variables anthropométriques, des mesures des plis cutanés (a` l’exception du rapport tronc/ extrémités) et de la masse grasse et une augmentation de la masse maigre (p < 0,0001) ont été remarquées. Des diminutions des volumes de tissu adipeux abdominal ont également été observées (–23 %, –26 %, –18 %, –19 %, –17 %, p < 0,0001 pour le tissu adipeux total, tissu adipeux viscéral, tissu adipeux sous-cutané, TASCP et TASCS, respectivement). De plus, les surfaces de tissu adipeux de la mi-cuisse ont diminué (–18 %, –18 %, –17 %, p < 0,0001 pour le tissu adipeux total, profond et sous-cutané, respectivement). Une réduction (–9 %, p < 0,0001) du muscle a` atténuation faible et une augmentation (+1 %, p < 0,05) du muscle a` atténuation normale ont aussi été remarquées. Une relation positive a été notée entre le changement de tissu adipeux viscéral et les changements de TASCP (r = 0,65, p < 0,0001) ou TASCS (r = 0,63, p < 0,0001). Par ailleurs, bien que les changements absolus du TASCP étaient plus grands que les changements du TASCS, les changements relatifs de ces deux dépôts étaient similaires indépendamment des changements de tissu adipeux viscéral. Des modifications des habitudes de vie d’une durée d’un an ont donc amélioré le patron de distribution du tissu adipeux ainsi que la qualité du tissu musculaire au niveau de la mi-cuisse chez des hommes avec une obésité abdominale. Mots-clés : anthropométrie, exercice, nutrition, obésité viscérale, qualité du muscle, tissu adipeux sous-cutané.

Received 19 June 2013. Accepted 7 December 2013. N. Villeneuve, E. Pelletier-Beaumont, N. Alméras, A. Tremblay,* and J.-P. Després. Centre de recherche de l’Institut universitaire de cardiologie et de pneumologie de Québec, Pavilion Marguerite-D’Youville, 2725 chemin Ste-Foy, Québec QC G1V 4G5, Canada; Department of Kinesiology, Faculty of Medicine, Université Laval, Québec, QC G1V 0A6, Canada. J.-A. Nazare and I. Lemieux. Centre de recherche de l’Institut universitaire de cardiologie et de pneumologie de Québec, Pavilion Marguerite-D’Youville, 2725 chemin Ste-Foy, Québec QC G1V 4G5, Canada. J. Bergeron. Lipid Research Center, CHUQ Research Center, Québec, QC G1V 4G2, Canada. P. Poirier. Centre de recherche de l’Institut universitaire de cardiologie et de pneumologie de Québec, Pavilion Marguerite-D’Youville, 2725 chemin Ste-Foy, Québec QC G1V 4G5, Canada; Faculty of Pharmacy, Université Laval, Québec, QC G1V 0A6, Canada. Corresponding author: Jean-Pierre Després (e-mail: [email protected]). *All editorial decisions for this paper were made by Robert Boushel and Terry Graham. Appl. Physiol. Nutr. Metab. 39: 503–511 (2014) dx.doi.org/10.1139/apnm-2013-0270

Published at www.nrcresearchpress.com/apnm on 16 December 2013.

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Table 1. Physical activity, cardiorespiratory fitness, diet, anthropometric and body composition variables of subjects at baseline and after the 1-year lifestyle modification program. 1-year changes

Baseline (N = 109)

1-year follow-up (N = 109)

Absolute

%

Age (y)

47.6±8.6

48.7±8.6

+1.12±0.07*

+2*

Physical activity and cardiorespiratory fitness Heart rate; 3.5 miles/h (5.6 km/h), 2% (beats/min) Exercise output at 150 beats/min (METs) Daily step count (no. of steps per day)

118±14 7.52±1.45 7546±2849

104±14 8.89±1.61 9624±3062

−13±11* +1.32±1.33* +1955±2735*

−11* +20* +36*

Reported dietary intake/composition Total energy (kcal/day) Carbohydrate (% of energy intake) Lipid (% of energy intake) Protein (% of energy intake)

3045±646 45.4±6.7 34.4±6.0 16.1±3.0

2476±520 47.5±6.3 30.3±5.5 19.1±2.8

−548±668* +1.77±7.28† −4.23±6.74* +2.91±3.45*

−16* +5† −10* +21*

Anthropometry Weight (kg) Body mass index (kg/m2) Waist circumference (cm) Hip circumference (cm) Waist-to-hip ratio Sagittal diameter (cm)

94.9±11.9 31.1±3.1 108.2±8.9 107.0±6.9 1.01±0.05 32.8±3.0

88.2±12.1 28.9±3.3 99.9±10.0 102.8±6.9 0.97±0.06 29.6±3.4

−6.68±4.64* −2.17±1.51* −8.47±5.30* −4.34±2.65* −0.04±0.04* −3.26±1.77*

−7* −7* −8* −4* −4* −10*

Skinfolds Trunk (mm) Extremity (mm) Trunk/extremity Sum of 6 (mm)

114.0±26.7 39.9±15.0 3.07±0.85 153.9±38.6

83.8±25.6 28.3±9.7 3.05±0.65 112.1±34.0

−31.3±20.9* −11.9±8.9* −0.02±0.63 −43.2±26.6*

−27* −28* +3 −27*

Body composition % Body fat Fat mass (kg) Fat-free mass (kg)

30.7±4.6 29.4±7.1 65.5±7.2

26.1±5.7 23.5±7.7 64.7±6.9

−4.58±3.26* −5.92±3.82* −0.76±1.73*

−15* −21* −1*

Note: Data are means ± SD. *p < 0.0001; †p < 0.05.

Introduction Overweight/obesity has been associated with increased cardiovascular morbidity and mortality (Manson et al. 1995; Willett et al. 1995). However, it is being more and more recognized that the location of body fat, particularly excess adipose tissue accumulation in the abdominal cavity (visceral adipose tissue (VAT)) and ectopic fat depots are of utmost importance in determining the health hazards of overweight and obesity (Cornier et al. 2011; Després et al. 1990; Després and Lemieux 2006; Després 2012). However, unlike VAT, the association between the amount of subcutaneous adipose tissue (SAT) and obesity-related metabolic complications are still under debate (Bays et al. 2010; Johnson et al. 2001; Porter et al. 2009). In addition, abdominal SAT can be further subdivided into superficial SAT (SSAT) and deep SAT (DSAT) and it has been proposed that these 2 depots could present distinct metabolic properties, with DSAT being potentially more closely associated with VAT than SSAT and with a deleterious cardiometabolic risk profile (Kelley et al. 2000; Ross et al. 2002a; Smith et al. 2001; Toth et al. 2001). On the other hand, glutealfemoral adipose tissue has even been suggested to provide protection against the development of insulin resistance, dyslipidemia, type 2 diabetes and cardiovascular disease (Okura et al. 2004; Pouliot et al. 1991; Snijder et al. 2004; Tanko et al. 2003; Van Pelt et al. 2002). Despite the evidence that VAT and other ectopic fat depots increase cardiometabolic risk (Després and Lemieux 2006), most lifestyle modification interventions have focused on weight loss rather than VAT reductions as the primary endpoints (Hallgreen and Hall 2008; Jakicic et al. 1999; Skender et al. 1996; Wadden et al. 1998). Lifestyle interventions that incorporate the restriction of caloric intake and (or) increased energy expenditure with exercise have been shown to reduce the amount of VAT, thereby improv-

ing the cardiometabolic risk profile (Hallgreen and Hall 2008). Serial quantification of VAT content/volume by computed tomography (CT) has shown that a healthy lifestyle intervention program positively affects VAT content (Borel et al. 2012; Paré et al. 2001; Ross et al. 2002b, 2004; Ross and Katzmarzyk 2003). However, less is known about the regional reduction of various specific body fat compartments, especially SSAT and DSAT in response to changes in lifestyle habits producing a negative energy balance. It is recognized that VAT and SAT depots present anatomical, cellular, molecular, physiological, clinical and prognostic differences (Ibrahim 2010). On the basis of anatomical and metabolic differences between VAT, SAT, DSAT, and SSAT, we hypothesized that there would be heterogeneous changes in these various adipose depots and differences in their interrelationships in response to a 1-year lifestyle modification program in a sample of viscerally obese men. Therefore, the main objectives of the present study were to (i) measure the effect of a 1-year lifestyle modification program on a comprehensive set of body fat distribution/anthropometric variables; (ii) determine which changes in anthropometric markers were more specifically associated with changes in VAT, SAT, DSAT and SSAT; and (iii) quantify specific changes in the 2 abdominal SAT (DSAT and SSAT) volumes in response to the lifestyle intervention program.

Materials and methods Subjects One hundred and forty-four men aged between 30 and 65 years and characterized by abdominal obesity (waist circumference ≥ 90 cm) and by an atherogenic dyslipidemia (triglycerides ≥ 1.69 mmol/L and (or) high-density lipoprotein cholesterol < 1.03 mmol/L) were recruited to participate in this lifestyle intervention study. Over 1 year, 27 men dropped out from the intervention and 8 additional Published by NRC Research Press

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Table 2. Abdominal and midthigh adipose tissue areas/volumes and muscle areas at baseline and after the 1-year lifestyle modification program. Baseline (N = 109)

1-year follow-up (N = 109)

1-year changes Absolute

%

L2−L3 — Abdominal adipose and muscle tissue areas (cm2) TAT 509.9±123.4 399.1±129.0 VAT 305.2±74.9 235.4±86.0 SAT 206.4±82.2 166.2±73.6 DSAT 109.6±52.6 82.3±44.2 SSAT 98.0±35.4 83.9±32.1 MT 184.8±21.9 180.6±20.9

−111.5±80.4* −71.1±53.2* −39.5±32.3* −25.7±21.6* −14.4±14.2* −4.34±7.86*

−23* −24* −19* −24* −14* −2*

L4−L5 — Abdominal adipose and muscle tissue areas (cm2) TAT 563.8±132.8 436.7±148.5 VAT 257.3±75.2 184.6±81.4 SAT 308.6±98.2 252.0±93.9 DSAT 212.5±72.2 175.9±69.4 SSAT 96.1±31.0 76.2±28.1 MT 181.2±20.5 177.1±20.1

−129.9±83.5* −72.7±51.6* −57.1±43.8* −36.8±34.4* −20.3±14.0* −4.38±7.69*

−24* −29* −19* −17* −21* −2*

Abdominal adipose tissue volumes (cm3) TAT 3720.7±886.9 VAT 1949.1±482.9 SAT 1782.1±635.8 DSAT 1119.9±433.1 SSAT 672.7±232.6

−825.0±557.0* −492.2±347.6* −328.2±262.0* −214.3±189.5* −118.8±89.3*

−23* −26* −18* −19* −17*

−38.4±26.0* −2.51±2.65* −35.9±24.0*

−18* −18* −17*

−4.46±11.9† −6.11±8.24* +2.95±11.3†

−1† −9* +1†

2903.6±930.3 1467.7±562.4 1452.1±571.2 895.8±387.2 556.3±201.1

Midthigh adipose and muscle tissue areas (cm2) Adipose tissue 223.9±69.6 188.1±72.6 TATth DATth 14.5±7.2 12.0±6.6 209.4±65.2 176.1±68.3 SATth Muscle tissue Total 346.6±35.2 341.9±35.2 Low-attenuation 65.8±17.1 59.9±18.3 Normal-attenuation 264.6±34.8 267.2±34.5

Note: Data are means ± SD. *p < 0.0001; †p < 0.05. DATth, deep adipose tissue at midthigh; DSAT, deep subcutaneous adipose tissue; SAT, subcutaneous adipose tissue; SATth, subcutaneous adipose tissue at midthigh; SSAT, superficial subcutaneous adipose tissue; TAT, total adipose tissue; TATth, total adipose tissue at midthigh; VAT, visceral adipose tissue.

individuals had missing data for CT. Therefore, analyses of the present study were conducted in 109 men for whom we had full baseline and 1-year anthropometry/body composition and fat distribution data. Subjects with type 2 diabetes, body mass index (BMI) values 40 kg/m2, or taking medication targeting blood glucose or lipid levels as well as blood pressure were excluded. Eligible participants were recruited through the media and were living in and around the Québec City metropolitan area. Informed written consent was obtained from all participants prior to their inclusion in the study, which had been approved by the local medical ethics committees of Université Laval and Institut universitaire de cardiologie et de pneumologie de Québec. Description of the intervention Subjects were individually counselled once every 2 weeks during the first 4 months of management with subsequent monthly visits to improve their nutritional and physical activity/exercise habits, as previously described (Borel et al. 2012; Nazare et al. 2013). Each visit included an interactive session with a registered nutritionist followed by a meeting with a kinesiologist. The nutritional counselling was adapted to elicit a 500-kcal daily energy deficit. The diet aimed at targeting a macronutrient composition of 45%–50% of carbohydrates, 20%–25% of proteins (preferentially fish and lean sources) and 25%–30% of lipids (preferentially unsaturated). The physical activity program aimed at reaching 160 min/week of moderate-intensity endurance exercise. Men received a personalized training program elaborated according to their history and preferences in physical activities and based on results of a maximal treadmill test and on the rating of self-

perceived exhaustion (modified Borg scale) (American College of Sports Medicine (ACSM) 1995). The physical activity/exercise prescription included 2 to 7 sessions of 30 to 60 min each per week. Men had free access to an onsite fitness centre for 3 months and were allowed to perform exercise on site or outside at their convenience. As an additional objective of increasing occupational activity, participants were also asked to wear a pedometer and to reach a target of 10 000 daily steps. Diet and physical activity/exercise assessment The daily caloric intake was estimated at baseline and at 1 year by a 3-day dietary journal, including a nonworking day to evaluate mean daily energy and macronutrient intake, as previously reported (Tremblay et al. 1983). Energy and macronutrient intakes were calculated using the computerized Canadian Nutrient File (2001). Mean number of steps per day was obtained from the pedometer. Moreover, to have an objective marker of participation to vigorous physical activity/exercise, we relied on cardiorespiratory fitness data which was assessed using a submaximal standardized exercise test. Two variables were retained as fitness endpoints to evaluate cardiorespiratory fitness: (i) heart rate (mean of the last 3 min) at a standardized submaximal treadmill stage (3.5 miles/h (5.6 km/h), 2% slope) and (ii) the estimated metabolic equivalent of task reached by the subject at a heart rate of 150 beats/min and calculated using formulas of the ACSM (ACSM 1995). Anthropometric measurements and body composition Anthropometric measurements, including skinfolds (extremities: triceps, biceps and medial calf; trunk: subscapular, suprailiac Published by NRC Research Press

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and abdominal), height, body weight, hip circumference (Lohman et al. 1988), waist circumference (van der Kooy and Seidell 1993), and sagittal diameter, were measured according to standardized procedures. Dual-energy X-ray absorptiometry (DEXA; Lunar Prodigy, GE, Madison, Wis., USA) imaging technology was performed to assess body composition (fat mass and fat-free mass). CT CT was performed on subjects at baseline and after 1 year using previously described procedures (Després et al. 2009; Ferland et al. 1989). Measurements were performed at L2–L3 and L4–L5 intervertebral space with subjects lying in the supine position with both arms stretched above the head. Images were obtained using standardized procedures and analyzed using the specialized sliceOmatic image analysis software (Tomovision, Montréal, Que., Canada). VAT area was determined by delineating the middle of the muscle wall surrounding the abdominal cavity. The SAT corresponded to the amount of fat located from the skin to the middle of the muscle wall surrounding the abdominal cavity. By use of the fascia superficialis, SAT was further subdivided into DSAT and SSAT depots. Abdominal muscle tissue cross-sectional area was also quantified. Calculations of the partial volumes of VAT and SAT between L2–L3 and L4–L5 were performed using the product of the mean of L2–L3 and L4–L5 cross-sectional areas multiplied by the distance separating the 2 slices, as previously described (Paré et al. 2001). Abdominal adipose tissue areas were computed using an attenuation range of –190 to –30 Hounsfield units (HU). CT was also performed at midthigh to assess cross-sectional areas of both thighs and determine total adipose tissue (TATth), SATth and deep adipose tissue (DATth) also using an attenuation range of –190 to –30 HU. Finally, cross-sectional areas of total muscle tissue (attenuation range of –29 to 100 HU) were quantified and further characterized as low-attenuation muscle areas (attenuation range of 0 to 34 HU) and normal-attenuation muscle areas (attenuation range of 35 to 100 HU). Low-attenuation muscle would reflect a fat-infiltrated muscle, whereas normal-attenuation muscle would reflect a low-muscle fat content, as previously described (Goodpaster et al. 1999). Statistical analyses All data are reported as means ± standard deviation in tables. Paired t tests were used to assess the statistical significance of change of each variable over the first year of the lifestyle modification program. A linear mixed model was formed to compare groups according to tertiles of changes in VAT volume or in fat mass and region (SSAT or DSAT) with an interaction term. Covariance matrix was stated to a compound symmetric structure. Shapiro–Wilk test was used to examine the distribution of statistical model. Statistical significance was set a priori at p < 0.05. All statistical analyses were performed using the SAS statistical package version 9.2 (SAS Institute, Cary, N.C., USA).

Results From the 144 subjects who initially started the lifestyle intervention program, 117 completed the first year of intervention (81%). However, only participants who had data on visceral adipose tissue measured at L4–L5 at baseline and at 1 year were kept in the present analyses (n = 109). The 109 men who completed the 1 year of intervention and with complete data on visceral adipose tissue (L4–L5) were not different at baseline from the 35 who did not, except for the self-reported daily caloric intake, which was higher in men who completed than in those who did not complete the 1-year intervention (3045 ± 646 vs. 2705 ± 652, p < 0.05). Baseline and 1-year follow-up data of the sample of 109 abdominally obese, dyslipidemic men involved in the present analyses are shown in Table 1. As expected, men significantly reduced their reported total daily energy intake and lipid intake and increased their carbohydrate and protein intake (Table 1). Moreover, signif-

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Table 3. Correlations between 1-year changes in various adiposity or body fat distribution variables and 1-year changes in abdominal adipose tissue volumes. Variables

TAT

VAT

SAT

DSAT

SSAT

Anthropometry Weight Body mass index Waist circumference Hip circumference Waist-to-hip ratio Sagittal diameter

0.91* 0.91* 0.84* 0.72* 0.65* 0.77*

0.81* 0.81* 0.74* 0.55* 0.59* 0.69*

0.87* 0.87* 0.81* 0.70* 0.62* 0.75*

0.86* 0.86* 0.79* 0.73* 0.58* 0.75*

0.74* 0.76* 0.70* 0.54* 0.59* 0.63*

Skinfolds Trunk Extremity Trunk/extremity Sum of 6

0.56* 0.32† — 0.55*

0.46* 0.30† — 0.46*

0.64* 0.30† 0.26† 0.61*

0.65* 0.29† 0.28† 0.61*

0.51* 0.28† — 0.49*

Body composition % Body fat Fat mass Fat-free mass

0.77* 0.88* 0.47*

0.69* 0.79* 0.44*

0.72* 0.84* 0.45*

0.69* 0.83* 0.47*

0.64* 0.72* 0.38*

Note: *p < 0.0001; †p < 0.05. DSAT, deep subcutaneous adipose tissue; SAT, subcutaneous adipose tissue; SSAT, superficial subcutaneous adipose tissue; TAT, total adipose tissue; VAT, visceral adipose tissue.

Table 4. Correlations between 1-year changes in abdominal adipose tissue volumes and 1-year changes in midthigh adipose tissue and muscle areas. Variables

TAT

VAT

Abdominal adipose tissue volumes VAT 0.94* — SAT 0.90* 0.69* DSAT 0.87* 0.65* SSAT 0.80* 0.63*

SAT

DSAT

SSAT

0.69* — 0.97* 0.88*

0.65* 0.97* — 0.76*

0.63* 0.88* 0.76* —

0.82* 0.69* 0.82*

0.72* 0.56* 0.72*

0.29† 0.44* —

0.27† 0.33† —

Midthigh adipose tissue and muscle areas Adipose tissue TATth 0.84* 0.72* 0.84* 0.74* 0.63* 0.69* DATth SATth 0.83* 0.71* 0.84* Muscle tissue Total 0.36† 0.38* 0.29† Low-attenuation 0.52* 0.54* 0.44* Normal-attenuation — — —

Note: *p < 0.0001; †p < 0.05. DATth, deep adipose tissue at midthigh; DSAT, deep subcutaneous adipose tissue; SAT, subcutaneous adipose tissue, SATth, subcutaneous adipose tissue at midthigh; SSAT, superficial subcutaneous adipose tissue; TAT, total adipose tissue; TATth, total adipose tissue at midthigh; VAT, visceral adipose tissue.

icant improvements in cardiorespiratory fitness and daily step count were also observed (Table 1). Significant reductions in levels of all anthropometric variables were observed after the 1-year lifestyle modification program. Moreover, skinfold thicknesses were also significantly reduced following the lifestyle intervention, except for the trunk/extremity ratio, which did not change. Body fat mass (in kg or %) assessed by DEXA was substantially decreased after 1 year. There was a small but statistically significant decrease in fat-free mass (less than 1%) in response to the 1-year intervention (Table 1). Adipose tissue areas/volumes measured by CT scan are presented in Table 2. After 1 year of intervention, decreases in abdominal TAT, VAT, SAT, DSAT and SSAT, expressed either by areas or volumes, were all significant (p < 0.0001). A slight but significant reduction in abdominal muscle tissue area was also observed (p < 0.0001). Moreover, as shown in Table 2, adipose tissue areas at the midthigh level (TATth, DATth and SATth) decreased significantly (p < 0.0001). On the other hand, a significant reduction Published by NRC Research Press

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Table 5. Correlations between 1-year changes in dietary and physical activity/exercise variables and 1-year changes in various adiposity or body fat distribution variables, abdominal adipose tissue volumes and midthigh adipose tissue and muscle areas. Variables

Heart rate at 3.5 miles/h (5.6 km/h); 2%

Exercise output at 150 beats/min

Daily step count

Total energy intake

Carbohydrate (%)

Lipid (%)

Protein (%)

Anthropometry Weight Body mass index Waist circumference Hip circumference Waist-to-hip ratio Sagittal diameter

0.65* 0.65* 0.58* 0.39* 0.50* 0.57*

−0.63* −0.63* −0.52* −0.52* −0.36† −0.52*

— — — — — —

— — — — — —

— — — — — —

— — — — — —

−0.22† — — — — −0.24†

Skinfolds Trunk Extremity Trunk/extremity Sum of 6

0.46* 0.29† — 0.45*

−0.45* −0.33† — −0.46*

— — — —

— — — —

— 0.26† −0.22† —

— — — —

— −0.36† 0.24† —

Body composition % Body fat Fat mass Fat-free mass

0.55* 0.64* 0.32†

−0.58* −0.63* −0.27†

— — —

— — —

— — —

— — —

— −0.26† —

−0.68* −0.64* −0.57* −0.54* −0.48*

— — — — —

— — — — —

— — — — —

— — — — —

— −0.21† — — —

−0.62* −0.55* −0.61*

— −0.22† —

— — —

— — —

— — —

−0.21† −0.32† —

−0.26† −0.45† —

— — 0.24†

— — —

— — —

— — —

— — —

Abdominal adipose tissue volumes TAT 0.65* VAT 0.61* SAT 0.58* DSAT 0.57* SSAT 0.48* Midthigh adipose tissue and muscle areas Adipose tissue areas TATth 0.60* DATth 0.44* SATth 0.59* Muscle tissue Total 0.22† Low-attenuation 0.37† Normal-attenuation —

Note: *p < 0.0001; †p < 0.05. DATth, deep adipose tissue at midthigh; DSAT, deep subcutaneous adipose tissue; SAT, subcutaneous adipose tissue; SATth, subcutaneous adipose tissue at midthigh; SSAT, superficial subcutaneous adipose tissue; TAT, total adipose tissue; TATth, total adipose tissue at midthigh; VAT, visceral adipose tissue.

(p < 0.0001) in low-attenuation muscle area (reflecting muscle infiltrated with lipids) and a significant increase (p < 0.05) in normal-attenuation muscle area (reflecting muscle with a low lipid content) were observed following the lifestyle intervention program. Correlations between 1-year changes in abdominal adipose tissue volumes and anthropometric, skinfold and body composition variables are presented in Table 3. Highly significant associations between changes in anthropometric variables and changes in abdominal adipose tissue volumes were found (p < 0.0001). Weaker, but statistically significant associations were also observed between changes in skinfolds (especially trunk, extremity and sum of 6 skinfolds) and changes in abdominal adipose tissue volumes. Finally, changes in TAT, VAT, SAT, DSAT and SSAT volumes presented weaker associations with changes in body fat-free mass than fat mass, although all correlations were significant (p < 0.0001). Correlations were also computed to examine interrelationships between changes in the various CT-derived measurements (Table 4). Changes in abdominal adipose tissue volumes were all well correlated with each other (p < 0.0001), but the strongest correlations were found with changes in TAT volume. Changes in all adiposity distribution and muscle variables measured at midthigh (p < 0.05) were correlated with changes in abdominal adipose tissue variables, except normal muscle tissue area, which was not correlated with changes in abdominal adipose tissue variables. For instance, a highly significant correlation was noted between changes in VAT volumes and changes in the area of low-attenuation muscle at the midthigh level.

Finally, correlations were computed between changes in total daily amount of calories, macronutrient composition, daily step count, changes in cardiorespiratory fitness (exercise output at 150 beats/min and heart rate at 3.5 miles/h (5.6 km/h); 2% slope) and changes in body composition and fat distribution variables (Table 5). These analyses generally showed that the most significant correlations regarding changes in body composition and fat distribution variables were with changes in heart rate at 3.5 miles/h (5.6 km/h); 2% slope and changes in exercise output at 150 beats/min, which are 2 indicators of changes in cardiorespiratory fitness. To further examine individual variations in several body fat distribution/anthropometric variables following the 1-year lifestyle intervention program, men were ranked according to their changes in body weight (Fig. 1A), starting from the left with individuals who experienced the greatest body weight reduction to subjects who lost the least or even gained body weight (right). Changes in abdominal fat volumes and fat-free mass were quite heterogeneous in response to the intervention program (Fig. 1B–F). For instance, the most substantial body weight losses were not systematically predictive of the greatest reductions in VAT volume. Such discordance was particularly notorious for changes in fatfree mass, which were quite dissociated from changes in body weight. Finally, we quantified the absolute and relative changes in DSAT and SSAT volumes according to tertiles of changes in VAT volumes or in fat mass (Fig. 2). Results of this analysis showed that there was a positive relationship between changes in VAT volPublished by NRC Research Press

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Fig. 1. One-year changes in (A) body weight, (B) fat-free mass (FFM), (C) visceral adipose tissue volume (VAT), (D) subcutaneous adipose tissue (SAT) volume, (E) deep subcutaneous adipose tissue (DSAT) volume, and (F) superficial subcutaneous adipose tissue (SSAT) volume in response to the lifestyle modification program. Individual changes in body weight over the 1-year intervention are ranked in decreasing order while individual changes for panels B to F are represented in the same order as panel A.

umes or fat mass and changes in either DSAT or SSAT volumes (p < 0.0001 for both SSAT and DSAT and for VAT volumes and fat mass). Moreover, although absolute changes in DSAT volume were greater than changes in SSAT volume for the middle and high tertiles of changes in VAT volumes or fat mass, relative changes in both depots were almost similar, except for the third tertile of change in fat mass.

Discussion To the best of our knowledge, this is the first study to examine the interrelationships between changes of a comprehensive set of anthropometric/abdominal fat/body composition variables such as SSAT and DSAT in response to a 1-year lifestyle modification program in a sample of initially viscerally obese, dyslipidemic and sedentary men. We showed that volumes of both subcutaneous abdominal fat compartments (SSAT and DSAT) expressed in relative changes decreased in a similar manner, a finding that suggests that there was no preferential loss of DSAT over SSAT. Moreover, we also demonstrated that regardless of the magnitude of changes in VAT volumes, similar relative reductions in SSAT and DSAT were observed following the 1-year lifestyle intervention program.

Findings of the present intervention confirm previous studies that also showed beneficial changes in anthropometric variables and most importantly in adipose tissue distribution at the abdominal and midthigh levels induced by a negative energy balance (Borel et al. 2012; Bouchard et al. 1990; Hallgreen and Hall 2008; Paré et al. 2001; Ross et al. 1996, 2000; Slentz et al. 2004; Tuomilehto et al. 2001). The physical activity/exercise component included in the present lifestyle modification program was expected to maintain or at least limit the loss of muscle mass. A study comparing dieting alone or diet with exercise in sedentary men demonstrated that whole-body muscle was maintained in both exercise groups (aerobic and resistance) but not within the diet-only group (Ross et al. 1996). In the present study, fat-free mass showed a significant but slight decrease (–1%) whereas body fat mass was decreased by 21%. Total muscle tissue areas at the midthigh level also remained relatively stable following the lifestyle intervention program, a result consistent with the finding that fat-free mass was largely preserved despite weight loss in the present study. Abdominally obese men of the study also exhibited significant reductions in all CT-derived variables after the 1-year intervention program. These results confirm previous reports from several Published by NRC Research Press

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Fig. 2. Absolute (A and B) and relative (C and D) changes in superficial and deep subcutaneous adipose tissue volumes according to changes in either visceral adipose tissue (VAT) volumes (A and C) or fat mass (B and D). Cut-off values for changes in VAT volume were –317.2 cm3 and –628.4 cm3 and for changes in fat mass were –4.1 kg and –7.7 kg. *, p ≤ 0.0002 for difference within tertile.

groups, including ourselves, which have studied the effect of exercise training and (or) caloric restriction on weight loss and body fat distribution (Després and Lamarche 1993; Paré et al. 2001; Ross and Rissanen 1994; Zamboni et al. 1993). Several studies had demonstrated a preferential decrease in VAT compared with SAT (Borel et al. 2012; Janssen and Ross 1999; Paré et al. 2001; Ross and Rissanen 1994; Zamboni et al. 1993). However, to the best of our knowledge, this was the first time that the hypothesis of a selective mobilization of DSAT as opposed to SSAT in response to a lifestyle intervention program was tested, as DSAT had been suggested to be metabolically closer to VAT than SSAT (Smith et al. 2001). Results of the present study showed that relative changes in volumes of both subcutaneous abdominal fat compartments decreased in a similar manner. Therefore, there was no preferential loss of DSAT over SSAT after the 1-year intervention program. Whether this finding of a lack of difference in the responsiveness of DSAT and SSAT to a lifestyle modification program aiming at weight loss applies to women and to other ethnic groups (our sample only included Caucasian men) will, however, require further investigation. Results also showed that both (DSAT and SSAT) subcutaneous depots decreased as a function of reduction in VAT volumes and that the relative reductions in the 2 depots were similar. The present study did not support the hypothesis that DSAT and SSAT volumes respond differently to a lifestyle modification program, inducing a negative energy balance and weight loss. Excess VAT is well recognized to be related to an increased risk of developing a deteriorated cardiometabolic risk profile associated with an increased risk of type 2 diabetes and cardiovascular disease (Després and Lemieux 2006; Després et al. 2008).

Recent studies suggested that abdominal DSAT may be associated with the same deleterious metabolic effects as VAT (Deschenes et al. 2003; Kelley et al. 2000; Koska et al. 2008). On the other hand, a recent study has suggested that high abdominal SSAT may have protective properties against the development of an altered cardiometabolic risk profile in patients with type 2 diabetes (Golan et al. 2012). This finding supports the notion that the subcutaneous adipose tissue should act as a protective metabolic sink for the clearance and storage of excess calories when facing a positive energy balance (Després and Lemieux 2006; Després et al. 2008). Moreover, we observed that low-attenuation muscle areas at the midthigh level decreased while normal-attenuation muscle areas slightly increased, suggesting a decrease in muscle fat content. As previously reported, a reduced attenuation value of skeletal muscle would most likely reflect an increased fat content in the skeletal muscle (Goodpaster et al. 1999; Kelley et al. 2000; Smith et al. 2001) and normal-density muscle area would reflect a lower fat and possibly a healthier muscle. The present finding of endurance exercise training inducing delipidation of skeletal muscle is consistent with previously published studies (Prior et al. 2007; Ryan et al. 2000, 2006) and may contribute to the beneficial effects of exercise training on glucose-insulin homeostasis and cardiometabolic risk profile (Prior et al. 2007). In this regard, the significant association between changes in low-attenuation muscle and changes in VAT volume suggests than such reduction in lowattenuation muscle area in response to an exercise program may represent a CT-imaging marker of ectopic fat mobilization (in this case in the skeletal muscle), which is to be expected from a loss of VAT. Published by NRC Research Press

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We also examined relationships between changes in CT-derived abdominal adipose tissue volumes and all variables investigated in the present study. As skinfold measurements are not expensive, they have been extensively used in large cohorts to estimate body adiposity (Jackson and Pollock 1976; Lohman 1981). We believe that our results clearly show that skinfold measurements are of little use in clinical practice for the estimation of changes in abdominal fat compartment volumes (Cornier et al. 2011). Changes in waist circumference and sagittal diameter were much better predictors of changes in VAT volumes. On the other hand, strong associations were also found between weight loss or BMI changes and changes in TAT, SAT volumes or in VAT volumes. This observation is at variance from other studies that had shown that changes in body weight correlated with changes in TAT or SAT, but to a lesser extent with changes in VAT (Matsushita et al. 2012; Zamboni et al. 1993). However, other studies performed in men have also demonstrated significant relationships between weight or BMI reductions and changes in TAT, SAT and VAT (Kuk and Ross 2009; Paré et al. 2001). Several factors may likely contribute to differences among studies, such as baseline characteristics (all our subjects were viscerally obese and overweight/obese), age, sex, ethnicity and the weight loss approach. For instance, subjects of the present study represented a relatively homogeneous sample of abdominally obese Caucasian men. Therefore, our findings and interpretation only apply to this subpopulation and cannot be generalized to the general population. Whether changes in a given adipose tissue variable could reflect changes in other adiposity indices remains unclear. As previously discussed, it appears that changes in body weight is a decent marker of changes in abdominal VAT, SAT, DSAT and SSAT volumes when studying a homogeneous sample of viscerally obese men. However, results of Fig. 1 also clearly show that individuals with the greatest changes in body weight were not necessarily those who exhibited the greatest changes in VAT volume. These data support the notion of heterogeneity in the response of individual adipose tissue depots following a 1-year lifestyle modification program. In conclusion, this study provides evidence that the 1-year lifestyle modification program improved the body fat distribution pattern and the midthigh muscle lipid content in viscerally obese, dyslipidemic and sedentary men. Skinfold measurements were found to be poor predictors of changes in all abdominal adipose tissue variables and their widespread clinical use is therefore questionable. Changes in waist circumference and sagittal diameter compared with skinfolds appeared to be much better anthropometric tools to evaluate changes in both abdominal VAT and SAT volumes in response to the lifestyle modification program. A disconnect between changes in body weight and changes in abdominal adipose tissue volumes and fat-free mass confirmed that changes in body weight are not always a good predictor of VAT reduction. Finally, regardless of the magnitude of changes in VAT volumes, similar relative reductions in both subcutaneous depots (SSAT and DSAT) were observed following the 1-year lifestyle intervention program. Future studies will be necessary to document the heterogeneity in the response of the various body adipose tissue and muscle compartments to various lifestyle interventions in both men and women from different populations.

Acknowledgements Dr. Nazare is a post-doctoral fellow supported by a fellowship from the Canadian Institute of Health Research. Dr. Angelo Tremblay is partly funded by the Canada Research Chair in Environment and Energy Balance. Dr. Paul Poirier is a senior clinical scientist from the Fonds de recherche du Québec – Santé (FRQ-S). Dr. Jean-Pierre Després is the Scientific Director of the International Chair on Cardiometabolic Risk, which is based at Université Laval.

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Copyright of Applied Physiology, Nutrition & Metabolism is the property of Canadian Science Publishing and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.

Interrelationships between changes in anthropometric variables and computed tomography indices of abdominal fat distribution in response to a 1-year physical activity-healthy eating lifestyle modification program in abdominally obese men.

The objectives were to (i) measure the effects of a 1-year lifestyle modification program on body fat distribution/anthropometric variables; (ii) dete...
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