Fat is stored in the human body in essentially three major compartments: 1) intra-abdominal visceral fat mass (VFM), 2) subcutaneous fat mass (SFM) and 3) intra-muscularly (7). Recent studies have shown that the reduction in VFM is associated with a significant decrease in the risk of coronary heart disease and noninsulin dependent diabetes mellitus(10,12). Alteration of caloric balance either by restricting caloric intake and/or increasing energy expenditure (increased physical activity) have been shown to reduce VFM. However, the specific mechanisms by which either of these caloric perturbations independently affects VFM is not clear. Caloric intake restriction alone(14,16,23,27) results in significant decreases in VFM and SFM; the effect on VFM is significantly greater. The negative is that caloric restriction also leads to a decrease in muscle mass. Caloric restriction, in combination with increased energy expenditure (aerobic or resistance exercise), results in greater decreases in VFM(19), then seen with caloric restriction alone. However, the independent effects of exercise on VFM remain controversial as exercise has been shown to have a greater impact on SFM(10,20).
The present study was designed to investigate the effect of varying frequencies of aerobic exercise training and caloric restriction on VFM and SFM reduction. If decreasing SFM and VFM is more related to caloric expenditure rather than caloric restriction, then the higher frequency of exercise should cause greater loss of SFM and VFM than the exercise with a lower frequency and caloric restriction.
Subjects. Twenty-six healthy women aged 19-23 yr who were sedentary (engaged in exercise less than 30 min·d-1, 1 d·wk-1) provided written informed consent to participate in the study. Subjects were randomly divided into three groups: a control group (C;N = 8), a group that performed aerobic exercise 1-2 sessions/wk and followed a program of caloric restriction (1-2SW; N = 9), and a group that performed aerobic exercise 3-4 sessions/wk while maintaining caloric intake (3-4SW; N = 9). The methods and procedures were approved by the Institutional Review Board of the Tokyo Metropolitan University.
Aerobic exercise programs. The training programs were administered for 13 wk. Each group was instructed to strictly follow their training protocol (1-2SW or 3-4SW), which consisted of stationary cycling for 30 min per session. The prescribed intensity of the exercise program was 50-60% of maximal heart rate reserve (0.5≈0.6 [maximal pulse - resting pulse] + resting pulse) as calculated from a maximal exercise test. Criteria for maximal exercise were leveling off of oxygen uptake or a respiratory-exchange ratio greater than 1.1 at maximal exercise. All training sessions were supervised and heart rate was monitored continuously.
Dietary restriction. Three-day dietary questionnaires (two weekdays and one weekend day) were recorded before training and during the final week of training in both the exercise and control groups to monitor their caloric intake. Subjects in 1-2SW training group were instructed to maintain a regimen of moderate dietary restriction, in which they were requested to restrict caloric intake by ≈ 200 kcal·d-1 below baseline. The control group and 3-4SW were instructed not to change their usual lifestyle or daily food intake.
Measurements of percentage body fat and TFM. Body density (BD) was measured by the hydrostatic weighing technique as previously described(1). Pulmonary residual volume was measured using the oxygen dilution method of Rahn et al. (18). The mean of three measurements was used in the calculation of body fat percentage from BD using the equation of Siri (22). Total body fat mass(TFM) was obtained by multiplying body fat percentage by body weight.
Measurements of VFM and SFM. Total and segmental subcutaneous fat mass (SFM) were estimated from body surface areas and mean thickness of subcutaneous adipose tissue layers measured by B-mode ultrasonography(2,3). The whole body surface was divided into six sections (face and neck, upper arm, forearm, thigh, lower leg, and trunk) according to the method of Shintani (21). Scalp, hand, and foot segments were excluded from SFM calculations because of the lack of fat in those regions. Body surface area was calculated using the equation of Nakamura (17):
Body surface area = 70.98 × (body mass)0.425 ×(height)0.725
The ultrasonographic evaluation of subcutaneous adipose tissue (including skin) was performed using a real-time linear electronic scanner (SSD-500, Aloka Co., Ltd., Tokyo, Japan). Several sites were selected from each segment(except forearm) covering the anterior and posterior aspects of the segment, and the mean of adipose tissue (AT) thicknesses of those sites represented the AT thickness of each segment. Six sites (juxta-umbilicus, subscapula, suprailiac, mid-axillary, anterior chest, and sternum) were selected for measurements of the trunk taking into account the large variation of AT thickness in this region. Sites were precisely located and marked with a surgical pen before the measurement as described by Abe et al.(2). Dermis thickness (24) was excluded from ultrasound-measured subcutaneous AT thickness. The density of fat was taken as 900 (kg/m3) (11). The proportion of fat in adipose tissue was considered to be 0.80 according to Baker(6) and Garrow (13).
VFM was calculated as the difference between total fat mass (TFM) and subcutaneous fat mass (SFM). The authors have previously confirmed that the deviations in repeated VFM and SFM measurements are 2.5% and 5.0%, respectively (2).
Statistical analysis. Data are expressed as means ± SD. Exercise frequency and training interactions were tested by two-way repeated-measures ANOVA with group (1-2SW, 3-4SW, and control) and time (pre- and post-training) as grouping variables. Post hoc testing was performed by paired (within group) or unpaired (between groups) Student'st tests. Relationships between relative changes in selected variables (post-training value minus pretraining value) in the exercise group were examined using Pearson product correlations. Partial correlations between average exercise frequency and the changes in body fat distribution were calculated to eliminate the effect of change in caloric intake. In each statistical analysis the level of significance was set at P < 0.05.
Total kilocalories consumed per day did not differ before and at the end of the training (1699 ± 354 vs 1673 ± 325 kcal·d-1) in C. In the training groups, individual differences in the changes in caloric intake were observed, and total energy intake was reduced by 15% on average in the 1-2SW group (1664 ± 143 vs 1424 ± 265 kcal·d-1). On the other hand, there was no apparent difference in energy intake (1784 ± 187 vs 1773 ± 421 kcal·d-1) for the 3-4SW group before and at the end of the program. The average weekly exercise frequencies of the 1-2SW and 3-4SW groups were 1.4 ± 0.5 and 2.8 ± 0.2 sessions per week, respectively. The energy cost of each exercise training session ranged from 150 to 220 kcal. Approximate weekly caloric deficits were 1960 kcal·wk-1 (about 1680 kcal·wk-1 because of dietary restriction, plus 280 kcal·wk-1 because of exercise) for 1-2SW group and 640 kcal·wk-1 (about 80 kcal·wk-1 because of dietary restriction, plus 560 kcal·wk-1 because of exercise) for 3-4SW group.
Table 1 depicts changes in body fat distribution for the three groups before and after the 13-wk aerobic exercise training programs. In the C group, there were no training-induced differences in body mass (52.4 ± 6.6 vs 51.8 ± 6.3 kg), body fat percentage (28.5± 2.8 vs 28.6 ± 2.7%), SFM (11.4 ± 2.8 vs 11.1 ± 2.3 kg), and VFM (3.6 ± 1.3 vs 3.8 ± 1.5 kg). The reduction in total body weight, percent body fat, and total fat mass following training was significant both in the 1-2SW and 3-4SW groups. SFM was significantly reduced in 3-4SW (-16.2%, P < 0.01), but not in 1-2SW (-4.9%). In 3-4SW, significant reductions were observed in the segmental SFM except for face and neck and lower leg segments. The relative decrease in the trunk SFM (-20.5%) was significantly greater than in the thigh (-14.8%), upper arm (-12.0%), or forearm (-11.1%). There were significant VFM reductions in both the 1-2SW(-37.5%) and 3-4SW (-22.2%) groups.
In both groups, initial SFM was not related to changes in total SFM after the experimental period (1-2SW group: r = 0.37, 3-4SW group: r = 0.57; bothP > 0.05). However, in the 3-4SW group, initial trunk and upper arm SFM were related to changes in SFM in the respective sites (r = 0.64;P < 0.05, r = 0.83; P < 0.01, respectively). The changes in VFM were highly correlated with the initial VFM (r = 0.88,P < 0.01) in the 3-4SW group.
Figure 1 shows the relationships between the average weekly exercise frequency and the changes in SFM and VFM of the training groups (N = 18). There was no significant correlation between the change in VFM and the weekly exercise frequency (r = 0.20, P > 0.05). However, the average weekly exercise frequency was negatively correlated with changes in total SFM (r = -0.65, P < 0.01) and also with changes in truncal (r = -0.57, P < 0.05) and femoral (r= -0.57, P < 0.05) SFM.
After the elimination of the caloric intake effect because of the change in total energy intake, a significant correlation still existed between the average exercise frequency and changes in total SFM as well as changes in truncal and femoral SFM. The change in VFM was not significantly related to exercise frequency (Table 2).
Although the estimation procedure used in the present study to measure SFM and VFM is theoretically sound (8), whether it reflects the actual body fat mass has yet to be determined. Chowdhury et al.(7) found that the fat accumulates mainly subcutaneously, and the remainder accumulates in the abdominal region surrounding the viscera. The fat accumulation of these two areas has been reported to represent 98.2% of the total body fatness (7). Therefore, the difference between the total amount of fat and SFM appears to reflect the amount of VFM. Previous experiments from our laboratory (2) showed a high correlation (r = 0.90) for subcutaneous AT area of umbilicus level versus estimated SFM, and a significant correlation (r = 0.78) for visceral AT area versus estimated VFM. Hence, the estimation method of SFM and VFM used in the current study appears accurate and appropriate for our purposes.
Previous studies have reported the effects of aerobic exercise on body fat distribution evaluated by skinfold and circumference measures in young and older subjects. Despres et al. (9) reported that the sum of the trunk skinfolds decreased by 22% compared with a 12.5% decrease in the extremity skinfolds in young men who lost 2.6 kg of body fat after a 20-wk aerobic exercise training program. In a similar study which evaluated the effect of a 9- to 12-month aerobic exercise training program on sedentary older men and women, a significantly greater reduction was observed in the upper trunk fat compared with the extremity (15). In the present study we also observed a greater loss of SFM in the truncal segment compared with the limb segments. The finding that SFM preferentially decreased in the trunk is consistent with the observation that adipocytes in abdominal subcutaneous adipose tissue are more lipolytically active compared with adipocytes in the femoral region (26).
Schwartz et al. (20) reported that intra-abdominal and central subcutaneous AT areas significantly decreased after a 6-month endurance exercise training program in young and old men. Treuth et al.(25) found that visceral AT decreased significantly after a 16-wk strength training program, but no significant change in the abdominal subcutaneous AT area or percentage body fat were seen. Computed intra-abdominal visceral AT tomography showed no significant reduction in area for subjects who underwent a 14-month aerobic exercise program(10). Although their studies observed no significant changes in estimated energy balance throughout the training program, the effects of exercise training on intra-abdominal visceral fat is equivocal.
In this study we investigated the effect of exercise frequency on VFM and SFM distributions. The most interesting finding was the difference in the response of SFM and VFM to various training frequencies. The American College of Sports Medicine (ACSM) recommends aerobic exercise training with frequency of 3-5 times per week for cardiovascular fitness (4). Although VFM was decreased significantly, the diet group (1-2SW) which exercised less frequently than the ACSM guideline did not reduce SFM. On the contrary, the 3-4SW exercise group without diet restriction demonstrated significant decreases in both SFM and VFM. The reduction in SFM was correlated highly with the training frequency, whereas the reduction in VFM was not related to the training frequency but caloric imbalance. This study demonstrated that aerobic exercise with a frequency of 3-5 times per week as recommended by the ACSM is important to decrease SFM, while the reduction in VFM could be achieved either by caloric restriction or by aerobic exercise(increased energy expenditure: 150-220 kcal/session) with less frequency (1-2 times/wk).
A possible mechanism for the difference in SFM and VFM reduction could be the difference in lipolytic effect as it relates to hormonal sensitivity between SFM and VFM. It has been established through in vivo andin vitro investigations that the lipolytic activity rate of human adipose tissue is high in the visceral region, intermediate in the subcutaneous abdominal region, and low in the subcutaneous gluteal/femoral region (5). It is possible that the lipolytic activity of visceral fat cell is such that even the low training frequency (1-2 times/wk) of aerobic exercise could significantly reduce VFM. However, the hormonal effect of lipolysis in SFM and VFM is beyond the scope of this study and requires further research.
We would like to thank Dr. William F. Brechue in the Department of Kinesiology, Indiana University, for his helpful comments and suggestions for the development of the manuscript.
This work was supported by Grants-in-Aid for Scientific Research No. 06780091 to T. Abe from the Ministry of Education, Science, Sports and Culture of Japan.
Address for correspondence: Dr. Takashi Abe, Department of Exercise and Sport Science, Faculty of Science, Tokyo Metropolitan University, 1-1 Minamiohsawa, Hachioji, Tokyo 192-03, Japan.
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