- Email: [email protected]
Daily exercise lowers blood pressure and reduces visceral adipose tissue areas in overweight Japanese men
Diabetes Research and Clinical Practice 62 (2003) 149 /157 www.elsevier.com/locate/diabres
Daily exercise lowers blood pressure and reduces visceral adipose tissue areas in overweight Japanese men Nobuyuki Miyatake a,*, Kayo Takahashi b, Jun Wada c, Hidetaka Nishikawa a, Akie Morishita a, Hisao Suzuki b, Mie Kunitomi c, Hirofumi Makino c, Shohei Kira d, Masafumi Fujii a a
Okayama Southern Institute of Health, 408-1 Hirata, Okayama 700-0952, Japan b Faculty of Education, Okayama University, Okayama, Japan c Department of Medicine and Clinical Science, Okayama University Graduate School of Medicine and Dentistry, Okayama, Japan d Department of Public Health, Okayama University Graduate School of Medicine and Dentistry, Okayama, Japan Received 24 April 2003; received in revised form 16 June 2003; accepted 23 July 2003
Abstract Objective: To investigate the link between a reduction in blood pressure (BP) and daily exercise. Design: Crosssectional and longitudinal clinical intervention study with exercise education. Subjects: 43 overweight Japanese men aged 32 /59 years (BMI, 29.09/2.3 kg/m2) at baseline. Among the participants, a randomly selected 23 overweight men (BMI, 28.59/1.7) were further enrolled into the 10 months exercise program. Measurements: BP was measured every week and steps per day were also recorded every day throughout the observation period. Fat distribution was evaluated by visceral fat (V) and subcutaneous fat (S) areas measured with computed tomography (CT) scanning at umbilical level, at before, 5 months and after intervention. Anthropometric parameters were also measured at same point. Aerobic exercise level, muscle strength, flexibility and calorie intake and insulin resistance (HOMA index) were investigated at before and after the study. Results: In a cross sectional analysis, systolic BP (SBP) and diastolic BP (DBP) were significantly correlated with body composition. In a second longitudinal analysis, SBP was significantly reduced at 2 months and DBP was also reduced at 3 months, and almost maintained until the end of the observation period. Increasing daily walking was observed in 3 months and maintained until 10 months. Body composition, aerobic exercise level, muscle strength, flexibility and insulin resistance were significantly improved. There was positive correlation between DDBP and Dvisceral fat area (1 /5, 5 /10, 1 /10 months). By stepwise multiple regression analysis, only Dvisceral fat area was independently related to DDBP at a significant level (1 /10 months: DDBP / /0.608/ 0.105Dvisceral fat area, r2 /0.227, P /0.0334). Conclusion: The present study indicated daily exercise lowers BP and visceral fat area is the critical factor for BP change. # 2003 Elsevier Ireland Ltd. All rights reserved. Keywords: Visceral adipose tissue; Anthropometric parameters; Computed tomography
* Corresponding author. Tel.: /81-86-246-6250; fax: /81-86-246-6331. E-mail address: [email protected] (N. Miyatake). 0168-8227/03/$ - see front matter # 2003 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/S0168-8227(03)00176-1
150
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
1. Introduction It has been shown that a number of obese subjects have a high mortality rate [1], and are associated with atherogenic risk factors, such as hypertension, coronary heart disease, diabetes mellitus and dyslipidemia [2,3]. Recent advances in our understanding of the pathophysiology of obesity convinces us that intra-abdominal or visceral adipose tissue accumulation is closely related to insulin resistance and the development of atherosclerosis [4,5]. In addition, the modern life style of a high-calorie diet and reduced physical activities are closely related to the increasing population of obese subjects. In order to provide proper management and control of obesity, the exact assessments of obesity as well as the development of effective treatments are required. In this respect, physical exercise greatly improves insulin action [6], and continued exercise is, therefore, recommended as a supplemental form of therapy to a specific diet treatment for obese subjects. However, it is important to clarify how exercise program induced weight loss is associated with comparable reductions in blood pressure (BP), and what is the critical factor of BP change. In this study, we investigated the effectiveness of daily exercise on BP, body composition, insulin resistance and physical fitness in overweight Japanese men.
2. Subjects and methods 2.1. Subjects Japanese overweight men (n/43), aged 32/59 years (45.29/7.5) were enrolled into this study with written informed consent. Overweight was diagnosed according to the criteria of WHO [7] and the average body mass index (BMI) of overweight subjects was 29.09/2.3 (26.4/37.8), respectively. No subjects received any medications for diabetes, hypertention, and/or dyslipidemia throughout the observation period. In a first cross-sectional analysis, we used baseline data on 43 overweight subjects (Table 1), aged
Table 1 Clinical profiles of subjects Number of subjects Age Body weight (kg) BMI (kg/m2) Body fat percentage (%) Waist circumference (cm) Hip circumference (cm) Waist hip ratio Visceral fat area (cm) Subcutaneous fat area (cm) SBP (mmHg) DBP (mmHg)
43 4.5.29/7.5 82.79/7.9 29.09/2.3 30.39/4.5 95.49/5.9 100.19/3.9 0.959/0.04 121.19/51.5 154.69/46.2 141.3/10.9 86.29/8.3
Mean9/S.D.
32/59 years, and investigated the relationships among body composition and BP. In a second longitudinal analysis, we used follow-up data of 23 subjects (47.19/6.9 years) randomly selected from 43 overweight participants, who met the following criteria: (1) no electrocardiogram changes in response to exercise, (2) a repeat CT scanning at follow-up, (3) a follow up duration of 10 months, and (4) joining exercise program at Okayama Southern Institute of Health. They visited Okayama Southern Institute of Health on a weekly basis and were monitored for 10 months. All of the subjects were instructed not to change eating habits, and trained nutritionists determined total calorie intake using food diaries before and after the 10 months follow up. Daily steps were also measured by pedometer (WZ100A, SEIKO Corporation, Japan) and the average of every month was monitored throughout the follow up period. Subjects joined an exercise program (%HRmax: 50 /65) at Okayama Southern Institute of Health every week. In addition, they were instructed to check daily steps every day and increase their daily walk at least 1000 steps besides the daily walk at baseline. Thus a negative energy balance would be induced by exercise. In addition, to evaluate the effect of daily exercise, anthropometric parameters and fat distribution were measured at before, 5 months and after the study. Aerobic exercise, muscle strength, flexibility and insulin resistance were also measured at before and after the study.
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
2.2. BP measurements Every week, BP of each participant was measured after resting at least 15 min in a sitting position before the exercise program at Okayama Southern Institute of Health, and the average of every month was recorded. Hypertension was diagnosed according to the WHO criteria.
151
measured at the widest circumferences over the trochanter in standing subjects after normal expiration. Body fat percentage was measured by an air displacement plethysmograph called the BOD POD Body Composition System (Life Measurement Instruments, Concord, CA) [11,12].
2.6. Aerobic exercise level 2.3. Blood sampling and hormone assays After subjects fasted overnight for 10 /12 h, we collected blood samples in order to determine serum levels of insulin and plasma glucose. Serum insulin was measured by immunoradiometric assay (IRMA) using INSULIN RIABEAD II (DAINABOT, Tokyo, Japan). Plasma glucose was measured by using the glucose-oxidant method. The insulin resistance was evaluated using the homeostasis model assessment, the HOMA index [fasting plasma glucose (mg/dl) /fasting serum insulin (mU/ml)/405], according to the method developed by Matthews et al. [8]. 2.4. Visceral and subcutaneous fat areas The intra-abdominal visceral fat and the subcutaneous fat areas were measured by computed tomography (CT) scanned at the umbilical [9]. CT films were converted into digital images and both visceral and subcutaneous fat areas were measured with image analysis software OPTIMAS version 6.5 (Media Cybernetics, Silver Spring, MD, USA). The intraperitoneal area with the same density as the subcutaneous fat layer was defined as the visceral fat area [10]. 2.5. Anthropometric and body composition measurements Their anthropometric and body composition were evaluated by using the following respective parameters such as, height, body weight, BMI, waist circumference, hip circumference, waist hip ratio and body fat percentage. BMI was calculated by weight/[height]2 (kg/m2). The waist circumference was measured midway between the lower rib margin and the iliac crest and the hip was
An incremental sub-maximal exercise test was done on an electrically stationary upright cycle ergometer (Excalibur V2.0, Lode BV, Groningen, Netherlands) to estimate the aerobic exercise level of the subjects [13,14]. The height of the seat was adjusted for each subject to form a knee joint angle of 160/1658 with the bikes gear in the lowest position. Each subject was fitted with a cardiopulmonary gas exchange system (Oxycon Alpha, Mijnhrdt b.v., Netherlands) to collect respiratory gas and a microcomputer for on-line calculations. Their heart rates and BP were continuously measured, using an auscultator with a pressure cuff around the upper arm connected to a mercury sphygmomanometer. Ventilatory threshold (VT) was defined according to Wasserman’s formula [15] which was recommended for the parameter of aerobic exercise level.
2.7. Muscle strength To assess their muscle strength, grip and leg strength were measured at baseline and 10 months. Grip strength was measured by using the conventional method, while leg strength was measured by COMBIT CB-1 (MINATO, Japan). Leg strength was measured as follows: the subject sat in chair, grasping the armrest in order to fix the body position. Then the dynamometer was attached to the subject’s ankle joint by a strap, next they extended the leg to 608. In order to standardize the influence of the total body weight, we employed the weight bearing index (WBI), which was calculated by leg strength (kg)/body weight (kg) [16,17]. WBI is closely related to exercise capacity e.g. speed of walking up stairs, getting up from a chair as well as gait speed.
152
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
2.8. Flexibility To evaluate the flexibility of all the participants, they were measured as follows. Sit-and-reach measurements were obtained to assess the overall flexibility in the forward flexion, with the measurements recorded as the distance (in cm) between the fingertips and toes. The subject’s knees were kept straight throughout the test and ankles were maintained at 908 by having the soles of the feet pressed against a board perpendicular to the sitting surface [13]. 2.9. Statistical analysis All data are expressed as mean9/standard deviation (S.D.) values. Statistical analysis were performed by paired t-test, repeated measure ANOVA, Fisher’s PLSD and x2-test: P B/0.05 was considered to be statistically significant. The Pearson’s correlation coefficients were calculated as well as tested for significance of the linear relationship among continuous variables. Furthermore stepwise multiple regression analysis was performed to determine what factors correlated with the changes in BP.
3. Results In a first cross-sectional analysis, SBP was significantly correlated with body weight, BMI, waist circumference, waist hip ratio and visceral fat area. DBP was also correlated with BMI, body fat percentage, waist circumference, waist hip ratio and visceral fat area (Table 2). In a second longitudinal analysis, clinical profiles and changes of subjects were summarized in Table 3. There was no significant change in calorie intake, and additional negative energy balance would be induced by daily exercise. After 10 months exercise education, SBP and DBP were significantly reduced (SBP: pre 140.39/ 13.6 mmHg vs. post 135.29/10.5 mmHg, DBP: pre 86.29/10.0 mmHg vs. post 82.29/8.1 mmHg P B/ 0.05). The number of patients with hypertension was also significantly reduced (Table 4). We investigated the change in BP with exercise educa-
Table 2 Simple correlation analysis between BP and body composition SBP
Body weight (kg) BMI (kg/m2) Body fat percentage (%) Waist circumference (cm) Hip circumference (cm) Waist hip ratio Visceral fat area (cm2) Subcutaneous fat area (cm2)
DBP
r
P
r
0.306 0.417 0.244 0.455 0.286 0.370 0.336 0.169
* **
0.211 0.374 0.328 0.405 0.281 0.309 0.425 0.061
** * *
P
* **
**
*, P B/0.05; **, P B/0.01.
tion every month. SBP was significantly reduced at 2 months and DBP was also reduced at 3 months, and almost maintained until the end of the observation period (Fig. 1). In anthropometric and body composition measurements, body weight, BMI, body fat percentage, waist circumference, visceral fat areas and subcutaneous fat areas were significantly reduced at 5 months and maintained until the end of the study (Table 3). There was remarkable change in aerobic exercise level and WBI, blood sugar, insulin and also in HOMA index. Steps per day was remarkably increased with exercise education (pre: 73899/2576 vs. post: 90709/3359 P B/0.01) and increasing daily walking was noted in 3 months and maintained until 10 months (Fig. 2). We also studied the relationship between DBP (DBP represents the positive changes in BP) and Dbody composition (Dbody composition represents the positive changes in body composition) (Tables 5/7). There was a positive correlation between DDBP and Dvisceral fat area (1 /5 months: r /0.423, P B/0.05, 5 /10 months: r / 0.536, P B/0.05, 1 /10 months: r /0.477, P B/ 0.05). We also used stepwise multiple regression analysis to evaluate the effect of Dbody composition on DDBP and found that only Dvisceral adipose fat area was independently related to DDBP at a significant level (1 /10 months: DDBP / /0.608/0.105Dvisceral fat area, r2 / 0.227, P /0.0334). Although DSBP did not significantly correlate with the parameters of Dbody composition, the correlation rate between DSBP
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
153
Table 3 Clinical profiles and changes in overweight subjects with exercise education
Body weight (kg) BMI (kg/m2) Body fat percentage (%) Waist circumference (cm) Hip circumference (cm) Waist hip ratio Visceral fat area (cm2) Subcutaneous fat area (cm2) Aerobic exercise level (ml/kg per min) Grip strength (right) (kg) Grip strength (left) (kg) WBI Flexibility (cm) Blood sugar (mg/dl) Insulin (mU/ml) HOMAindex Calorie intake (kcal/day)
Pre (1 month)
5 months
Post (10 months)
82.09/7.7 28.59/1.7 29.19/3.4 93.59/4.3 99.49/4.1 0.949/0.03 108.79/49.1 147.79/36 14.49/2.1 48.99/6.5 45.19/7.5 0.899/0.15 6.79/9.8 105.09/14.1 11.19/5.3 2.869/1.38 19489/398
79.59/8.1** 27.69/1.8** 25.89/5.0** 91.29/4.5** 98.19/0.05 0.939/0.05 85.99/40.9** 119.79/43.0**
79.09/8.5** 27.59/2.0** 26.69/4.2** 89.99/5.4** 98.39/4.1 0.929/0.04** 87.09/43.1** 122.69/38.7** 15.99/2.5** 48.19/7.6 44.99/6.7** 1.029/0.17 7.79/ 9.6* 98.49/10.8* 8.69/3.7* 2.079/0.86** 19229/365
Mean9/S.D.; *, P B/0.05 vs. pre; **, P B/0.01 vs. pre. Table 4 Change in patients with hypertension
Hypertension (/) Hypertension ( /)
Pre
Post
12 11
4 19
P B/0.05.
and Dvisceral fat area was comparatively high, but not significant (1 /5 months: r /0.379, P /0.0743, 5 /10 months: r /0.239, P/0.2963, 1 /10 months: r /0.367, P /0.1021) (Tables 5 /7).
moderate-intensity physical activity on most, and preferably all, days of the week [18]. In some literatures, exercise programs including walking, running, cycling, and swimming have demonstrated significant BP lowering effects in hypertensive individuals [19 /22]. However, most of them were designed for short duration and the program could not be performed easily. In this study, exercise education, i.e. regular exercise once a week at institute and increasing daily walk at least 1000 steps besides the daily walk have lowered BP Table 5 Simple correlation analysis between DBP and Dbody composition (1 /5 months)
4. Discussion It is well known that exercise is recommended as a supplemental form of therapy to a specific diet treatment for obese subjects. In addition, regular exercise lowers BP in patients with hypertension. The American College of Sports Medicine and Centers for Disease Control and Prevention (ACSM-CDC) developed a physical activity recommendation geared toward getting more people active. This guideline recommends that every US adult should accumulate at least 30 min of
DSBP R DBody weight (kg) DBMI (kg/m2) DBody fat percentage (%) DWaist circumference (cm) DHip circumference (cm) DWaist hip ratio DVisceral fat area (cm2) DSubcutaneous fat area (cm2) *, P B/0.05.
/0.159 /0.161 0.038 /0.089 0.052 /0.140 0.379 /0.070
DDBP P
r 0.021 0.021 0.087 0.070 0.055 0.025 0.423 0.140
P
*
154
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
Fig. 1. Time course change of SBP and DBP in Japanese overweight men with exercise education program (n/23). Data are indicated by mean9/S.D.; *, P B/0.05 vs. 1 month, #, P B/0.05 vs. 2 months, P B/0.05 vs. 3 months, /, P B/0.05 vs. 4 months.
significantly in overweight Japanese men. We monitored daily steps every day and monitored BP every week for an extended duration of 10 months. According to daily steps, overweight Japanese men were free to accumulate those steps Table 6 Simple correlation analysis between DBP and Dbody composition (5 /10 months) DSBP r DBody weight (kg) DBMI (kg/m2) DBody fat percentage (%) DWaist circumference (cm) DHip circumference (cm) DWaist hip ratio DVisceral fat area (cm2) DSubcutaneous fat area (cm2) *, P B/0.05.
0.244 0.234 0.001 0.232 0.071 0.114 0.239 0.307
DDBP P
r 0.105 0.093 0.065 /0.046 /0.154 0.083 0.536 0.219
P
*
in whatever way fit their life style, and no intensity recommendation was given. Overweight Japanese men increased their walking by an average of 1681 steps per day. It is obvious that obesity, especially excess of body fat, is closely related to hypertension, type 2 diabetes mellitus, dyslipidemia, and coronary heart disease and the underlying insulin resistance is considered to play a central role of arteriosclerosis [23 /25]. It has been shown that when visceral fat becomes enlarged, several bioactive compounds are produced in the adipose tissue i.e. free fatty acids, tumor necrosis factor alpha, leptin, and plasminogen activator inhibitor-1. These compounds may be involved in the pathogenesis of some of the complication [26]. According to the relationship between visceral fat and hypertension, Oshida Y et al. reported that insulin is an important factor in BP elevation in older obese subjects [27]. Kanai et al. reported that, by combination of low calorie diet and exercise
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
155
Fig. 2. Time course change of daily steps per day in Japanese overweight men with exercise education program (n/23). Data are indicated by mean9/S.D.; *, P B/0.05 vs. 1 month, #, P B/0.05 vs. 2 months, P B/0.05 vs. 3 months, /, P B/0.05 vs. 4 months.
therapy, improvement of glucose intolerance may be involved in BP change in obese hypertensive women [28]. We also found that improvement of insulin and HOMA index by daily exercise in Table 7 Simple correlation analysis between DBP and Dbody composition (1 /10 months) DSBP r DBody weight (kg) DBMI (kg/m2) DBody fat percentage (%) DWaist circumference (cm) DHip circumference (cm) DWaist hip ratio DVisceral fat area (cm2) DSubcutaneous fat area (cm2) P B/0.05.
/0.056 /0.055 /0.118 /0.141 /0.212 /0.025 0.367 /0.025
DDBP P r 0.128 0.126 0.017 0.037 /0.062 0.089 0.477 0.142
P
*
overweight Japanese men. Although we could not investigate other possible factors, it is obvious that visceral fat is closely linked to hypertension. The depressor effect of exercise has been attributed to factors known to influence BP such as body composition, insulin levels and diet [29 /31]. According to the body composition, some studies have shown exercise to lower BP in hypertensives independent of body mass changes [19 /22]. Also, a recent review by Hagberg et al. [32] reported that no significant correlation of 0.11 between the reduction in SBP and the reduction in body mass in 61 studies that reported body weight changes in hypertensives with exercise training. The authors concluded that the exercise training-induced reductions in SBP and DBP do not appear to be the result of weight changes with exercise. In our study, DBP was not correlated with Dbody weight as previous studies. However, there was significant correlation between DDBP and Dvisceral fat area
156
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
and only Dvisceral fat area was the determinant factor of DDBP by multiple regression analysis with long-term daily exercise. In addition, the correlation rate between DSBP and Dvisceral fat area was comparatively high, but not significant. Although other factors may strongly affect on DSBP with daily exercise [33], visceral fat not body weight is the critical factor of changes in BP in overweight Japanese men, and reducing visceral fat is important for preventing and improving BP in overweight Japanese men. In conclusion, BP was reduced by daily exercise for 10 months, and visceral fat is critically involved in BP change in overweight Japanese men.
[8]
[9]
[10]
[11]
Acknowledgements
[12]
This research was supported in part by Health Sciences Research Grants for ‘‘Research on Health Services’’ from the Ministry of Health, Labor and Welfare, Japan.
[13]
[14]
References [1] L.V. Sjostrom, Mortality of severely obese subjects, Am. J. Clin. Nutr. 55 (Suppl. 2) (1992) 516S /523S. [2] L.V. Sjostrom, Morbidity of severely obese subjects, Am. J. Clin. Nutr. 55 (Suppl. 2) (1992) 508S /515S. [3] M.C. Pouliot, J.P. Despres, A. Nadeeau, S. Moorjani, D. Prud’Homme, P.J. Lupien, A. Tremblay, C. Bouchard, Visceral obesity in men. Associations with glucose tolerance, plasma insulin, and lipoprotein levels, Diabetes 4 (1992) 826 /834. [4] D. Sparrow, G.A. Borkan, S.G. Gerzof, C. Wisniewski, C.K. Silbert, Relationship of body fat distribution to glucose tolerance: results of computed tomography in male participants of the normative aging study, Diabetes 35 (1986) 411 /415. [5] S. Fujioka, Y. Matsuzawa, K. Tokunaga, S. Tarui, Contribution of intra-abdominal visceral fat accumulation to the impairment of glucose and lipid metabolism in human obesity, Metabolism 36 (1987) 54 /59. [6] Y. Oshida, K. Yamanouchi, S. Hayamizu, Y. Sato, Longterm mild jogging increases insulin action despite no influence on body mass index or VO2max, J. Appl. Physiol. 66 (1989) 2206 /2210. [7] NHBI obesity education initiative expert panel on the identification, evaluation, and treatment of overweight and obesity in adults: clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in
[15]
[16]
[17]
[18]
[19]
[20]
[21]
adults */the evidence report, Obesity Res. 6 (1998) 51S / 63S. D.R. Matthews, J.P. Hosker, A.S. Rudenski, B.A. Naylor, D.F. Treacher, R.C. Turner, Homeostasis model assessment: insulin resistance and b-cell function from fasting plasma glucose and insulin concentrations in man, Diabetologia 28 (1985) 412 /419. K. Tokunaga, Y. Matsuzawa, K. Ishikawa, S. Tarui, A novel technique for the determination of body fat by computed tomography, Int. J. Obes. 7 (1983) 437 /445. M. Kunitomi, J. Wada, K. Takahashi, Y. Tsuchiyama, Y. Mimura, K. Hida, N. Miyatake, M. Fujii, S. Kira, K. Shikata, H. Makino, Relationship between reduced serum IGF-1 levels and accumulation of visceral fat in Japanese men, Int. J. Obes. Metab. Disord. 26 (2002) 361 /369. N. Miyatake, K. Nonaka, M. Fujii, A new air displacement plethysmograph for the determination of Japanese body composition, Diabetes Obes. Metab. 1 (1999) 347 / 351. M.A. Mccrory, T.D. Gomez, E.M. Bernauer, P.A. Mole, Evaluation of a new air displacement plethysmograph for measuring human body composition, Med. Sci. Sports Exerc. 27 (1995) 1686 /1691. N. Miyatake, H. Nishikawa, M. Fujii, Clinical evaluation of physical fitness in male obese Japanese, Chin. Med. J. 114 (2001) 707 /710. M. Kunitomi, K. Takahashi, J. Wada, H. Suzuki, N. Miyatake, S. Ogawa, S. Ohta, H. Sugimoto, K. Shikata, H. Makino, Re-evaluation of exercise prescription for Japanese type 2 diabetic patients by ventilatory threshold, Diabetes Res. Clin. Pract. 50 (2000) 109 /115. K. Wasserman, B.J. Whipp, S.N. Koyl, W.L. Beaver, Anaerobic threshold and respiratory gas exchange during exercise, J. Appl. Physiol. 35 (1973) 236 /243. N. Miyatake, M. Fujii, H. Nishikawa, J. Wada, K. Shikata, H. Makino, I. Kimura, Clinical evaluation of muscle strength in 20 to 79 years-old obese Japanese, Diabetes Res. Clin. Pract. 48 (2000) 15 /21. N. Miyatake, H. Muta, C. Murota, M. Haga, M. Fujii, Bone status assessment in Japanese subjects using speed of sound along the tibia, Chin. Med. J. 115 (2002) 254 /257. R.R. Pate, M. Pratt, S.N. Blare, W.L. Haskell, C.A. Macera, C. Bouchard, D. Buchner, W. Ettinger, G.W. Heath, A.C. King, Physical activity and public health: a recommendation from the Center for Disease Control and Prevention and the American College of Sports Medicine, J. Am. Med. Assoc. 273 (1995) 402 /407. A. Kiyonaga, K. Arakawa, H. Tanaka, M. Shindo, Blood pressure and hormonal responses to aerobic exercise, Hypertension 7 (1985) 125 /131. D.R. Seals, H.G. Silverman, M.J. Reiling, K.P. Davy, Effect of regular aerobic exercise on elevated blood pressure in postmenopausal women, Am. J. Cardiol. 80 (1997) 49 /55. H. Tanaka, D.R. Bassett, Jr, E.T. Howley, D.L. Thompson, M. Ashraf, F.L. Rawson, Swimming training lowers
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
[22]
[23] [24]
[25]
[26]
[27]
the resting blood pressure in individuals with hypertension, J. Hypertens. 15 (1993) 651 /657. M. Motoyama, Y. Sunami, F. Kinoshita, A. Kiyonaga, H. Tanaka, M. Shindo, T. Irie, H. Urata, J. Sasaki, K. Arakawa, Blood pressure lowering effect of low intensity aerobic training in elderly hypertensive patients, Med. Sci. Sports Exerc. 30 (1998) 818 /823. G.M. Reaven, Role of insulin resistance in human disease, Diabetes 37 (1988) 1595 /1607. N.M. Kaplan, The deadly quartet; upperbody obesity, glucose intolerance, hypertriglyceridemia, and hypertension, Arch. Int. Med. 149 (1989) 1514 /1520. R.A. DeFronzo, E. Ferrannini, A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease, Diabetes Care 14 (1991) 173 /194. M.A. Banerji, N. Faridi, R. Arluri, R.L. Chaiken, H.E. Lebovits, Body composition, visceral fat, leptin, and insulin resistance in asian indian men, J. Clin. Endocrinol. Metab. 84 (1999) 137 /144. Y. Oshida, K. Yamanouchi, I. Ohsawa, K. Usui, J. Sato, M. Kajita, Y. Sato, Relationship between insulin and
[28]
[29]
[30] [31]
[32]
[33]
157
blood pressure in Japanese obese subjects, Intern. Med. 38 (1999) 467 /471. H. Kanai, K. Tokunaga, S. Fujioka, S. Yamashita, K. Kakeda-Takemura, Y. Matsuzawa, Decrease in intraabdominal visceral fat may reduce blood pressure in obese hypertensive women, Hypertension 27 (1996) 125 /129. W.B. Kannel, R.J. Garrison, A.L. Dannenberg, Secular blood pressure trends in normotensive persons: the Framingham study, Am. Heart J. 125 (1993) 1154 /1158. A.P. Rocchini, Cardiovasucular regulation in obesityinduced hypertension, Hypertension 19 (1992) I56 /I60. A.P. Rocchini, P.C. Moorehead, S. Deremer, T.L. Goodfriend, D.L. Ball, Hyperinsulinemia and the aldosterone and pressor responses to angiotensin II, Hypertension 15 (1990) 861 /866. J.M. Hagberg, J.J. Park, M.D. Brown, The role of exercise training in the treatment of hypertension: an update, Sports Med. 30 (2000) 193 /206. E. Anderson, A. Mark, The vasodilator action of insulin: implications for the insulin hypothesis of hypertension, Hypertension 21 (1993) 136 /141.
Daily exercise lowers blood pressure and reduces visceral adipose tissue areas in overweight Japanese men Nobuyuki Miyatake a,*, Kayo Takahashi b, Jun Wada c, Hidetaka Nishikawa a, Akie Morishita a, Hisao Suzuki b, Mie Kunitomi c, Hirofumi Makino c, Shohei Kira d, Masafumi Fujii a a
Okayama Southern Institute of Health, 408-1 Hirata, Okayama 700-0952, Japan b Faculty of Education, Okayama University, Okayama, Japan c Department of Medicine and Clinical Science, Okayama University Graduate School of Medicine and Dentistry, Okayama, Japan d Department of Public Health, Okayama University Graduate School of Medicine and Dentistry, Okayama, Japan Received 24 April 2003; received in revised form 16 June 2003; accepted 23 July 2003
Abstract Objective: To investigate the link between a reduction in blood pressure (BP) and daily exercise. Design: Crosssectional and longitudinal clinical intervention study with exercise education. Subjects: 43 overweight Japanese men aged 32 /59 years (BMI, 29.09/2.3 kg/m2) at baseline. Among the participants, a randomly selected 23 overweight men (BMI, 28.59/1.7) were further enrolled into the 10 months exercise program. Measurements: BP was measured every week and steps per day were also recorded every day throughout the observation period. Fat distribution was evaluated by visceral fat (V) and subcutaneous fat (S) areas measured with computed tomography (CT) scanning at umbilical level, at before, 5 months and after intervention. Anthropometric parameters were also measured at same point. Aerobic exercise level, muscle strength, flexibility and calorie intake and insulin resistance (HOMA index) were investigated at before and after the study. Results: In a cross sectional analysis, systolic BP (SBP) and diastolic BP (DBP) were significantly correlated with body composition. In a second longitudinal analysis, SBP was significantly reduced at 2 months and DBP was also reduced at 3 months, and almost maintained until the end of the observation period. Increasing daily walking was observed in 3 months and maintained until 10 months. Body composition, aerobic exercise level, muscle strength, flexibility and insulin resistance were significantly improved. There was positive correlation between DDBP and Dvisceral fat area (1 /5, 5 /10, 1 /10 months). By stepwise multiple regression analysis, only Dvisceral fat area was independently related to DDBP at a significant level (1 /10 months: DDBP / /0.608/ 0.105Dvisceral fat area, r2 /0.227, P /0.0334). Conclusion: The present study indicated daily exercise lowers BP and visceral fat area is the critical factor for BP change. # 2003 Elsevier Ireland Ltd. All rights reserved. Keywords: Visceral adipose tissue; Anthropometric parameters; Computed tomography
* Corresponding author. Tel.: /81-86-246-6250; fax: /81-86-246-6331. E-mail address: [email protected] (N. Miyatake). 0168-8227/03/$ - see front matter # 2003 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/S0168-8227(03)00176-1
150
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
1. Introduction It has been shown that a number of obese subjects have a high mortality rate [1], and are associated with atherogenic risk factors, such as hypertension, coronary heart disease, diabetes mellitus and dyslipidemia [2,3]. Recent advances in our understanding of the pathophysiology of obesity convinces us that intra-abdominal or visceral adipose tissue accumulation is closely related to insulin resistance and the development of atherosclerosis [4,5]. In addition, the modern life style of a high-calorie diet and reduced physical activities are closely related to the increasing population of obese subjects. In order to provide proper management and control of obesity, the exact assessments of obesity as well as the development of effective treatments are required. In this respect, physical exercise greatly improves insulin action [6], and continued exercise is, therefore, recommended as a supplemental form of therapy to a specific diet treatment for obese subjects. However, it is important to clarify how exercise program induced weight loss is associated with comparable reductions in blood pressure (BP), and what is the critical factor of BP change. In this study, we investigated the effectiveness of daily exercise on BP, body composition, insulin resistance and physical fitness in overweight Japanese men.
2. Subjects and methods 2.1. Subjects Japanese overweight men (n/43), aged 32/59 years (45.29/7.5) were enrolled into this study with written informed consent. Overweight was diagnosed according to the criteria of WHO [7] and the average body mass index (BMI) of overweight subjects was 29.09/2.3 (26.4/37.8), respectively. No subjects received any medications for diabetes, hypertention, and/or dyslipidemia throughout the observation period. In a first cross-sectional analysis, we used baseline data on 43 overweight subjects (Table 1), aged
Table 1 Clinical profiles of subjects Number of subjects Age Body weight (kg) BMI (kg/m2) Body fat percentage (%) Waist circumference (cm) Hip circumference (cm) Waist hip ratio Visceral fat area (cm) Subcutaneous fat area (cm) SBP (mmHg) DBP (mmHg)
43 4.5.29/7.5 82.79/7.9 29.09/2.3 30.39/4.5 95.49/5.9 100.19/3.9 0.959/0.04 121.19/51.5 154.69/46.2 141.3/10.9 86.29/8.3
Mean9/S.D.
32/59 years, and investigated the relationships among body composition and BP. In a second longitudinal analysis, we used follow-up data of 23 subjects (47.19/6.9 years) randomly selected from 43 overweight participants, who met the following criteria: (1) no electrocardiogram changes in response to exercise, (2) a repeat CT scanning at follow-up, (3) a follow up duration of 10 months, and (4) joining exercise program at Okayama Southern Institute of Health. They visited Okayama Southern Institute of Health on a weekly basis and were monitored for 10 months. All of the subjects were instructed not to change eating habits, and trained nutritionists determined total calorie intake using food diaries before and after the 10 months follow up. Daily steps were also measured by pedometer (WZ100A, SEIKO Corporation, Japan) and the average of every month was monitored throughout the follow up period. Subjects joined an exercise program (%HRmax: 50 /65) at Okayama Southern Institute of Health every week. In addition, they were instructed to check daily steps every day and increase their daily walk at least 1000 steps besides the daily walk at baseline. Thus a negative energy balance would be induced by exercise. In addition, to evaluate the effect of daily exercise, anthropometric parameters and fat distribution were measured at before, 5 months and after the study. Aerobic exercise, muscle strength, flexibility and insulin resistance were also measured at before and after the study.
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
2.2. BP measurements Every week, BP of each participant was measured after resting at least 15 min in a sitting position before the exercise program at Okayama Southern Institute of Health, and the average of every month was recorded. Hypertension was diagnosed according to the WHO criteria.
151
measured at the widest circumferences over the trochanter in standing subjects after normal expiration. Body fat percentage was measured by an air displacement plethysmograph called the BOD POD Body Composition System (Life Measurement Instruments, Concord, CA) [11,12].
2.6. Aerobic exercise level 2.3. Blood sampling and hormone assays After subjects fasted overnight for 10 /12 h, we collected blood samples in order to determine serum levels of insulin and plasma glucose. Serum insulin was measured by immunoradiometric assay (IRMA) using INSULIN RIABEAD II (DAINABOT, Tokyo, Japan). Plasma glucose was measured by using the glucose-oxidant method. The insulin resistance was evaluated using the homeostasis model assessment, the HOMA index [fasting plasma glucose (mg/dl) /fasting serum insulin (mU/ml)/405], according to the method developed by Matthews et al. [8]. 2.4. Visceral and subcutaneous fat areas The intra-abdominal visceral fat and the subcutaneous fat areas were measured by computed tomography (CT) scanned at the umbilical [9]. CT films were converted into digital images and both visceral and subcutaneous fat areas were measured with image analysis software OPTIMAS version 6.5 (Media Cybernetics, Silver Spring, MD, USA). The intraperitoneal area with the same density as the subcutaneous fat layer was defined as the visceral fat area [10]. 2.5. Anthropometric and body composition measurements Their anthropometric and body composition were evaluated by using the following respective parameters such as, height, body weight, BMI, waist circumference, hip circumference, waist hip ratio and body fat percentage. BMI was calculated by weight/[height]2 (kg/m2). The waist circumference was measured midway between the lower rib margin and the iliac crest and the hip was
An incremental sub-maximal exercise test was done on an electrically stationary upright cycle ergometer (Excalibur V2.0, Lode BV, Groningen, Netherlands) to estimate the aerobic exercise level of the subjects [13,14]. The height of the seat was adjusted for each subject to form a knee joint angle of 160/1658 with the bikes gear in the lowest position. Each subject was fitted with a cardiopulmonary gas exchange system (Oxycon Alpha, Mijnhrdt b.v., Netherlands) to collect respiratory gas and a microcomputer for on-line calculations. Their heart rates and BP were continuously measured, using an auscultator with a pressure cuff around the upper arm connected to a mercury sphygmomanometer. Ventilatory threshold (VT) was defined according to Wasserman’s formula [15] which was recommended for the parameter of aerobic exercise level.
2.7. Muscle strength To assess their muscle strength, grip and leg strength were measured at baseline and 10 months. Grip strength was measured by using the conventional method, while leg strength was measured by COMBIT CB-1 (MINATO, Japan). Leg strength was measured as follows: the subject sat in chair, grasping the armrest in order to fix the body position. Then the dynamometer was attached to the subject’s ankle joint by a strap, next they extended the leg to 608. In order to standardize the influence of the total body weight, we employed the weight bearing index (WBI), which was calculated by leg strength (kg)/body weight (kg) [16,17]. WBI is closely related to exercise capacity e.g. speed of walking up stairs, getting up from a chair as well as gait speed.
152
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
2.8. Flexibility To evaluate the flexibility of all the participants, they were measured as follows. Sit-and-reach measurements were obtained to assess the overall flexibility in the forward flexion, with the measurements recorded as the distance (in cm) between the fingertips and toes. The subject’s knees were kept straight throughout the test and ankles were maintained at 908 by having the soles of the feet pressed against a board perpendicular to the sitting surface [13]. 2.9. Statistical analysis All data are expressed as mean9/standard deviation (S.D.) values. Statistical analysis were performed by paired t-test, repeated measure ANOVA, Fisher’s PLSD and x2-test: P B/0.05 was considered to be statistically significant. The Pearson’s correlation coefficients were calculated as well as tested for significance of the linear relationship among continuous variables. Furthermore stepwise multiple regression analysis was performed to determine what factors correlated with the changes in BP.
3. Results In a first cross-sectional analysis, SBP was significantly correlated with body weight, BMI, waist circumference, waist hip ratio and visceral fat area. DBP was also correlated with BMI, body fat percentage, waist circumference, waist hip ratio and visceral fat area (Table 2). In a second longitudinal analysis, clinical profiles and changes of subjects were summarized in Table 3. There was no significant change in calorie intake, and additional negative energy balance would be induced by daily exercise. After 10 months exercise education, SBP and DBP were significantly reduced (SBP: pre 140.39/ 13.6 mmHg vs. post 135.29/10.5 mmHg, DBP: pre 86.29/10.0 mmHg vs. post 82.29/8.1 mmHg P B/ 0.05). The number of patients with hypertension was also significantly reduced (Table 4). We investigated the change in BP with exercise educa-
Table 2 Simple correlation analysis between BP and body composition SBP
Body weight (kg) BMI (kg/m2) Body fat percentage (%) Waist circumference (cm) Hip circumference (cm) Waist hip ratio Visceral fat area (cm2) Subcutaneous fat area (cm2)
DBP
r
P
r
0.306 0.417 0.244 0.455 0.286 0.370 0.336 0.169
* **
0.211 0.374 0.328 0.405 0.281 0.309 0.425 0.061
** * *
P
* **
**
*, P B/0.05; **, P B/0.01.
tion every month. SBP was significantly reduced at 2 months and DBP was also reduced at 3 months, and almost maintained until the end of the observation period (Fig. 1). In anthropometric and body composition measurements, body weight, BMI, body fat percentage, waist circumference, visceral fat areas and subcutaneous fat areas were significantly reduced at 5 months and maintained until the end of the study (Table 3). There was remarkable change in aerobic exercise level and WBI, blood sugar, insulin and also in HOMA index. Steps per day was remarkably increased with exercise education (pre: 73899/2576 vs. post: 90709/3359 P B/0.01) and increasing daily walking was noted in 3 months and maintained until 10 months (Fig. 2). We also studied the relationship between DBP (DBP represents the positive changes in BP) and Dbody composition (Dbody composition represents the positive changes in body composition) (Tables 5/7). There was a positive correlation between DDBP and Dvisceral fat area (1 /5 months: r /0.423, P B/0.05, 5 /10 months: r / 0.536, P B/0.05, 1 /10 months: r /0.477, P B/ 0.05). We also used stepwise multiple regression analysis to evaluate the effect of Dbody composition on DDBP and found that only Dvisceral adipose fat area was independently related to DDBP at a significant level (1 /10 months: DDBP / /0.608/0.105Dvisceral fat area, r2 / 0.227, P /0.0334). Although DSBP did not significantly correlate with the parameters of Dbody composition, the correlation rate between DSBP
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
153
Table 3 Clinical profiles and changes in overweight subjects with exercise education
Body weight (kg) BMI (kg/m2) Body fat percentage (%) Waist circumference (cm) Hip circumference (cm) Waist hip ratio Visceral fat area (cm2) Subcutaneous fat area (cm2) Aerobic exercise level (ml/kg per min) Grip strength (right) (kg) Grip strength (left) (kg) WBI Flexibility (cm) Blood sugar (mg/dl) Insulin (mU/ml) HOMAindex Calorie intake (kcal/day)
Pre (1 month)
5 months
Post (10 months)
82.09/7.7 28.59/1.7 29.19/3.4 93.59/4.3 99.49/4.1 0.949/0.03 108.79/49.1 147.79/36 14.49/2.1 48.99/6.5 45.19/7.5 0.899/0.15 6.79/9.8 105.09/14.1 11.19/5.3 2.869/1.38 19489/398
79.59/8.1** 27.69/1.8** 25.89/5.0** 91.29/4.5** 98.19/0.05 0.939/0.05 85.99/40.9** 119.79/43.0**
79.09/8.5** 27.59/2.0** 26.69/4.2** 89.99/5.4** 98.39/4.1 0.929/0.04** 87.09/43.1** 122.69/38.7** 15.99/2.5** 48.19/7.6 44.99/6.7** 1.029/0.17 7.79/ 9.6* 98.49/10.8* 8.69/3.7* 2.079/0.86** 19229/365
Mean9/S.D.; *, P B/0.05 vs. pre; **, P B/0.01 vs. pre. Table 4 Change in patients with hypertension
Hypertension (/) Hypertension ( /)
Pre
Post
12 11
4 19
P B/0.05.
and Dvisceral fat area was comparatively high, but not significant (1 /5 months: r /0.379, P /0.0743, 5 /10 months: r /0.239, P/0.2963, 1 /10 months: r /0.367, P /0.1021) (Tables 5 /7).
moderate-intensity physical activity on most, and preferably all, days of the week [18]. In some literatures, exercise programs including walking, running, cycling, and swimming have demonstrated significant BP lowering effects in hypertensive individuals [19 /22]. However, most of them were designed for short duration and the program could not be performed easily. In this study, exercise education, i.e. regular exercise once a week at institute and increasing daily walk at least 1000 steps besides the daily walk have lowered BP Table 5 Simple correlation analysis between DBP and Dbody composition (1 /5 months)
4. Discussion It is well known that exercise is recommended as a supplemental form of therapy to a specific diet treatment for obese subjects. In addition, regular exercise lowers BP in patients with hypertension. The American College of Sports Medicine and Centers for Disease Control and Prevention (ACSM-CDC) developed a physical activity recommendation geared toward getting more people active. This guideline recommends that every US adult should accumulate at least 30 min of
DSBP R DBody weight (kg) DBMI (kg/m2) DBody fat percentage (%) DWaist circumference (cm) DHip circumference (cm) DWaist hip ratio DVisceral fat area (cm2) DSubcutaneous fat area (cm2) *, P B/0.05.
/0.159 /0.161 0.038 /0.089 0.052 /0.140 0.379 /0.070
DDBP P
r 0.021 0.021 0.087 0.070 0.055 0.025 0.423 0.140
P
*
154
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
Fig. 1. Time course change of SBP and DBP in Japanese overweight men with exercise education program (n/23). Data are indicated by mean9/S.D.; *, P B/0.05 vs. 1 month, #, P B/0.05 vs. 2 months, P B/0.05 vs. 3 months, /, P B/0.05 vs. 4 months.
significantly in overweight Japanese men. We monitored daily steps every day and monitored BP every week for an extended duration of 10 months. According to daily steps, overweight Japanese men were free to accumulate those steps Table 6 Simple correlation analysis between DBP and Dbody composition (5 /10 months) DSBP r DBody weight (kg) DBMI (kg/m2) DBody fat percentage (%) DWaist circumference (cm) DHip circumference (cm) DWaist hip ratio DVisceral fat area (cm2) DSubcutaneous fat area (cm2) *, P B/0.05.
0.244 0.234 0.001 0.232 0.071 0.114 0.239 0.307
DDBP P
r 0.105 0.093 0.065 /0.046 /0.154 0.083 0.536 0.219
P
*
in whatever way fit their life style, and no intensity recommendation was given. Overweight Japanese men increased their walking by an average of 1681 steps per day. It is obvious that obesity, especially excess of body fat, is closely related to hypertension, type 2 diabetes mellitus, dyslipidemia, and coronary heart disease and the underlying insulin resistance is considered to play a central role of arteriosclerosis [23 /25]. It has been shown that when visceral fat becomes enlarged, several bioactive compounds are produced in the adipose tissue i.e. free fatty acids, tumor necrosis factor alpha, leptin, and plasminogen activator inhibitor-1. These compounds may be involved in the pathogenesis of some of the complication [26]. According to the relationship between visceral fat and hypertension, Oshida Y et al. reported that insulin is an important factor in BP elevation in older obese subjects [27]. Kanai et al. reported that, by combination of low calorie diet and exercise
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
155
Fig. 2. Time course change of daily steps per day in Japanese overweight men with exercise education program (n/23). Data are indicated by mean9/S.D.; *, P B/0.05 vs. 1 month, #, P B/0.05 vs. 2 months, P B/0.05 vs. 3 months, /, P B/0.05 vs. 4 months.
therapy, improvement of glucose intolerance may be involved in BP change in obese hypertensive women [28]. We also found that improvement of insulin and HOMA index by daily exercise in Table 7 Simple correlation analysis between DBP and Dbody composition (1 /10 months) DSBP r DBody weight (kg) DBMI (kg/m2) DBody fat percentage (%) DWaist circumference (cm) DHip circumference (cm) DWaist hip ratio DVisceral fat area (cm2) DSubcutaneous fat area (cm2) P B/0.05.
/0.056 /0.055 /0.118 /0.141 /0.212 /0.025 0.367 /0.025
DDBP P r 0.128 0.126 0.017 0.037 /0.062 0.089 0.477 0.142
P
*
overweight Japanese men. Although we could not investigate other possible factors, it is obvious that visceral fat is closely linked to hypertension. The depressor effect of exercise has been attributed to factors known to influence BP such as body composition, insulin levels and diet [29 /31]. According to the body composition, some studies have shown exercise to lower BP in hypertensives independent of body mass changes [19 /22]. Also, a recent review by Hagberg et al. [32] reported that no significant correlation of 0.11 between the reduction in SBP and the reduction in body mass in 61 studies that reported body weight changes in hypertensives with exercise training. The authors concluded that the exercise training-induced reductions in SBP and DBP do not appear to be the result of weight changes with exercise. In our study, DBP was not correlated with Dbody weight as previous studies. However, there was significant correlation between DDBP and Dvisceral fat area
156
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
and only Dvisceral fat area was the determinant factor of DDBP by multiple regression analysis with long-term daily exercise. In addition, the correlation rate between DSBP and Dvisceral fat area was comparatively high, but not significant. Although other factors may strongly affect on DSBP with daily exercise [33], visceral fat not body weight is the critical factor of changes in BP in overweight Japanese men, and reducing visceral fat is important for preventing and improving BP in overweight Japanese men. In conclusion, BP was reduced by daily exercise for 10 months, and visceral fat is critically involved in BP change in overweight Japanese men.
[8]
[9]
[10]
[11]
Acknowledgements
[12]
This research was supported in part by Health Sciences Research Grants for ‘‘Research on Health Services’’ from the Ministry of Health, Labor and Welfare, Japan.
[13]
[14]
References [1] L.V. Sjostrom, Mortality of severely obese subjects, Am. J. Clin. Nutr. 55 (Suppl. 2) (1992) 516S /523S. [2] L.V. Sjostrom, Morbidity of severely obese subjects, Am. J. Clin. Nutr. 55 (Suppl. 2) (1992) 508S /515S. [3] M.C. Pouliot, J.P. Despres, A. Nadeeau, S. Moorjani, D. Prud’Homme, P.J. Lupien, A. Tremblay, C. Bouchard, Visceral obesity in men. Associations with glucose tolerance, plasma insulin, and lipoprotein levels, Diabetes 4 (1992) 826 /834. [4] D. Sparrow, G.A. Borkan, S.G. Gerzof, C. Wisniewski, C.K. Silbert, Relationship of body fat distribution to glucose tolerance: results of computed tomography in male participants of the normative aging study, Diabetes 35 (1986) 411 /415. [5] S. Fujioka, Y. Matsuzawa, K. Tokunaga, S. Tarui, Contribution of intra-abdominal visceral fat accumulation to the impairment of glucose and lipid metabolism in human obesity, Metabolism 36 (1987) 54 /59. [6] Y. Oshida, K. Yamanouchi, S. Hayamizu, Y. Sato, Longterm mild jogging increases insulin action despite no influence on body mass index or VO2max, J. Appl. Physiol. 66 (1989) 2206 /2210. [7] NHBI obesity education initiative expert panel on the identification, evaluation, and treatment of overweight and obesity in adults: clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in
[15]
[16]
[17]
[18]
[19]
[20]
[21]
adults */the evidence report, Obesity Res. 6 (1998) 51S / 63S. D.R. Matthews, J.P. Hosker, A.S. Rudenski, B.A. Naylor, D.F. Treacher, R.C. Turner, Homeostasis model assessment: insulin resistance and b-cell function from fasting plasma glucose and insulin concentrations in man, Diabetologia 28 (1985) 412 /419. K. Tokunaga, Y. Matsuzawa, K. Ishikawa, S. Tarui, A novel technique for the determination of body fat by computed tomography, Int. J. Obes. 7 (1983) 437 /445. M. Kunitomi, J. Wada, K. Takahashi, Y. Tsuchiyama, Y. Mimura, K. Hida, N. Miyatake, M. Fujii, S. Kira, K. Shikata, H. Makino, Relationship between reduced serum IGF-1 levels and accumulation of visceral fat in Japanese men, Int. J. Obes. Metab. Disord. 26 (2002) 361 /369. N. Miyatake, K. Nonaka, M. Fujii, A new air displacement plethysmograph for the determination of Japanese body composition, Diabetes Obes. Metab. 1 (1999) 347 / 351. M.A. Mccrory, T.D. Gomez, E.M. Bernauer, P.A. Mole, Evaluation of a new air displacement plethysmograph for measuring human body composition, Med. Sci. Sports Exerc. 27 (1995) 1686 /1691. N. Miyatake, H. Nishikawa, M. Fujii, Clinical evaluation of physical fitness in male obese Japanese, Chin. Med. J. 114 (2001) 707 /710. M. Kunitomi, K. Takahashi, J. Wada, H. Suzuki, N. Miyatake, S. Ogawa, S. Ohta, H. Sugimoto, K. Shikata, H. Makino, Re-evaluation of exercise prescription for Japanese type 2 diabetic patients by ventilatory threshold, Diabetes Res. Clin. Pract. 50 (2000) 109 /115. K. Wasserman, B.J. Whipp, S.N. Koyl, W.L. Beaver, Anaerobic threshold and respiratory gas exchange during exercise, J. Appl. Physiol. 35 (1973) 236 /243. N. Miyatake, M. Fujii, H. Nishikawa, J. Wada, K. Shikata, H. Makino, I. Kimura, Clinical evaluation of muscle strength in 20 to 79 years-old obese Japanese, Diabetes Res. Clin. Pract. 48 (2000) 15 /21. N. Miyatake, H. Muta, C. Murota, M. Haga, M. Fujii, Bone status assessment in Japanese subjects using speed of sound along the tibia, Chin. Med. J. 115 (2002) 254 /257. R.R. Pate, M. Pratt, S.N. Blare, W.L. Haskell, C.A. Macera, C. Bouchard, D. Buchner, W. Ettinger, G.W. Heath, A.C. King, Physical activity and public health: a recommendation from the Center for Disease Control and Prevention and the American College of Sports Medicine, J. Am. Med. Assoc. 273 (1995) 402 /407. A. Kiyonaga, K. Arakawa, H. Tanaka, M. Shindo, Blood pressure and hormonal responses to aerobic exercise, Hypertension 7 (1985) 125 /131. D.R. Seals, H.G. Silverman, M.J. Reiling, K.P. Davy, Effect of regular aerobic exercise on elevated blood pressure in postmenopausal women, Am. J. Cardiol. 80 (1997) 49 /55. H. Tanaka, D.R. Bassett, Jr, E.T. Howley, D.L. Thompson, M. Ashraf, F.L. Rawson, Swimming training lowers
N. Miyatake et al. / Diabetes Research and Clinical Practice 62 (2003) 149 /157
[22]
[23] [24]
[25]
[26]
[27]
the resting blood pressure in individuals with hypertension, J. Hypertens. 15 (1993) 651 /657. M. Motoyama, Y. Sunami, F. Kinoshita, A. Kiyonaga, H. Tanaka, M. Shindo, T. Irie, H. Urata, J. Sasaki, K. Arakawa, Blood pressure lowering effect of low intensity aerobic training in elderly hypertensive patients, Med. Sci. Sports Exerc. 30 (1998) 818 /823. G.M. Reaven, Role of insulin resistance in human disease, Diabetes 37 (1988) 1595 /1607. N.M. Kaplan, The deadly quartet; upperbody obesity, glucose intolerance, hypertriglyceridemia, and hypertension, Arch. Int. Med. 149 (1989) 1514 /1520. R.A. DeFronzo, E. Ferrannini, A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease, Diabetes Care 14 (1991) 173 /194. M.A. Banerji, N. Faridi, R. Arluri, R.L. Chaiken, H.E. Lebovits, Body composition, visceral fat, leptin, and insulin resistance in asian indian men, J. Clin. Endocrinol. Metab. 84 (1999) 137 /144. Y. Oshida, K. Yamanouchi, I. Ohsawa, K. Usui, J. Sato, M. Kajita, Y. Sato, Relationship between insulin and
[28]
[29]
[30] [31]
[32]
[33]
157
blood pressure in Japanese obese subjects, Intern. Med. 38 (1999) 467 /471. H. Kanai, K. Tokunaga, S. Fujioka, S. Yamashita, K. Kakeda-Takemura, Y. Matsuzawa, Decrease in intraabdominal visceral fat may reduce blood pressure in obese hypertensive women, Hypertension 27 (1996) 125 /129. W.B. Kannel, R.J. Garrison, A.L. Dannenberg, Secular blood pressure trends in normotensive persons: the Framingham study, Am. Heart J. 125 (1993) 1154 /1158. A.P. Rocchini, Cardiovasucular regulation in obesityinduced hypertension, Hypertension 19 (1992) I56 /I60. A.P. Rocchini, P.C. Moorehead, S. Deremer, T.L. Goodfriend, D.L. Ball, Hyperinsulinemia and the aldosterone and pressor responses to angiotensin II, Hypertension 15 (1990) 861 /866. J.M. Hagberg, J.J. Park, M.D. Brown, The role of exercise training in the treatment of hypertension: an update, Sports Med. 30 (2000) 193 /206. E. Anderson, A. Mark, The vasodilator action of insulin: implications for the insulin hypothesis of hypertension, Hypertension 21 (1993) 136 /141.