The body constitution of current Japanese students has improved from that in the past years (18). Mean height and weight at 16 yr in 1986 were 169.4 cm and 60.4 kg for males and 157.5 cm and 52.8 kg for females, and those in 2006 were 170.0 cm and 62.0 kg for males and 157.8 cm and 53.4 kg for females, respectively (18). However, the physical strength of current Japanese students has dramatically decreased. In 1986, for 16-yr-olds, the mean time for running a 50-m sprint and mean distance for throwing a handball were 7.34 s and 28.0 m, respectively, among males and 8.78 s and 16.8 m, respectively, among females; however, the same measurements in 2006 were 7.45 s and 26.4 m, respectively, among males and 9.02 s and 14.6 m, respectively, among females (15). The Ministry of Education, Culture, Sports, Science, and Technology has recently warned that current Japanese students are unwilling to play sports, belong to a sports club at school, or participate in daily exercise (18).
The dramatic changes of body constitution and physical strength among current Japanese students were identified, but there have been no official body composition data for Japanese students, except for height, weight, and seated height (18). Body proportion and fat accumulation dramatically change throughout the pubertal years (23,24). The growth pattern of body composition differs between males and females (10). Males gain greater amounts of fat-free mass (FFM), which consists of bone and muscle, and females acquire significantly more fat mass (FM) (10,23,24). The most important step in elucidating the change of physique and physical strength among current Japanese students is to investigate the dynamics of FFM that are most strongly associated with physical exercise and sports (4). Especially, it has been widely recognized that the peak bone mass (PBM) in Japanese populations can be reached as late as approximately 20 yr (12,17). However, we hypothesized that a change of PBM has occurred among Japanese students on the basis of Ministry of Education, Culture, Sports, Science, and Technology reports (15,18). Also, two different growth patterns of FFM and PBM may be observed whether students engage in habitual physical activity or not. The PBM and FFM of students who belong to a sports club may develop with age; however, those of students who are not willing to do sport may be inhibited.
Thus, we evaluated the effect of exercise on bone status and body composition in current Japanese students using air displacement plethysmography (ADP) and quantitative ultrasound (QUS). The Bod Pod body composition system (Life Measurement Inc. Concord, CA), which uses ADP, can precisely assess body fat percentage (%BF) as well as dual-energy x-ray absorptiometry, which is the gold standard for assessing body composition and bone status (28). ADP is a noninvasive and accurate method for assessing %BF (6,19). Compared with dual-energy x-ray absorptiometry, QUS uses less ionizing radiation and is lower in cost, simpler, and a more portable method for evaluating bone status (13). The Food and Drug Administration approved the use of QUS for assessing bone status (8,22). QUS provides effective information about bone condition, such as broadband ultrasound attenuation (BUA (dB·MHz−1)), speed of sound (SOS (m·s−1)), and stiffness (30). BUA reflects structural factors, such as pore size and number, and SOS reflects bone architecture (25,26). Stiffness is a linear combination of BUA and SOS and is considered to be a more robust indicator of bone density than either parameter by itself (27).
The aim of this study was to examine the dynamics of FFM and stiffness in relation to aging and training in current Japanese students. It is currently unclear whether exercise will help to accumulate more overall PBM in childhood and adolescence (4). Furthermore, there has been no updated national report about bone growth patterns in Japanese students. This study therefore may contribute to improve national guidelines in Japanese school health.
The study protocol was approved by the ethics committee of the University of Nagasaki (Nagasaki, Japan). The purpose and procedures of this study were explained, and informed consent was obtained from both the participants and their parents. Data were obtained from two high school students and university students in Nagasaki Prefecture, Japan. We conducted the cross-sectional study with an enrollment of a total of 710 subjects (491 males and 219 females between 15 and 20 yr). We further divided the subjects into two groups: an exercise group (288 males and 87 females between 15 and 20 yr) and a nonexercise group (203 males and 132 females between 15 and 20 yr). Students who regularly engaged in physical exercise more than three times per week or who belonged to a sports club, including karate, kendo, soccer, judo, swimming, softball, table tennis, basketball, badminton, volleyball, boat, baseball, rugby, and track and field, were placed into the exercise group. Students who were excluded from the exercise group were assigned to the nonexercise group.
Height was measured to the nearest millimeter, and body weight was measured to the nearest gram. Body weight was calculated after subtracting the weight of the swimsuit. Body mass index (BMI) was determined as the Quetelet index (kg·m−2). Waist and hip circumferences were measured, and the waist-to-hip ratio (W/H) was calculated. %BF in subjects was measured using ADP according to the manufacturer’s instructions and recommendations, with each subject wearing tight-fitting swimsuits and a swim cap (Bod Pod MAB-1000 Ver 1.68; Life Measurement Instruments, Concord, CA). Body volume was measured indirectly by determining the pressure change caused by the volume of air displacement when the subject was seated inside a tightly closed chamber. A single ADP procedure consisted of two measurements of body volume unless they differed by more than 150 mL, in which case the system required that a third measurement be performed. Values for these two raw volume measurements, which were left uncorrected for the effects on body volume of isothermal conditions created by the subject due to thoracic gas and skin surface area, appeared transiently on the screen during the procedure and were recorded. Predicted lung volume was used to calculate body volume. Appropriate correlations for thoracic gas volume and skin surface area artifacts in children and adolescents were applied to this raw measurement to obtain an actual body volume. The final results are reported as the average of the raw measurements. For the measurement of thoracic gas volume, the subjects were connected to a breathing circuit in the system. The subjects were instructed to take full breaths, and the real-time breathing record was displayed on the computer monitor. The examiner observed the breathing monitor and, on expiration, verbally signaled the subject just before airway occlusion. The subject contracted and relaxed the diaphragm muscle while the airway and chamber pressures were simultaneously recorded. Thoracic gas volume procedures needed to be performed only once; however, some subjects needed two or three times to obtain a satisfactory result. Data on body density were converted to body composition values. The formula of Brozek et al. (5) was used to estimate %BF from body density. FM and FFM were derived from %BF and body weight. QUS measurements of the right calcaneus were performed using the Achilles ultrasound bone densitometer (A-1000; Lunar Corporation, Madison, WI). After cleaning the skin with diluted alcohol, the subject’s heel was positioned in a small measurement device. The device uses 0.5 MHz that is electrically excited to produce a broadband spectrum. The ultrasonic wave is transmitted through the heel and detected by a receiving transducer. Three parameters were measured using this device: BUA, which corresponds to the frequency-dependent attenuation of the ultrasonic wave as it passes through the heel; SOS, which is the velocity of the ultrasonic wave as it passes through the heel; and stiffness, which is a combination of the two previous parameters. Stiffness, a function of the BUA and SOS measurements, was calculated by the following formula: 0.67 BUA + 0.28 SOS − 420 (7).
The anthropometric variables and bone statuses are expressed as mean ± SD. The proportions of gender and age between the exercise group and the nonexercise group were analyzed by a chi-square test. Differences in body composition and bone status between the exercise and nonexercise groups were evaluated using ANOVA. Differences in stiffness during each year were assessed using Bonferroni correction. The Pearson correlation coefficient (r) was also used to assess associations among each measurement variable for each sex and in each exercise group. The analyses between stiffness and age and between stiffness and FFM were presented as scatterplots and linear regression lines. Values of P < 0.05 were considered statistically significant. All statistical analyses were performed using the SPSS v 18.0 software for Windows (SPSS Japan, Tokyo, Japan).
Comparisons of body composition and bone status between the exercise and the nonexercise groups.
The overall mean height and weight for both the exercise and nonexercise groups were 170.0 cm and 60.4 kg, respectively, in males and 157.8 cm and 51.2 kg, respectively, in females. Sample heights and weights did not differ significantly from the values in the 2008 National Nutrition Survey (Ministry of Health, Labour and Welfare: 170.2 cm and 60.3 kg for males 15–20 yr and 157.9 cm and 51.1 kg for females in the same age range) (16). The proportions of gender and age were not significantly different between the exercise group and nonexercise group. Table 1 shows demographic, anthropometric, and body composition data in the exercise group and nonexercise group in both sexes. Age, height, weight, BMI, waist circumference, hip circumference, W/H, lung volume, and body volume between the exercise and nonexercise groups were not significantly different in both sexes; however, FFM, SOS, BUA, and stiffness in the exercise group were statistically higher than those in the nonexercise group (P < 0.05). Both FM and %BF in the exercise group were significantly lower than those in the nonexercise group for both sexes (P < 0.01).
Associations between age and stiffness in the exercise group and nonexercise group.
Figures 1 and 2 show associations between age and stiffness in males and females. In males, stiffness values at 15, 16, 17, 18, 19, and 20 yr were 106.3, 109.5, 112.7, 115.8, 119.0, and 122.2, respectively, in the exercise group and 94.2, 96.9, 99.6, 102.3, 105.0, and 107.8, respectively, in the nonexercise group (Fig. 1). The overall mean stiffness was significantly different between the exercise and the nonexercise groups (P < 0.001). Stiffness differed significantly between the exercise and the nonexercise groups in each age group (P < 0.01). In females, stiffness values at 15, 16, 17, 18, 19, and 20 yr were 91.2, 94.6, 97.9, 101.3, 104.7, and 108.1, respectively, in the exercise group and 95.0, 94.5, 93.9, 93.4, 92.8, and 92.3, respectively, in the nonexercise group (Fig. 2). The overall mean stiffness was significantly different between the exercise and nonexercise groups (P < 0.001); however, stiffness did not differ significantly between the exercise and nonexercise groups, except for the 19- and 20-yr group (P < 0.001).
Associations between FFM and stiffness in the exercise and nonexercise groups
Figures 3 and 4 present the associations between stiffness and FFM in males and females. In males, stiffness values at FFM of 40, 50, 60, and 70 kg were 99.0, 108.8, 118.5, and 128.2, respectively, in the exercise group and 90.2, 99.0, 107.9, and 116.7, respectively, in the nonexercise group (Fig. 3). In females, mean stiffness at FFM of 30, 40, and 50 kg was 90.7, 98.4, and 106.2, respectively, in the exercise group and 86.5, 94.1, and 101.7, respectively, in the nonexercise group (Fig. 4). In the same FFM range, stiffness in the exercise group was statistically higher than that in the nonexercise group for both sexes (P < 0.001).
Correlations between stiffness and anthropometric variables in the exercise and nonexercise groups.
Table 2 presents the correlations between stiffness and body composition divided into exercise and nonexercise groups. For both sexes, stiffness positively correlated with FFM in both the exercise and nonexercise groups (P < 0.01). Stiffness was negatively correlated with %BF and FM, except for among the nonexercise group in females (P < 0.05). In males, stiffness in both the exercise and nonexercise groups was positively correlated with age (P < 0.01) (Table 2 and Fig. 1). In females, stiffness was positively correlated with age in the exercise group (P < 0.001); however, it was negatively correlated with age in the nonexercise group (Table 2 and Fig. 2).
The School Health Survey in Japan, which investigates physical characteristics of school children, has been ongoing since 1900 (18). However, there have been no national data reported on the PBM growth curve for Japanese students. Our results clearly showed a trend of PBM, including the response to exercise in current Japanese students. Stiffness in the exercise group was significantly higher than that in the nonexercise group among young adults of both sexes. Routine physical exercise during childhood and adolescence can strongly influence the development of bone formation in both sexes. In 2008, 27.3% and 49.6% of male and female Japanese students, respectively, did not participate in sports clubs or recreational activities (16). In childhood and adolescence, sports and physical exercise are highly effective in supporting bone maintenance and bone formation, including the accumulation of minerals in addition to strengthening muscles and decreasing the amount of FM (4). These findings show that the difference in bone density between the exercise and nonexercise groups in Japanese students may widen.
This research shows that stiffness in males increased with age in both the nonexercise group and the exercise group. In females, stiffness increased with age in the exercise group. However, stiffness in the nonexercise group slowly decreased. This result shows that stiffness decreased with age among Japanese pubertal females who did not have a history of regular exercise. After PBM, bone resorption begins to outpace bone formation (23). These results suggest that currently, among Japanese females, PBM occurs earlier compared with previous reports (12,17). Also, a sex difference exists in relation to PBM. Our results showed that the relationship between FFM and stiffness persists with age in both genders; however, the relationship between age and stiffness in females does not hold until 20 yr. Furthermore, what is important in these results is that regular exercise or participating in sports clubs as children and adolescents is essential for the development of bone density. Recently, it was reported that the physical development of Japanese children gradually progressed until the age of 16 yr, at which time it could be considered complete (20). Our results also showed that PBM of current Japanese females might be advanced by about 5 yr. These findings suggest that a longitudinal and continuous exercise history from early childhood, especially in females, is essential for the increase of bone density.
Body weight was divided into two groups: FM and FFM (4,24). In this study, no statistical difference was observed in body weight between the exercise and nonexercise groups in both sexes. However, FFM was significantly higher in the exercise group than in the nonexercise group. FFM is the greatest contributor to bone density (2). Also, FFM is strongly enhanced by physical exercise and participation in sports activity (1). We conclude that an exercise-induced vigorous lifestyle contributes to an increase of FFM in the exercise group in this study. However, FM in the exercise group was significantly lower than that in the nonexercise group for both sexes because exercise is highly effective in decreasing the amount of FM (4).
To increase stiffness in childhood and adolescence is important for metabolic bone disease later in life, and an increase in PBM has been associated with a decreased risk for osteoporotic fractures (9). One strategy for preventing osteoporotic fractures may increase PBM in children and adolescents, counteracting age- and menopause-related bone loss (11). Primary prevention of osteoporosis in the elderly should aim to increase stiffness acquisition through physical activity during puberty (3). Peak bone accretion in both genders occurs during puberty (21,23). Pubertal body composition may predict adult body composition and affect future health (14). Thus, exercise habits throughout puberty play an important role in the increase of PBM and the prevention of osteoporotic fractures in later life.
Despite these compelling findings, several limitations are worthy of note. First, this study did not consist of the same number of participants in terms of gender, age group, and exercise distribution. Second, we were unable to perform endocrine diagnostic techniques. Third, we were unable to consider genetic factors, individual differences in growth pattern, and daily food habits for each participant. Fourth, we need to mention that the heel might not be the best indicator of BMD in the skeleton in the whole body. All sports will not stimulate BMD accretion in the heel. According to a previous research using QUS, BUA, SOS, and stiffness of soccer players and dancers with weight bearing exercise were significantly higher than those of swimmers (29). Finally, we were unable to consider an exercise history for each participant. It is quite likely that this study did not allow conclusions as to causality between the exercise group and the nonexercise group.
The current findings contribute to those of previous studies in several ways. We have demonstrated the effect of exercise in childhood and adolescence among Japanese students on bone status and body composition. Routine physical exercise during puberty plays an important role in the development of FFM and stiffness in both sexes. We also clarified sex differences in PBM and precocity of bone development in current Japanese students. In particular, bone density among females in childhood and adolescents who do not have regular sports habits slowly decreases with age. Thus, we suggest the establishment of a new Japanese school health policy involving physical exercise that aims to increase FFM, including bone density. This policy contributes not only to improve physical strength but also to prevent osteoporotic fractures later in life. Further studies are required to clarify variations in body composition in a larger population and a wider range of age groups.
This research was supported in part by the grant-in-aids for scientific research (B) (163701107) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
This research has not received other specific grants from any funding agency in the public, commercial, or not-for-profit sectors. Kazuo Minematsu, Masanori Noguchi, Satoshi Muraki, Rika Fukuda, Kensuke Goto, Kazumi Tagami, Motoyuki Yuasa, Eiji Marui, and Noriaki Tsunawake declare no conflicts of interest.
The authors thank all the participants and staff members who participated in this study.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
1. Abe T, Kojima K, Kearns CF, Yohena H, Fukuda J. Whole body muscle hypertrophy from resistance training: distribution and total mass. Br J Sports Med. 2003; 37 (6): 543–5.
2. Ackerman A, Thornton JC, Wang J, Pierson RN Jr, Horlick M. Sex difference in the effect of puberty on the relationship between fat mass
and bone mass in 926 healthy subjects, 6 to 18 years old. Obesity (Silver Spring). 2006; 14 (5): 819–25.
3. Anderson JJ, Rondano P, Holmes A. Roles of diet and physical activity in the prevention of osteoporosis. Scand J Rheumatol Suppl. 1996; 103: 65–74.
4. Borer KT. Physical activity in the prevention and amelioration of osteoporosis in women: interaction of mechanical, hormonal and dietary factors. Sports Med. 2005; 35 (9): 779–830.
5. Brozek J, Grande F, Anderson JT, Keys A. Densitometric analysis of body composition: revision of some quantitative assumptions. Ann N Y Acad Sci. 1963; 110: 113–40.
6. Collins MA, Millard-Stafford ML, Sparling PB, et al.. Evaluation of the BOD POD for assessing body fat in collegiate football players. Med Sci Sports Exerc. 1999; 31 (9): 1350–6.
7. Committee for Health Examination of Osteoporosis. Manual for the Prevention of Osteoporosis in Young Females. Tokyo (Japan): Health Care Bureau, Chuouhoki Publishing; 1995. 72 p. Japanese.
8. Compston JE, Cooper C, Kanis JA. Bone densitometry in clinical practice. BMJ. 1995; 310 (6993): 1507–10.
9. Cooper C, Javaid K, Westlake S, Harvey N, Dennison E. Developmental origins of osteoporotic fracture: the role of maternal vitamin D insufficiency. J Nutr. 2005; 135 (11): 2728–34S.
10. Hattori K, Tahara Y, Moji K, Aoyagi K, Furusawa T. Chart analysis of body composition change among pre- and postadolescent Japanese subjects assessed by underwater weighing method. Int J Obes Relat Metab Disord. 2004; 28 (4): 520–4.
11. Iwamoto J, Otaka Y, Kudo K, Takeda T, Uzawa M, Hirabayashi K. Efficacy of training program for ambulatory competence in elderly women. Keio J Med. 2004; 53 (2): 85–9.
12. Kaga M, Kamimura H. Bone mass in puberty. Clin Calcium. 2008; 18 (8): 1193–9. Japanese.
13. Krieg MA, Cornuz J, Ruffieux C, et al.. Comparison of three bone ultrasounds for the discrimination of subjects with and without osteoporotic fractures among 7562 elderly women. J Bone Miner Res. 2003; 18 (7): 1261–6.
14. Loomba-Albrecht LA, Styne DM. Effect of puberty on body composition. Curr Opin Endocrinol Diabetes Obes. 2009; 16 (1): 10–5.
15. Ministry of Education, Culture, Sports, Science, and Technology, Japan. School Health Survey in 2006. Tokyo (Japan): Lifelong Learning Policy Bureau, Analytical Research Planning Division; 2006. 209 p. Japanese.
16. Ministry of Health, Labour and Welfare, Japan. National Survey of the Physical Strength, Exercise Ability and Exercise Habits in 2008. Tokyo (Japan): Lifelong Learning Policy Bureau, Policy Planning and Coordination Division; 2008. 176 p. Japanese.
17. Ministry of Education, Culture, Sports, Science, and Technology, Japan. Dietary Habit in School Students. Tokyo (Japan): Sports and Youth Bureau, School Health Education Division; 2009. 48 p. Japanese.
18. Ministry of Education, Culture, Sports, Science, and Technology, Japan. School Health Survey in 2010. Tokyo (Japan): Lifelong Learning Policy Bureau, Analytical Research Planning Division; 2010. 209 p. Japanese.
19. Miyatake N, Takenami S, Kawasaki Y, Kunihashi Y, Nishikawa H, Numata T. Clinical evaluation of body fat in 11,833 Japanese measured by air displacement plethysmograph. Intern Med. 2005; 44 (7): 702–5.
20. Nohara T, Ueda M, Ohta A, Sugimoto T. Correlation of body growth and bone mineral density measured by ultrasound densitometry of the calcaneus in children and adolescents. Tohoku J Exp Med. 2009; 219 (1): 63–9.
21. Perez-Lopez FR, Chedraui P, Cuadros-Lopez JL. Bone mass gain during puberty and adolescence: deconstructing gender characteristics. Curr Med Chem. 2010; 17 (5): 453–66.
22. Prins SH, Jorgensen HL, Jorgensen LV, Hassager C. The role of quantitative ultrasound in the assessment of bone: a review. Clin Physiol. 1998; 18 (1): 3–17.
23. Sievogel RM, Demerath EW, Schubert C, et al.. Puberty and body composition. Horm Res. 2003; 60 (Suppl 1): 36–45.
24. Tahara Y, Moji K, Aoyagi K, et al.. Age-related pattern of body density and body composition in Japanese males and females, 11 and 18 years of age. Am J Hum Biol. 2002; 14 (3): 327–37.
25. Toussirot E, Michel F, Wendling D. Bone density
, ultrasound measurements and body composition in early ankylosing spondylitis. Rheumatology (Oxford). 2001; 40 (8): 882–8.
26. Toyras J, Nieminen MT, Kroger H, Jurvelin JS. Bone mineral density, ultrasound velocity, and broadband attenuation predict mechanical properties of trabecular bone differently. Bone. 2002; 31 (4): 503–7.
27. Wear KA, Armstrong DW 3rd. Relationships among calcaneal backscatter, attenuation, sound speed, hip bone mineral density, and age in normal adult women. J Acoust Soc Am. 2001; 110 (1): 573–8.
28. Weyers AM, Mazzetti SA, Love DM, Gomez AL, Kraemer WJ, Volek JS. Comparison of methods for assessing body composition changes during weight loss. Med Sci Sports Exerc. 2002; 34 (3): 497–502.
29. Yung PS, Lai YM, Tung PY, et al.. Effects of weight bearing and non-weight exercises on bone properties using calcaneal quantitative ultrasound. Br J Sports Med. 2005; 39 (8): 547–51.
30. Zhu ZQ, Liu W, Xu CL, Han SM, Zu SY, Zhu GJ. Ultrasound bone densitometry of the calcaneus in healthy Chinese children and adolescents. Osteoporos Int. 2007; 18 (4): 533–41.
Keywords:©2012The American College of Sports Medicine
BONE DENSITY; STIFFNESS; FAT MASS; FAT-FREE MASS; BODY FAT PERCENTAGE