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1 From the Department of Nutrition, Schools of Public Health and Medicine, University of North Carolina, Chapel Hill.
See corresponding Perspective on 1381.
INTRODUCTION
Skeletal development requires reasonable intakes of all the nutrients required by bone tissue, but energy and protein are critical for attainment of growth commensurate with hereditary determinants. Although clearly important for skeletal development, the amounts of calcium needed for optimizing skeletal mass and size remain difficult to determine. Many children in both developed and developing nations gain near-optimal skeletal mass and size with low calcium intakes, without adverse effects. A currently missing determinant in most considerations of requirements by nutritionists is the lifestyle variable of physical activity.
In this perspective, I attempt to incorporate the role of activity into the thinking about calcium requirements in the early stages of the life cycle, ie, the first 2 decades of life. Even though cells of soft tissues have essential needs for calcium ions to support life, the body's clearly overwhelming quantitative need for calcium resides in its skeletal utilization, not in its soft tissue uses. A greater bone mass gained early in life is now considered a critical factor in protecting against osteoporotic fractures later in life. The critical years for skeletal growth and accumulation of bone mass lie in the prepubertal and pubertal decade beginning at 10 y in girls (1).
MULTIPLE FACTOR CONTRIBUTIONS TO BONE
Epidemiology uses the concept of multifactorial etiology to understand causation of disease, eg, heart disease. The same concept can be applied to skeletal development. Many factors contribute to the growth of the various bones—growth not only in length but also in width or size, which varies as a result of these multiple factors. The difficulty with this approach arises from uncertainties about the relative significance of the variables, such as dietary calcium and physical activity. Nevertheless, statistical analyses such as multiple regression consider simultaneously many variables and attempt to quantitate their importance to bone outcomes, such as mass, area, and density. These statistical models never fully explain all the contributions to bone, especially the largely unknown hereditary contributions, which are estimated to be 60–80% for bone mass. However, these models do identify which variables consistently influence bone development in populations and assign approximate relative values of the importance of each variable. This approach provides a potential tool for assessing the contributions of various determinants of bone during the developmental phases of life.
EFFECT OF PHYSICAL ACTIVITY ON BONE
Physical activity as a contributor to bone development has been undervalued by researchers in the field of nutrition. Early investigators showed a strong relation between muscle and bone in males, especially in athletes and others who exercised regularly (2, 3). More recently, similar findings were reported for females (4), especially prepubertal girls (5). In general, high correlations exist between muscle mass and skeletal mass in exercising subjects. Under conditions of disuse and inactivity, both skeletal and muscle tissues atrophy, even in those who are in their growth periods.
In recent decades, scientific investigations have advanced understandings of the anatomic and functional bases of the muscle-bone relation. In exercising and physically active individuals, muscle strength or muscle mass is directly correlated with the mass of bone associated with the specific muscle or group of muscles (6). Increases in bone mass also accrue in parallel with incremental gains in muscle mass, as shown in Figure 1 (6).
FIGURE 1. . The linear relation between muscle mass (Psoas muscle of back) and bone mass (third lumbar vertebra), as determined by Doyle et al (6).
The early gain and later loss of skeletal mass is the normal sequence characteristic of human populations throughout the world (7). The achievement of peak bone mass is shown in Figure 2. Puberty has significant influences on changes in skeletal mass (8). Gains in skeletal muscle mass tend to be similar to gains in bone mass.
FIGURE 2. . The early gain of bone mass, as shown by Garn (7), consists of 3 phases: childhood growth; pubertal growth, including an important prepubertal period; and attainment of peak bone mass (PBM). If environmental conditions, such as diet and physical activity, are sufficient, bone mass accumulation will become optimal.
Mechanical loading of sufficient intensity promotes an increase in skeletal mass, especially during growth in the first 2 decades of life (9). The increase (or delta) in mass or density of bone tissue at a hypothetically mechanically loaded site, as illustrated in Figure 3, is in addition to the genetically determined mass of unloaded bone. Also, usual everyday physical activities of sufficient intensity may have an additional positive effect on skeletal mass.
FIGURE 3. . The postulated effects of physical activity on bone mass above a genetic baseline. Routine mechanical loading accounts for a proportion of the gain, and exercise activities can boost this gain higher, especially in the prepubertal period. Adapted from Turner (9).
The effects of weight bearing on the skeleton have also been identified under numerous special conditions of exercise. For example, in power and weight lifters, increases in bone mass, measured by dual-energy X-ray absorptiometry as bone mineral content and bone mineral density, occur in practically all bones of the skeleton (10). In tennis players, only the bones of the dominant arm show significant gains in bone mineral content and bone mineral density (11, 12), and in dancers, skaters, gymnasts (5, 13), and hockey players (14), greater increments in bone mass occur primarily in the legs, especially the distal parts. Girls who begin playing sports before menarche get about twice the benefit in bone mass gain as do girls who start sports after menarche, at least in racquet sports (15). Pubertal girls with greater bone mass than others may track at this higher plane, at least to menopause (5). In the extreme opposite example of near weightlessness during extended space flight, the loss of bone mass is independent of calcium intake (16).
Prospective studies of the physical activities of young children support the important contribution of weight-bearing activities to the accumulation of bone mass during childhood (17, 18). Weight-bearing activities by youths, beginning at the age of 12 y, were shown to have a significant influence on the gain of lumbar bone mineral density, which was not significantly affected by calcium intake (19). The positive effect of calcium intake on peak bone measurements at 27 y of age could not be substantiated in this study of Dutch boys and girls, but the mean intake of the 84 males and 98 females aged between 13 and 17 y was 1100 ± 366 mg/d, a relatively high amount compared with intakes by Americans of the same ages. In addition to weight-bearing activities, body weight was also found to be a significant determinant of lumbar bone mineral density in this study (19).
A study of 18-y-old intercollegiate female athletes receiving scholarships suggests that peak bone mass is achieved independently of usual calcium intake. In addition, the female athletes had already achieved maximal bone mineral density values before the age of 18 y that were significantly greater than bone mineral density values of sedentary control subjects of comparable body weight (Anderson et al, unpublished observations, 1999). Calcium intakes of the athletes and control subjects were similar at the age of 18 y and were well below the recommended 1200 mg/d (20) or 1300 mg/d (21).
BONE DEVELOPMENT: NOT BY DIET ALONE
Bone development requires sufficient amounts of many nutrients, but calcium has received the greatest attention because of its great mass in the skeleton: >1400 g in mature males and 1200 g in mature females. This mass is presumably accumulated in many individuals who have calcium intakes much lower than current recommendations in the United States. Therefore, a significant role of adaptation must be invoked to account for the skeletal accrual of an adequate skeletal mass with inadequate calcium intakes. The adaptive mechanisms probably involve the muscle-bone linkage stimulated by exercise, and the vitamin D adaptive function must also be important in young growing individuals who get regular exposure to sunlight. Other adaptive mechanisms for enhancing the skeletal accrual of calcium may also exist.
Without invoking some adaptational mechanism, it is nearly impossible to explain the robust skeletal mass obtained by so many youngsters who have known nutritional inadequacies of calcium and vitamin D but who are otherwise healthy and active. Nature must somehow be providing well for skeletal growth despite limited intakes of the critical nutrient, calcium, during periods of bone development.
CONCLUSIONS
The role of physical activity merits more careful attention as a counter or offset to low calcium intakes. The prepubertal years in particular are a good time for physical activities to increase bone mass and density. The importance of bone gain early in life for the prevention of osteoporosis, ie, during a period of relatively high plasticity of the skeleton to physical forces, has become an accepted axiom. Because optimal amounts of calcium are consumed by only small percentages of youths, the beneficial effect of physical activity may dominate as a determinant of bone mass and bone density early in life.
ACKNOWLEDGMENTS
I acknowledge the critical readings of this paper by Sanford Garner, Michael Symons, and Agna Boass.
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