Journal of the American College of Nutrition, Vol. 20, No. 2, 186S-191S (2001)
Published by the American College of Nutrition
Calcium Requirements during Adolescence to Maximize Bone Health
John J. B. Anderson, Ph.D., FACN
Schools of Public Health and Medicine, University of North Carolina, Chapel Hill, North Carolina
Address reprint requests to: John J. B. Anderson, PhD, Department of Nutrition, Schools of Public Health, University of North Carolina, Chapel Hill, NC 27599-7400. E-mail: jjb_andersonunc.edu.
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ABSTRACT
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The calcium requirements of boys and girls during adolescence have largely been based on balance studies, including more recently the use of stable nuclides. Bone measurements by dual energy X-ray absorptiometry (DXA) and similar instruments have provided an end-point by which to assess skeletal development, either of the entire skeleton or of specific bones, in relation to the consumption of calcium and other nutrients and to physical activity. Several cross-sectional studies, using measurements of bone mineral density (BMD) and bone mineral content (BMC), suggest that optimal calcium intakes for female adolescents may be somewhat lower than published as the Adequate Intakes (AIs) by the Institute of Medicine in 1997, but they may be somewhat higher for adolescent males. These results suggest that gender should be considered in establishing recommendations for calcium. In addition, other studies have provided evidence that prepubertal and postpubertal skeletal growth of males and females is enhanced by regular physical activities and that the optimal attainment of BMC and BMD by females by late adolescence may not be dependent on such a high calcium intake as previously thought, although males may need at least the recommended amount. Therefore, physical activity should also be considered in establishing recommendations for calcium. In summary, two lines of evidence suggest that more extensive information on diet and lifestyle should be considered in the future for making more specific recommendations on calcium intakes for optimal skeletal development for prepubertal and postpubertal boys and girls.
Key words: dietary calcium, physical activity, calcium recommendations, skeletal development, peak bone mass, peak bone density
Key teaching points:
• An adequate intake of nutrients, including calcium, is beneficial during prepubertal skeletal development.
• Adequate physical activity, including sports, during prepubertal skeletal development is beneficial.
• There is a potential interaction between dietary calcium and regular physical activity influencing the development of peak bone mass and density.
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INTRODUCTION
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This paper provides a review of both old and new information on the calcium needs of boys and girls from approximately nine to twenty years of age. This period represents the time of greatest skeletal growth of each gender, both prepubertal and pubertal growth. It is this period of life during which peak bone mass is largely accrued and also the period during which the prevention of late life bone loss and osteoporosis-related fractures is considered to begin. Both hereditary and environmental factors contribute to the bone gain during the periods of growth in early life. Hereditary contributions to skeletal development are unquestionably of importance, but only environmental factors can be modified at this time. This report focuses on two variables that affect skeletal development: calcium intake and physical activity.
Gender Differences in Skeletal Growth
A major difference between boys and girls is their physical development, according to age at the different Tanner stages of development [1]. The growth acceleration typically begins two to three years earlier in females, but it lasts longer in males, typically six years or so compared to about four years in girls. The result of this prepubertal and pubertal growth is the accrual of approximately 50% of total skeletal calcium.
The early gain and the later loss of skeletal mass is the normal sequence that is characteristic of human populations throughout the world [2]. The accrual of bone mass, often referred to as peak bone mass (PBM) development, is schematically presented in Fig. 1. Both the periods of prepuberty and puberty have significant influences on changes in skeletal mass in boys and girls [3,4], as illustrated in Fig. 2. In addition, gains in skeletal muscle mass tend to correlate with gains of bone mass.
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Fig. 1. Schematic illustration of PBM development in males and females. Theoretically bone accrual continues to 30 years of age or later, but practically all of the gain of PBM occurs by age 18 in girls and age 20 in boys. Adapted from Anderson and Garner [25].
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Fig. 2. Peak bone mineral content or mass of the total skeleton (PBM) as part of the development of boys and girls. Adapted from Boot et al. [3] and Martin et al. [4].
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In a study of total body bone mineral content (TBBMC) of prepubertal Asian, African-American and white children in New York City, African-American females had the highest mean TBBMC in grams, followed by white and then Asian females [5]. For males, African-Americans had the greatest TBBMC values, followed by Asians and then whites. Male values were greater than female values for each ethnic/racial group. No information was collected in this study on calcium intakes or on physical activity levels of these children, but historical data have shown that white children have considerably higher mean calcium intakes than either African-American or Asian-American children.
Need for Detailed Understanding of Calcium Requirements of Girls and Boys Separately during Prepuberty and Postpuberty
Calcium recommendations for children and adolescents have historically been based on classical balance studies which are fraught with the potential for error. Despite the large variability in estimates of calcium requirements, approximate values have been attained through a type of meta-analysis of numerous balance studies. In an important report, Matkovic and Heaney [6] summarized the published calcium balance data and arrived at composite estimates for both boys and girls. The threshold limit of calcium intakes was estimated to be 1200 mg per day [6]. The specificity for each gender was, however, submerged by this approach. Information on the calcium balance data is needed for each gender separately.
Using a stable nuclide of calcium, an advancement on balance studies, Abrams and Stuff [7] showed that girls in the early pubertal stages (Tanner stages I–III) had much greater retention of calcium than those in the later stages (IV–V). These authors found that early pubertal girls (Tanner stages 2 and 3) retained slightly less than 200 mg per day compared to approximately 50 mg per day by late pubertal girls (Tanner stages 4 and 5) (Fig. 3). Similar studies for boys using stable isotopes of calcium have not been performed, but these data are needed to advance our understanding of calcium requirements of young males. Martin et al. [4] estimated from their growth study that boys accumulate 282 mg of calcium a day during puberty and girls 212 mg a day. The congruence of these findings for girls suggest that they accrue 200 mg a day at peak velocity of skeletal growth.
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Fig. 3. Calcium balance (calculated retention) in prepubertal, pubertal and late pubertal girls, as determined by a stable nuclide of calcium. Adapted from Abrams and Stuff [7].
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More information is available about the calcium needs of girls than of boys, but even less is known about the amounts and types of exercise that promote bone gains during prepuberty and puberty in boys and girls.
How Much Physical Activity Is Needed for Skeletal Growth?
Regular physical activities by children and adolescents have historically been considered essential for the healthy growth and development of all organ systems of children, not simply the skeleton. Several recent reports suggest that regular physical activities make significant contributions to gains in BMC and BMD, beginning in the prepubertal years, at least in girls. Data for boys are scarce, but Bradney et al. [8] and Bailey et al. [9] have reported data that show the benefits of exercise on skeletal development in pubertal boys. The findings of gains in bone mineral density at several skeletal sites with moderate exercise in boys and girls from the report of Bradney et al. [8] are similar to those of Bass et al. [10] for girls only.
Mechanical loading of sufficient intensity promotes an increase in skeletal mass, especially during growth in the first two decades of life [10]. Mechanical loading on bone for the purpose of increasing bone mass (or density) has been shown to require maximal strains, i.e., greater than normal strains from everyday activities such as walking. Any gain in bone mass is considered to be in addition to the genetically determined mass of unloaded bone. Although typically of low strain levels, usual everyday physical activities of sufficient intensity may have an additional positive impact on the accrual of skeletal mass (Fig. 4).
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Fig. 4. The early gain of bone mass and possible scenarios of bone development depending on contributions of environmental variables such as regular activities and adequate intake of calcium. From Anderson [15] (with permission of American Journal of Clinical Nutrition.)
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Information gained over the last few decades suggests that muscular and skeletal benefits are greatest if these activities occur early in life, in girls especially before the onset of puberty [11] (Fig. 5). That physical activity, above all other environment determinants of bone mass, plays a dominant role in skeletal development is supported by data from a variety of approaches. The report by Seeman’s group in Australia [11] provides data on prepubertal girls that support their contention that physical activity in young girls, prior to age 11 years, may enhance bone development. It is furthermore assumed that this benefit remains until the postmenopausal years. Other reports on the effects of exercise by girls early in life support this conclusion [12,13]. Exercise during the pubertal years, i.e., adolescence, also continues the accrual of bone mass, as shown by girls of a Caucasian religious sect in South Dakota known as the Hutterites [14]. When the Hutterite adolescents reach age 18, they have greater mean BMC and BMD measurements of the total skeleton (Table 1) and at the regions of interest than almost any other white females.
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Fig. 5. Skeletal gains in prepubertal girls: Effects of exercise (gymnastics) on bone mineral density (BMD) compared to controls. Adapted from Bass et al. [10].
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In general, physical activities that require sufficient strains on the skeleton, such as in gymnastics, dance, and jumping sports, contribute to greater prepubertal and pubertal gains in bone mass and bone density.
Can Regular Physical Activities Compensate for a Low Calcium Intake?
Most, if not all, considerations of calcium requirements by panels of experts do not include physical activity as a contributor to skeletal growth [15]. Yet, it is likely that regular physical activity may compensate for a chronically low-calcium diet, judging from the examination of children from much of the world, specifically the developing nations. Of course, the combination of an adequate amount of calcium each day as a part of a healthy diet and regular physical activity is much more likely to lead to optimal skeletal development and bone mass by the end of the second decade of life. Nevertheless, studies of bone mass of children and women in Gambia by Prentice et al. [16] suggest that calcium intakes on the order of 300–500 mg a day have no apparent adverse effects on bone measurement variables. Aside from the differential contribution of hereditary factors in racial/ethnic groups, the main difference in lifestyle between Gambian and British subjects in this study is the amount of daily activities of walking, carrying of loads and other work chores.
In more active females during the prepubertal and pubertal years, optimal bone measurements are achieved, despite sub-optimal calcium intakes [17]. At least one report from the Netherlands, where mean calcium intakes approximate current US recommendations, concluded that physical activity may be a more critical variable in skeletal development of children and adolescents than calcium [18]. The same may be said for the Hutterite girls [14]. For optimal skeletal growth, getting an adequate intake of calcium as well as regular physical activity, however, seems ideal.
These studies lend support to the concept that physical activities during the critical growing years make important contributions to the accrual of bone mass, perhaps independently of calcium intakes. In other words, a low calcium intake may be compensated for by regular physical activities in the accrual of peak bone mass [15]. Whether high amounts of physical activity can totally compensate for low calcium intakes has not yet been established in any population.
Studies of Bone Measurements in Physically Active Girls and Boys
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 [19,20]. Weight-bearing activities by youths, beginning in prepuberty, were shown to result in greater accrual of bone mass (Fig. 6) [8,9]. A study of recruited intercollegiate female athletes, i.e., on athletic scholarships, suggests that peak bone mass is achieved despite lower than optimal calcium intakes. The female athletes had already achieved near-maximal PBM prior to age 18, i.e., BMC and BMD values, which were significantly greater than BMC and BMD measurements of a control group of sedentary subjects of comparable body weight [Anderson et al., unpublished data, 1999]. Calcium intakes of the athletes and control subjects were similar at age 18, but well below the recommended 1200 mg per day [21] or 1300 mg per day [22].
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Fig. 6. Total body bone mineral content gains (accrual velocity in grams per year) in girls and boys according to physical activity level (inactive, average or active). Adapted from Bailey et al. [9]. The active group was significantly greater than the inactive group for both boys and girls (p < 0.001).
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Studies of Bone Measurements and Calcium Intakes in Boys
The fewer reports of studies on bone development of boys make it difficult to draw firm conclusions, but two points require consideration. First, boys begin puberty later than girls by approximately two years. Secondly, boys have a longer period of prepuberty than girls, i.e., about two years, and also a longer period of puberty. The amount of calcium in the mature skeleton is approximately 1400 g in males and 1200 g in females. This mass is presumably accumulated in many individuals who have calcium intakes much below current recommended levels in the US [16]. Therefore, some adaptations must occur during the periods of growth to account for the skeletal accrual of an adequate skeletal mass despite inadequate calcium intakes. The adaptive mechanisms most likely involve the muscle-bone linkage stimulated by exercise and the vitamin D adaptive mechanism for calcium absorption. Each of these adaptations must be important in young growing individuals who get regular exercise and exposure to sunlight. Whether other adaptive mechanisms for enhancing the skeletal accrual of calcium exist remains uncertain.
Unpublished data [Anderson et al., 1990] on young adult white males (mean age 
21) from the University of North Carolina suggest that healthy, physically active males have usual calcium intakes of approximately 1200 mg per day (Table 2). These young men were active in intramural and recreational activities; none was on a varsity sports team. Their mean radial bone measurements were normal, according to limited information. In our experience, young adult males have calcium intakes closer to recommended levels than do young adult females [23]. Further data on bone measurements and calcium intakes in growing US males are needed.
Potential Interaction between Calcium Intake and Physical Activity in Girls and Boys
An interaction between calcium intake and physical activity has been identified in a few studies [24], but most investigations have not found one. The reasons for not finding such an interaction vary, but a common explanation is that most studies include too few subjects. Meta-analyses would, therefore, be more likely to find an interaction between these two variables. The report of female Hutterites suggests that a potential interaction between calcium intake and physical activity may permit near optimal skeletal development by 18 years of age when calcium intakes meet or nearly meet recommended levels and the physical activities are only modest [14]. Calcium consumption by the Hutterite girls under 18 years was only approximately 900 to 1000 mg a day from both dairy and non-dairy sources, and perhaps 800 mg of calcium or so were ingested daily by the females over age 18 years of age. These numbers are somewhat less than the recommended Adequate Intake of calcium of 1300 mg per day of the Institute of Medicine [22] (Table 3).
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COMMENTS
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Without invoking an adaptational mechanism, it is difficult to understand the sufficient skeletal mass accrued by so many youngsters with known nutritional inadequacies of calcium and, possibly, vitamin D, but who are otherwise healthy and physically active. Physical activity, at least in part, must make a significant contribution to skeletal growth, despite limited intakes of calcium and possibly of other nutrients critical for bone tissue during periods of bone development.
Based on the Hutterite report [14] and a few other studies, it seems that calcium per se or calcium in conjunction with other nutrients at adequate intake levels is not the major determinant of skeletal measurements achieved by the end of female growth in height, i.e., by age 18 or earlier. The physical activity determinant, thus, becomes quantitatively more significant than calcium, as shown in regression models of the Hutterite report [14] and of the Dutch study [18].
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CONCLUSIONS
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Physical activity must be important as a counter or offset to low calcium intakes in growing children, even if we do not understand the mechanisms involved in this accrual. The prepubertal years provide the greater gains in bone mass and density when both calcium intake and physical activities are or approach recommended levels. For the prevention of osteoporosis, the importance of bone gain early in life, i.e., during a period of relatively high plasticity of the skeleton to physical forces, has become an accepted axiom. Because optimal amounts of calcium are not consumed by practically all children, the positive effect of physical activity may dominate as a determinant of bone mass and bone density early in life.
The current calcium intake recommendations [22] may be set too high for girls and too low for boys during the prepubertal and pubertal years, but they are appropriate when we have less than ideal information upon which to base them. The IOM recommendations [22], however, did not consider the potentially important role of physical activity and a possible interaction of exercise with calcium, as has been shown for the female Hutterites and Dutch children. An interaction between calcium intake and physical activity remains a probable scenario through which growth of bone in early life may occur; that is, less than optimal calcium intakes may be compensated for by the strains of regular physical activities either from daily chores or from sports and other recreational activities.
Adequate calcium intakes are clearly needed for the accrual of bone mass during the prepubertal and pubertal growth periods, but the level of adequacy may vary according to the amount of physical activity of boys and girls during these periods of growth. The variable, physical activity, should no longer be ignored as a major determinant of bone mass during the critical growth periods, especially in prepuberty, when the skeletal gains are most robust.
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ACKNOWLEDGMENTS
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The critical readings by Drs. Agna Boass and Sanford C. Garner during the preparation of this manuscript are greatly appreciated.
Received November 22, 2000.
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ABSTRACT
INTRODUCTION
