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1School of Sport, Health and Exercise Sciences, University of Wales, Bangor LL57 2PX; and 2School of Psychology, University of Wales, Bangor LL57 2EN, Wales, United Kingdom
Submitted 19 February 2004 ; accepted in final form 11 May 2004
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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6 metabolic equivalents) and calcium intake were found at the total body in boys (b = 2.90 x 10–3) and in girls (b = 6.58 x 10–3) and at the proximal femur (b = 9.87 x 10–5) and femoral neck (b = 2.29 x 10–5; where b is the regression coefficient from final equation) in boys only; residualized BMC was high only if both vigorous activity and calcium intake were high. There were no interactive effects of total activity and calcium intake. This study provides evidence for synergistic action of habitual vigorous activity and calcium intake on bone mass in children. Recommendations for optimizing bone mass should reflect this synergism. accelerometry; dietary calcium; bone densitometry; prepubertal
Modern accelerometers can register accelerations and decelerations caused by bodily movements over several weeks. These accelerations and decelerations are integrated across user-defined epochs and stored for later download. Additionally, several published count cutoff values are available, allowing data to be expressed as minutes spent in varying intensities of physical activity (9, 20). Therefore, temporal analysis of movement data is possible, permitting analysis of total physical activity, time accumulated at different intensities of activity, and the pattern of activity. The time resolution of the accelerometer is important when assessing activity relevant to bone density, as this allows short periods of intense activity to be captured. For bone development, high intensities of strain to the musculoskeletal system are more important than the volume of activity (16). Other methods of assessing activity would likely miss these potentially important episodes. Physical activity assessed by one-dimensional (uniaxial) accelerometry has been shown to account for 1.5–9% of the variance in size-adjusted bone measures, in 4- to 6-yr-old children (13).
It is unclear whether physical activity or calcium intake is more important for bone mass accrual. Research has shown a greater influence on bone mass from calcium supplementation than physical activity interventions (10). Conversely, other studies have shown the contrary (24). It is well documented that a substantial percentage of children and adolescents, especially girls, do not consume and absorb enough dietary calcium during the period of peak bone mass accretion (7). Anderson (2) concluded that, as optimal amounts of calcium are consumed by few children, the beneficial effect of physical activity may dominate as a determinant of bone mass in early life.
To date, the statistical design of the majority of studies has considered calcium intake and physical activity to have independent effects on bone mass. However, potentially, there is a synergistic action of calcium intake and physical activity, whereby both have to be high for an optimal effect on bone mass. Two studies have recently performed longitudinal analyses to address this question. Specker and Binkley (25) used a 12-mo randomized, placebo-controlled intervention trial of activity (30 min/day of fine or gross motor activities) and calcium (500 mg/day or placebo) in 178 children, aged 3–5 yr. After 12 mo, there was little difference in leg BMC gain between gross and fine motor groups receiving the placebo (38.2 ± 1.2 vs. 38.5 ± 1.3 g), whereas, when supplemented with calcium, the gross motor group showed a 3.6-g higher BMC increase relative to the fine motor group (40.9 ± 1.3 vs. 37.3 ± 1.4 g, P < 0.05). However, the gain in cortical area and thickness in the leg by the calcium-supplemented gross motor group was similar to the gain shown by the fine motor group receiving the placebo. Therefore, these results should be interpreted with caution.
Iuliano-Burns et al. (11) found more consistent results following an 8.5-mo, randomized, placebo-controlled intervention trial of activity (low-impact or moderate-impact groups) and diet (calcium-fortified or nonfortified foods) in 66 pre- and early pubertal girls. There was little difference in femoral BMC gain between the moderate- and low-impact exercise groups receiving the nonfortified foods (25.4 ± 2.2 g compared with 26.6 ± 2.1 g, respectively), whereas there was a 10.5-g higher BMC gain in the moderate-impact exercise group relative to the low-impact exercise group receiving the calcium-fortified foods (31.7 ± 2.3 g compared with 21.2 ± 2.6 g, respectively, P < 0.05).
However, such an activity intervention is not an option for most children. Therefore, it is important to explore whether there are interactive effects of naturally occurring physical activity and dietary calcium levels on bone mass. The aim of the present study was to assess the effects of habitual physical activity (total and vigorous intensity) and calcium intake on BMC in prepubertal boys and girls. We predicted that bone mass would be at its highest when both calcium intake and physical activity were high. Furthermore, we anticipated that this effect would be more evident for vigorous physical activity than for total physical activity.
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METHODS |
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0.35 (R2 = 0.12). To detect an effect of this size, with a power of 0.80 and 
of 0.05, would require a sample size of 34 children (8). Boys and girls were to be analyzed separately. All participants were healthy, with no known diseases affecting bone metabolism. Ethics approval was granted by the North Wales Health Authority Research Ethics Committee. Written, informed consent was obtained from all parents, and verbal assent from all children. Each participant and their parents were visited at home, where all procedures were explained. A package was given containing an accelerometer, four food diary forms, and a maturational status form, with written instructions.
Anthropometric and maturational assessment. Height was measured to the nearest 0.1 cm, and body mass to the nearest 0.1 kg, by using a free-standing Seca stadiometer and Seca scales (Seca, Reinach, Switzerland). The children self-reported their pubertal status, aided by parents, using Tanner stages of breast development for girls and pubic hair development for boys (26). Girls were also questioned on their menstruation status.
Calcium intake. Food intake was recorded continuously by using a weighted food diary. Each child and their parent(s) were instructed how to keep the food diary and record the time and weight of all food and drink ingested. The diary was kept for 3 weekdays and 1 weekend day. Diaries were analyzed for average daily calcium content in milligrams by using commercially available software (Dietmaster, version 4, Swift Computer Systems, Surrey, UK).
Physical activity. Physical activity was measured by using triaxial accelerometers (RT3, Stayhealthy, Monrovia, CA). Data were collected during term time between March and September in a single year. Each child wore an accelerometer for up to 7 days. Data were scrutinized, and any day during which a monitor was evidently removed for more than 30 consecutive min was excluded from the data set. By this criterion, each child provided data for a minimum of 4 days (mean ± SD = 5.2 ± 0.9 days), as recommended by Trost et al. (27). The accelerometer was worn on the right hip, from the time the child got up in the morning until bedtime. The accelerometer was initialized and downloaded via a computer interface and had no external controls that could be manipulated. The accelerometer was programmed to record activity counts in 1-min epochs.
The use of triaxial accelerometry to assess movement in more than one plane is potentially advantageous, because unusual strain distributions are particularly advantageous to bone mineral density (BMD) (16). However, there are interunit variability problems with the RT3 accelerometer along the anterioposterior (Y) and mediolateral (Z) planes of motion (17). Therefore, in the present study, activity was analyzed by using the vertical (X) plane of motion only. The vertical plane is considered to be the most important axis of measurement, given the well-established relationship between impact-loading and weight-bearing activity and bone mass accrual (28, 29).
The mean daily activity count on the vertical axis (total activity) and mean times spent in very hard, hard, vigorous, moderate, and low-intensity activities were used as the output measures for physical activity (Table 1). Additionally, the mean time spent at an intensity of vigorous and greater was calculated ( vigorous activity).
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All scans were attended by the same two investigators (S. M. Powell or S. Stevens), and all scans were analyzed by the same investigator (S. M. Powell) in our laboratory. Quality assurance was performed daily by scanning a spine phantom supplied by the manufacturer. The in vivo precision error of dual-energy X-ray absorptiometry in our laboratory, expressed as the coefficient of variation, is 1.0% for the total proximal femur, 1.4% for the femoral neck, and 0.5% for the whole body.
Statistical analysis.
Descriptive statistics were calculated for all variables. Independent t-tests were used to analyze gender differences in anthropometric and bone measures. A series of six independent t-tests were carried out to examine gender differences in time spent at the various activity intensities. Where necessary, degrees of freedom were adjusted, owing to violation of the assumption of homogeneity of variance. The Bonferroni correction was used, reducing to 0.008 (0.05/6), to allow for multiple tests of significance.
BMD is an areal density measurement (g/cm2), i.e., BMC is divided by bone area. However, this does not adequately account for differing body sizes (18). Therefore, BMC was regressed on bone area and body mass, and the residuals were saved to form a new variable, residualized BMC (BMCR). Therefore, a child's BMCR score represented the extent to which the child's actual BMC score exceeded or fell below what would be expected, given the child's mass and bone area. Height was not included in this correction for body size, as it did not account for any variance in BMC beyond that explained by bone area and body mass (see Ref. 18).
Multiple moderated regression analyses (12) were used to assess whether calcium intake moderated the relationship between total activity and total body BMCR, proximal femur BMCR, and femoral neck BMCR. The independent variables were entered into the regression analysis in the following order: calcium intake, total activity, and product of calcium intake and total activity (calcium intake x total activity). A significant product term would indicate an interactive effect of calcium intake and total activity on BMCR. To avoid the problem of multicollinearity, the independent variables (calcium intake and total activity) were centered before entry into the analysis. Centering entailed subtracting the mean from each individual score; therefore, the mean of the centered variable was zero. The product term was calculated from these centered variables. When interpreting the regression output, the unstandardized solution was examined. To elucidate the form of a significant interactive effect, we would graph the relationship between total activity and BMCR when calcium intake was medium (at its mean), high (1 SD above the mean), and low (1 SD below the mean), as described by Jaccard and Turrisi (12).
It should be noted that, as this is a product-term model, the regression coefficients for total activity and calcium intake represent simple effects rather than main effects (12): the coefficient for total activity estimates the effect of activity on BMCR when calcium intake is at its mean (centered calcium intake is zero); and the coefficient for calcium intake estimates the effect of calcium on BMCR when total activity is at its mean (centered total activity is zero).
The importance of high-intensity activity was investigated by repeating the above analyses with vigorous activity in place of total activity. All analyses were conducted separately for each gender. The possibility of multicollinearity was examined by using variance inflation factor. In all cases, variance inflation factor was <2.5, indicating that multicollinearity was not a cause for concern (1).
An -level of 0.05 was used for all statistical tests. SPSS (version 11.0 for Windows; SPSS, Chicago, IL) was used for all statistical analyses.
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RESULTS |
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vigorous intensity activity (t54.1 = –3.3, P < 0.005).
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vigorous activity are presented in Table 3, bottom. There was a calcium x vigorous activity interaction at the total body in boys (b = 2.9 x 10–3, SE = 0.00) and girls (b = 6.58 x 10–3, SE = 0.00). In boys only, interactive effects were also present at the proximal femur (b = 9.87 x 10–5, SE = 0.00) and the femoral neck (b = 2.29 x 10–5, SE = 0.00). The interactive effects are depicted in Figs. 1–4. Each graph shows the relationship between vigorous activity and BMCR for three different levels of calcium intake: low (1 SD below the mean), medium (at the mean), and high (1 SD above the mean). These graphs indicate that, where an interactive effect was present, BMCR was only high if both calcium and vigorous activity were high, with no benefits from one variable alone being high. This was the case at the total body in boys and girls (Figs. 1 and 2) and at the proximal femur and femoral neck in boys only (Figs. 3 and 4). Furthermore, in boys, vigorous activity had a positive effect at the total body, proximal femur, and femoral neck if calcium intake were at its mean or higher (Figs. 1, 3, and 4), whereas, in girls, vigorous activity only had a positive effect at the total body if calcium intake were 1 SD above the mean (Fig. 2).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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These results extend the findings of Specker and Binkley (25) and Iuliano-Burns et al. (11), who both reported that an exercise intervention resulted in gains in bone mass at the leg or hip only when calcium intake was also supplemented. It appears that the same effect is present with habitual levels of vigorous activity and calcium intake in boys. However, in contrast to the present study, neither intervention study found an interactive effect of exercise and calcium at the total body.
It is surprising that few studies have addressed the interactive effect of calcium intake and physical activity on bone, as calcium appears necessary for exercise to have an optimal bone-stimulating action (6). Conclusions from studies that have addressed only the main effects of calcium intake or physical activity on bone may be misleading. For example, in a nonmoderated regression model, the main effect of physical activity on bone would be assessed across all levels of calcium intake (12). This would dilute any effect of physical activity on bone that only occurred at relatively high calcium intakes.
The importance of vigorous activity is not surprising, as high intensities of strain to the musculoskeletal system appear to be more important than the volume of activity to bone development (16). Our results support those of Janz et al. (13), who reported higher positive correlations of hip BMC with vigorous activity (r = 0.25 in boys and r = 0.28 in girls, P < 0.05) than with total physical activity (r = 0.20 in boys and r = 0.25 in girls, P < 0.05) in 4- to 6-yr-old American children. As well as high-intensity activity, high frequency of activity is important for the effective application of mechanical forces, which promote osteogenesis (28). The required mechanical load necessary to initiate new bone formation decreases as the loading frequency increases (28). This could contribute to the presence of a relationship between vigorous activity and residualized bone mass at the hip in the present study for boys, although not girls. The significantly lower number of minutes spent in vigorous activity in girls may indicate a lower frequency of activity.
Although not statistically significant, there was a trend for a higher intake in boys (762.9 ± 310.1 mg/day) than girls (672.6 ± 177.6 mg/day). In fact, high calcium intake in girls (1 SD above the mean = 850.2 mg/day) was similar to the mean score for boys. This is important as the interactions at the total body showed that vigorous activity had a beneficial effect on bone mass when calcium intake was at its mean or above in boys, but only if calcium intake was high (1 SD above the mean) in girls. Therefore, it is possible that there is a threshold calcium intake of 700–800 mg/day before vigorous activity impacts significantly on bone. This value is similar to the recommended dietary intake for 7- to 10-yr-olds (recommended dietary allowance) of 800 mg/day in the USA, but lower than the recommended nutrient intake of 550 mg/day in the UK. It is notable that the b coefficients for vigorous activity, when calcium intake is high, are very similar for boys and girls (boys: b = 1.806; girls: b = 1.751). This indicates that, when calcium intake is high, the nature of the relationship between vigorous activity and total body BMCR is similar for boys and girls.
Assuming calcium intake was 700–800 mg/day, 40 min per day of vigorous activity in boys and 25 min of vigorous activity in girls were associated with increased BMCR. This quantity of vigorous activity supports the conclusions of Janz et al. (13), who recommended that, to increase BMC at the hip and spine in 4- to 6-yr-olds by 2–3% of the mean, vigorous activity needed to be increased by 10 min to 40 min in boys and 35 min in girls. The effect in the present study is stronger, probably mainly due to no consideration of calcium intake, either in isolation or as an interactive effect with activity by Janz and colleagues.
The use of accelerometers set at a 1-min epoch may have resulted in an underestimation of time spent in vigorous activity (15). This may have impacted on the size of the detected relationships between vigorous activity and BMCR. Bailey et al. (3) observed that children engaged in very short bursts of intense physical activity interspersed with varying intervals of low and moderate intensity. The median duration of high-intensity activities was found to be only 3 s, with 95% lasting <15 s. Therefore, in the future, it would be more appropriate to use a 1-s epoch to capture a more precise picture of vigorous physical activity in children. However, the memory capacity of the accelerometers precludes the use of this epoch setting for longer than 7 h at present.
In conclusion, the evidence suggests that calcium intake and vigorous activity have a synergistic effect on bone. Results indicate that 8- to 11-yr-old children should participate in 25–40 min/day of vigorous activity (6 metabolic equivalents) and dietary calcium intake should be 700–800 mg/day for a positive impact on bone. It is notable that this calcium intake is higher than the current UK recommended nutrient intake of 550 mg/day. However, it must be acknowledged that weighted food diaries are potentially prone to reporter bias and increased food awareness while recording dietary intake.
Additionally, current recommendations for children's physical activity recommend 60 min of moderate activity (3 metabolic equivalents) per day (5). Further research is needed to investigate whether there are grounds to adapt these recommendations to optimize bone health in children, particularly as it appears that activity needs to be of a vigorous nature to stimulate an osteogenic response. This study was cross-sectional in nature, limiting the conclusions that can be drawn; the effect of habitual physical activity and dietary calcium should also be investigated in a longitudinal study to allow the effect of changes in calcium intake and physical activity on bone mass in children, across different pubertal stages, to be examined.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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