In this study we examined longitudinal associations among children’s everyday physical activity and FN structural measures of axial (CSA) and bending (Z) strength using multilevel (individual growth) modeling. The use of accelerometry technology to quantify physical activity and the use of HSA to estimate bone structural measures are novel components of this study. In addition, the statistical method of multilevel modeling provided a unique view of the relationship between children’s physical activity and bone strength. The use of multilevel models allowed us to circumvent several limitations of more commonly-used repeated measures techniques. For example, repeated-measures analysis of variance assumes that the overall pattern of change within the cohort generalizes to all children [6
]. On the other hand, multilevel models allowed us to fit each child with his or her own growth trajectory and that was important given slope and intercept coefficients varied across children in our study. This strategy improved the model’s fit. The effect of this approach was the identification of independent inter-group effects of MVPA on bone geometry measures (CSA and Z) while controlling for the effects of growth (age) and age-dependent covariates of body size (height, weight or lean mass) [2
In our cohort, physically active boys and girls had a greater CSA and Z than their less active peers throughout middle- and late-childhood. This result suggests that the bone geometry in children adapts to mechanical loading conditions imposed by their usual physical activity level. Mechanical loads imposed on bone during intervention studies may not generalize to normal playground activity. The observational nature of this work in children is important since it includes the everyday context in which mechanical loading occurs and more accurately reflects the type and amount of physical activity in which children voluntarily choose to engage. Ultimately, effective public health recommendations will require information from both intervention and observational studies.
The influence of MVPA on CSA and Z was greater in boys than girls in our study. Throughout the six years of observation, boys, on average, were more active than girls and this difference increased as the children aged. Specifically, girls were, on average, 24% less active than boys at age 5 yr based on MVPA, 35% less active at age 8 yr, and 47% less active at age 11 yr. These differences were a result of boys increasing their MVPA levels between ages 5 and 11 while during the same time period, the girls decreased their MVPA levels. Assuming a potential causal association between physical activity and bone structural measures, greater levels of MVPA would be expected to result in greater CSA and Z. As a side note, at age 11 the children self-reported their levels of organized and unorganized leisure activities and sports. There was no statistically significant difference between boys and girls with respect to the number of organized activities in which the children participated, their participation time (organized or unorganized), and there were few differences between boys and girls with respect to types of activities that they reported (organized or unorganized). This suggests that diverging gender-related patterns of MVPA (as measured using accelerometry) may exist within similar patterns of leisure activity participation.
In our study, there was an interaction effect between age and MVPA for boys, but not for girls. We interpret this result to indicate that throughout middle- and late-childhood, the influence of physical activity on CSA and Z is similar for girls as they age; however, as boys age, physical activity has a greater influence on CSA and Z. This finding suggests the possibility of a “window of opportunity” just prior to adolescence for using exercise as an intervention to improve bone strength in boys. Recently, Macdonald and colleagues [19
] reported concordant findings from the Action Schools! BC Study
in British Columbia. After a 16-month jumping intervention, they showed targeted loading effective for increasing tibial bone strength in prepurbertal boys, but not early pubertal boys (mean age at baseline 10.3 yr for all boys). In Healthy Bones
, another large school-based intervention in British Columbia, McKay and colleagues used HSA to show a greater apposition on the FN periosteal surface for peri-pubertal boys and a greater apposition on the FN endosteal surface for peri-pubertal girls [20
]. This latter work suggests that as children enter puberty, differences in hip geometry, particularly Z, associated with physical activity are greater in boys than girls. These maturity- and sex-specific differences may be driven by increasing levels of sex steroids or some other (unknown) mechanism. The interaction effect between age and MVPA that we observed in boys may also be due to subtle differences in the magnitude, type, and variety of the physical activities that the boys in our study selected as they aged, compared to the choices they made when they were younger.
The largest physiologic loads placed on bones are from muscle contractions. Since muscle forces scale with muscle size and lean mass is predominantly muscle, we examined whether physical activity predicted CSA and Z after controlling for total body lean mass [29
]. Recent investigations have shown strong predictive relationships between lean mass and bone structure measures [9
]. Our results suggest that lean mass may mediate the relationship between physical activity and FN bone structure measures in girls, but it does not fully explain the physical activity effect on these same measures in boys. This finding of a residual effect of physical activity after controlling for lean mass in boys is in contrast to a recent paper by the Saskatchewan Paediatric Bone and Mineral Accrual Study
]. The Saskatchewan investigators reported non-significant effects of physical activity on CSA and Z when total body lean mass or leg lean mass was included in regression models [10
]. The difference between our study results and the Saskatchewan study results may be due to differences in subject ages since we studied children and the Saskatchewan cohort was primarily adolescents. Or perhaps our use of accelerometry technology, rather than questionnaires, provided a more precise and direct quantification of physical activity that allowed us to detect its residual effects. In an earlier cross-sectional analysis of our cohort at age 5, after controlling for lean mass, we found physical activity to be independently associated with CSA and Z in both boys and girls [13
]. We did find that the effect of physical activity was reduced when compared to models that did not include lean mass, suggesting that most of the effect was mediated though greater muscle bulk. Since, on average, the boys in our cohort were more physically active than the girls and the gender-specific difference in physical activity levels increased with age, we speculate that a specific threshold or load of physical activity may be needed to detect its independent effect on FN bone structure parameters and that this amount of physical activity was not met by the girls in our study as they aged. Alternatively greater homogeneity in the activity level in girls may make a real effect more difficult to detect using these methods.
Our research has limitations. Though the cohort has been studied longitudinally, it is a convenience sample which suggests that subjects may not be representative of all U.S. children. Accelerometry as a measure of free-living physical activity is not error-free. For example, the accelerometry cut-point method that we used to determine MVPA was calibrated in laboratory settings [33
]. Greater variability would be expected during free-living activity; therefore, our MVPA variable should be interpreted as indicating a relatively high intensity of movement (≥ 3,000 movement counts.min−1
) rather than a precise metabolic or mechanical load. It is also likely that the one-minute time frame used to summarize our accelerometry movement count data missed shorter bouts of high-intensity physical activity [35
]. On the other hand, our cut-point approach, one-minute time frame, accelerometer model, number of days measured, and number of hours measured per day are nearly identical those used in a recently published Avon Longitudinal Study of Parents and Children
]. In this work, Tobias and colleagues showed that accelerometry-measured MVPA was related to bone size and BMD in a very large cohort (n = 4,457) of 11-year-old children [32
Other limitations of our study include potential differences in lean mass estimates between the Hologic 2000 DXA scanner that was used for age 5 and age 8 examinations and the Hologic 4500 DXA scanner that was used at the age 11 examination. In addition, we measured the left hip of all children but did not ascertain whether the left leg was non-dominant. Though the HSA program is commonly used in adults and more recently in children, there are limitations to its use [24
]. In particular, bending strength indices are measured only in the plane of the scan image; bending strength differences in other directions may exist; however, they cannot be determined by our method [4
]. In addition, the HSA algorithm assumes average mineralization of 1.05 g/cm3
which is appropriate for adults [3
]. Lower mineralization densities would be expected in children and, therefore, a systematic underestimation of (absolute) CSA and Z is assumed [12
]. Finally, maturational differences may have influenced our study results. We did not measure maturity throughout the six-year time span of the study. For most of our study period, it is logical to assume the children were not biologically mature. At the time of the age 11 examination, we estimated peak height velocity using the Mirwald method [22
]. Sixteen percent of the girls, but none of the boys, had reached or were post peak height velocity. This was not surprising, since girls, on average, mature 2 yr earlier than boys; however, the level of maturity in girls may have confounded our results. However, our results indicated that the effect of MVPA on CSA and Z did not change as the girls aged.
In conclusion, when compared to less active peers, more physically active boys and girls have greater CSA (an index of axial strength) and Z (an index of bending strength) at the femoral neck. The strength of the positive association between physical activity and hip geometry is enhanced with age in boys. These results provide evidence that mechanical loading of the skeleton during childhood results in a positive effect on bone structural strength.