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Abstract
The aim of this review is to provide a concise overview and update on recent advances in the field of physical activity in childhood and its effects on bone growth with an emphasis on the potential to prevent fractures. In addition, the review poses several unresolved questions in the field for future research.
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Introduction
Bone is a dynamic tissue that responds to the external and internal environments to which it is exposed across the life course. As a result of these many influences, its mass, structure and strength vary considerably between individuals. Specifically, this variability is a function of age, sex, genetics (the latter explaining as much as 80% of the variance at a given age1) and lifestyle. Of the modifiable lifestyle factors, amount and type of physical activity is a prominent influence and accounts for up to 17% of the variance in bone mineral density (BMD).2 Bone geometry, mass and structure contribute to bone strength, which largely determines bone's susceptibility to fracture. Indeed, it is estimated that in children, a reduction in bone mass of 6.4% doubles the risk of fracture.3 Fractures occur most frequently during adolescence and senescence (older age). Fractures in healthy children are an important but largely ignored public health issue, with a lifetime risk of sustaining a fracture in childhood being 42–64% in boys and 27–40% in girls.4 5 Fracture incidence peaks in children during early puberty (10–12 years in girls, 13–15 years in boys),6 the most common fracture site at this time being the distal forearm.7 Primary risk factors for fracture at the population level appear to be low BMD, previous fracture, overweight, low physical activity and low muscle mass.3 8 In senescence, fractures are largely associated with osteoporosis and predominantly affect the proximal femur (hip), lumbar spine and distal forearm and are more common in women (30–50%) than in men (15–30%).9 Alarmingly, the incidence of fractures is increasing in both age groups.3 10 Thus, with the projected increase in the proportions of older adults in western societies, the rising costs of healthcare related to fracture is also projected to increase substantially in the next two decades. Therefore, it comes as no surprise that there is substantial interest in identifying innovative models to prevent fractures at every age. Low cost interventions that target load-bearing physical activity during childhood as a means of enhancing bone strength and structure are likely to be an important part of the solution. Current hypotheses postulate that growth is a time when exercise is associated with an increase in bone strength; adulthood is a period when exercise may help to maintain bone strength, and older age is a time when exercise may attenuate the natural decline in bone strength.11
Physical activity and bone growth during childhood
Bone continually adapts to the habitual mechanical strains associated with physical activity or to the absence of these mechanical stimuli.12 Evidence from animal and human studies suggests that the growing skeleton has an amazing ability to adapt to external stimuli – perhaps more so during growth than at any other time during life. This is based on the hypothesis that mechanical strain has its greatest effect on bone surfaces that are covered with a larger proportion of osteoblasts during this period of net bone formation.13 During childhood and adolescence the skeleton undergoes profound changes, reaching ‘peak bone mass’ (PBM) in the young adult years. Approximately 26% of total adult bone mass is gained in approximately 2 years around the time of peak bone gain (12.5 years in girls and 14.1 years in boys).14 This rate of accrual approximates the entire amount of bone mineral lost between the ages of 50–80 years.10 Once PBM has been achieved, subsequent gains in bone mineral are minimal. Thus, engaging in healthy lifestyle behaviours such as physical activity is especially important during the growing years.
Long term benefits of enhanced PBM
There is a strong relationship between bone mass and bone strength throughout the life-course.15 PBM also appears to track, at least into young adulthood.16 There is some evidence that maximising PBM achieved in young adulthood and reducing bone loss later in life may positively influence the risk of fracture.15 17 Indeed, a theoretical analysis suggests that the effect of increasing childhood bone mass by 10% would be to delay postmenopausal osteoporosis by approximately 13 years.18 However, there is no direct evidence that augmented bone strength as a result of physical activity during youth reduces fracture risk in old age. Indeed, the very long term studies needed to address this question are not likely to be feasible. Evidence from animal studies is equivocal. While some studies19 20 indicate that training induced benefits to bone mass and structure are lost with cessation of training in young rats, at least one study has indicated that such benefits may persist throughout life.21 Longitudinal studies demonstrated that bone health benefits from exercise during growth progressively declined as youth approached young adulthood22 23 if exercise was not maintained. One theory suggests that bone mass may be governed by a homeostatic system that, if not ‘turned on’ by exercise, reverts to a genetically determined set point.24 Nevertheless, it seems prudent to enhance bone mass during the growing years as a preventive strategy against fracture risk during adolescence25 and later in life.
What type of exercise is optimal for bone health in children?
A number of excellent reviews speak to the beneficial effects of physical activity on bone strength during growth.25,–,28 Dynamic activities of short duration with multiple rest pauses and different kinds of activities that elicited ‘unusual’ strains were most effective to enhance bone strength,28 reflecting earlier findings from elegant animal studies.13 29 Further indirect evidence that bones adapt to different kinds of mechanical strains came from studies of athletes. Young athletes engaged in weight-bearing sports displayed significantly more bone mass in their loaded limbs compared with their less active peers, or those involved in non-weight-bearing sports.30,–,32 Landmark unilateral loading studies of racquet sport athletes clearly demonstrated bone mass and strength were enhanced in the playing arm compared with the non-playing arm.33 34 Bone strength was further enhanced if players began training in early puberty as compared to at a later age33 and benefits persisted over time.35 Thus, the notion arose that early puberty might provide a ‘window of opportunity’ when bone is most responsive to the osteogenic influences of sport.
More than a decade ago14 36 and more recently,37 epidemiological studies and long term prospective trials examined associations between bone status and habitual physical activity in children. Importantly, recreationally active children in the highest quartile of physical activity gained more bone during the 2 years around PBM accrual than those in the lowest quartiles. More recent studies used objective measures of physical activity38,–,40 corroborated earlier findings. An apparent paradox, however, exists. Within a large cohort, children who reported daily vigorous physical activity doubled their risk of sustaining a fracture compared with children who exercised less than four times per week.41 Stronger bones associated with increased physical activity may not fully compensate but may attenuate injury due to increased exposure to risk (ibid). Recent evidence indicates that higher levels of aerobic fitness in children are also associated with an increased risk of fracture, particularly in those with low forearm muscle strength.42 This raises the intriguing possibility that targeted muscle strengthening protocols may reduce upper limb fractures in adolescents.
Several recent randomised-controlled intervention trials applied the principles of loading derived from animal and sports models to the school setting.28 43 44 Interventions typically delivered vigorous activities over the school day (often jumping exercises) at least 3 times weekly, over a minimum of 6 months. Despite considerable differences in study design, most studies reported site-specific improvements in bone mass (measured with dual energy x-ray absorptiometry; DXA) of between 1% and 6%.
However, attention has increasingly shifted from measures of bone mass to potentially more important measures of bone geometry, structure and strength. Recent publications11 26 44 assessed exercise effects on bone strength during growth and reported small but significant effects on the lower extremities in children. The bone response to exercise depended upon the sex and maturity level of the child, the anatomical site measured and the length and intensity of the intervention.
Conclusions and future directions
Taken together, a wide range of extra-curricular sports, other activities and targeted school-based programs provide a weight-bearing stimulus that promotes children's bone health.45 Although bone strength benefits may persist into old age in animals,21 there is little direct evidence that the enhanced ‘bone bank’ similarly persists into old age in humans as these long term studies are challenging to conduct. However, longer term follow-up studies in children46 and retrospective studies of athletes47 48 support this notion.
In the short-term, there is a pressing need for well controlled trials and large scale, longer-term prospective cohort studies to unravel the relationships between physical activity, bone strength and fracture rates in children and adults. The limitations of relying on planar DXA-based measures alone are well known49 and the use of more advanced imaging techniques, including peripheral quantitative CT and MRI, that assess bone geometry, structure and strength would allow us to better understand the adaptive capabilities of growing bone to exercise.
Several other unresolved questions demand further investigation:
Is there a gender difference in the responsiveness of bone strength to exercise around puberty?50
What is the optimal exercise regime for enhancing bone strength in young people? Similarly what is the minimal effective dose of exercise that elicits a bone health response? More studies which directly compare different training approaches are needed.51
What is the best approach to target children susceptible to low bone strength and what role does gene/environment profiling play in identifying those ‘at risk’?
What is the utility of more sophisticated imaging techniques for characterising subtle changes in growing bone as a result disuse, disease, exercise or other interventions?
References
Footnotes
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Competing interests None.
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Provenance and peer review Not commissioned; externally peer reviewed.