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Exercise and bone health: optimising bone structure during growth is key, but all is not in vain during ageing
  1. Stuart J Warden,
  2. Robyn K Fuchs
  1. Department of Physical Therapy, School of Health and Rehabilitation Sciences, Indiana University, Indianapolis, Indiana, USA
  1. Correspondence to Dr Stuart J Warden, Department of Physical Therapy, School of Health and Rehabilitation Sciences, Indiana University, 1140 W Michigan St, CF-326, Indianapolis, IN 46202, USA; stwarden{at}iupui.edu

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The reduction in bone strength and resultant increase in low-trauma fractures associated with ageing represents a prominent and growing societal problem. Although numerous pharmacological agents have been developed to prevent and treat reductions in bone strength as a means to reduce fractures, a commonly advocated intervention is the prescription of load-bearing exercise.1 The skeleton is mechanosensitive across the lifespan and responds and adapts to its prevailing mechanical environment. This concept is supported by two independent, yet related, articles in this issue of the BJSM.2 3 These papers highlight the potential role of exercise on bone health at two differing stages of the lifespan. Kato et al2 performed a cross-sectional study to show that exercise when young may have lasting effects on bone health during ageing, whereas Martyn-St James and Carroll3 performed a systematic review and meta-analysis to demonstrate that exercise can have beneficial effects on the postmenopausal skeleton.

Exercise during growth may have lasting effects on bone health

A dichotomy exists between when the skeleton is most responsive to exercise and when it is prone to osteoporotic fracture. Reduced bone strength is predominantly an age-related phenomenon,4 whereas the ability of the skeleton to respond to mechanical loading is greatest during childhood and decreases with age.5 In fact, the skeletal benefit of a lifetime of exercise seems to occur mainly during the years of skeletal development.6 7 This disparate response of the skeleton to mechanical loading with ageing and the reduction in bone strength with age has raised the question of whether exercise-induced bone changes during growth persist into adulthood where they would be most advantageous in reducing fracture risk.

Kato et al2 address this issue in their study of postmenopausal bone health in former adolescent athletes and controls. Weight-bearing exercise when young was found to have persistent effects on bone mass and structure following cessation of exercise, suggesting that exercise during growth may have lasting effects on bone health. Previous studies support the potential short-term sustainability of exercise-induced benefits in bone mass8 9 10; however, these mass benefits do not appear to be maintained into older age where they may be advantageous in reducing the fracture-risk associated with osteoporosis.11 12 Also, the cross-sectional study design utilised by Kato et al2 introduces some bias due to the potential natural selection of certain individuals towards load-bearing athletic endeavours. Nevertheless, the suggestion of Kato et al2 that exercise-induced effects on bone structure may be maintained is interesting as (1) exercise during growth predominantly influences bone structure rather than mass and (2) mechanisms exist for the long-term maintenance of exercise effects on bone structure.

Exercise during growth predominantly influences bone structure, rather than mass, to enhance bone strength

Exercise during growth adds extra material to loaded sites to effectively increase the quantity of bone present. The conventional dogma is to maximise peak bone mass with exercise during the growing years in an effort to offset the loss of bone that occurs during ageing.13 14 However, mechanical loading associated with weight-bearing exercise generates large increases in bone strength without substantial increases in bone quantity. For instance, it has been demonstrated in animals that very small (<10%) changes in bone mass generated via mechanical loading can result in disproportionate (>60%) increases in skeletal mechanical properties.15 16 This occurs because the bone formation response to mechanical loading is site-specific and occurs where mechanical demands are greatest. The net result is structural optimisation of the skeleton whereby bone material is distributed in such a way that it is better positioned to resist external loads. This typically involves new bone being laid down as far as possible from the respective axis of bending or rotation, as observed in clinical trials whereby exercise during growth (especially before puberty) caused new bone to be preferentially laid down on the periosteal (outer) surface of loaded bones.17 18 Such site-specific depositing of new bone is functionally important as it enables a small amount of new bone material to increase bone strength where it is needed most without overtly increasing the overall weight (quantity) of the skeleton.19 As a consequence of the predominantly structural effects of exercise, there should be a paradigm shift away from the effects of exercise on bone quantity and towards its effect in generating an optimal bone structure.

Mechanisms exist for the long-term maintenance of exercise effects on bone structure

Mechanisms exist for exercise-induced benefits in bone structure to remain intact until senescence where they may have anti-fracture benefits. Age-related loss of bone quantity is principally mediated by endocortical and not periosteal surface changes.20 21 During ageing there is progressive periosteal bone apposition, but this is unable to sustain bone quantity due to the more rapid loss of endosteal bone, particularly during the menopausal transition (fig 1A). The net result is progressive structural decay during ageing. As exercise during growth primarily induces periosteal adaptation and ageing is not associated with loss of bone from the periosteal surface, the enhanced structure induced by exercise during growth may remain intact to have anti-fracture properties later in life (fig 1B).12 This hypothesis is supported by a recent animal study, which found exercise-induced changes in bone structure and strength, but not quantity, persist lifelong following the cessation of exercise during growth.22

Figure 1

Bone structural changes associated with (A) ageing and (B) exercise. (A) Bone loss during ageing occurs primarily via bone resorption on the endocortical surface. There is concomitant bone formation on the periosteal surface, which helps to maintain bone structure, but this is insufficient to maintain bone mass (adapted from Seeman21). (B) Exercise during growth facilitates periosteal bone formation, which optimises bone structure. As bone loss during ageing occurs from the inside-out, the enhanced structure induced by exercise during growth has the potential to remain intact irrespective of age related changes in bone mass.

Exercise has a role in the health of the mature skeleton

Exercise should be advocated during growth to optimise bone structure and strength; however, all may not be in vain for already mature individuals. This is confirmed by Martyn-St James and Carroll3 who demonstrate in this issue of BJSM that exercise can also have beneficial effects on the postmenopausal skeleton. In particular, they show by way of systematic review and meta-analysis that exercise programmes combining differing types of impact loading (such as jumping and skipping) with resistance training and protocols combining jogging with other forms of low-impact exercise (such as climbing stairs and walking) have the potential to preserve bone quantity during ageing. These data indicate that the mature skeleton maintains some ability to respond to its mechanical environment. Whether this bone quantity response also protects against the bone structural decay associated ageing is not known as there are currently very few randomised controlled trials of the effect of exercise on bone structure in the mature skeleton. Also, exercise of the postpubertal skeleton appears to stimulate structural adaptation of the endocortical, as opposed to periosteal, bone surface that contributes less to bone mechanical properties.17 18 Nonetheless, the findings of Martyn-St James and Carroll3 confirm that exercise should also be encouraged during adulthood to optimise skeletal health.

The exercise continuum for bone health

The collective works of Kato et al,2 Martyn-St James and Carroll3 and others suggest an exercise continuum for bone health throughout the lifespan. Exercise early in life (and especially before puberty) should be promoted to optimise bone structure. The objective is to develop a skeleton with the most ideal structural design, with the hope that this design persists long-term to have benefits later in life. Appropriate exercises during this phase include high impact activities that introduce loads in multiple directions, such as basketball and gymnastics. Also, simple jumping activities may be performed as they only take a few minutes of the school day to complete and have been shown to be osteogenic.23 24 During early and mid-adulthood, the objective of exercise shifts towards preserving bone quantity so as to enter late adulthood with maximal bone stock. Age-appropriate exercises during this phase are highly individual but may include a combination of moderate impact loading and resistance training. During late adulthood, the focus of exercise swings from the enhancement of bone health to the protection of the skeleton from excessive loads.25 This is not to imply that exercise in late adulthood cannot have skeletal effects, but these effects are likely to be small and individuals may be better served by protecting themselves against loads that may be injurious. As falls account for most osteoporotic fractures in the elderly, this age group should perform exercises that mediate risk factors for falls.26 Also, they should be encouraged to maintain an upright posture so as to reduce the elevated spinal loads associated with an exaggerated thoracic kyphosis.27 Appropriate exercises in this age group may include balance activities, supervised resistance training and general conditioning programmes.

Using this continuum approach, exercise may be performed throughout the lifespan to target the escalating problem of low-trauma fractures associated with ageing. Whether performance of such exercise actually results in a reduction in the occurrence of osteoporotic fractures requires investigation by way of controlled clinical trials. Unfortunately, these may not be completed any time soon as the number of participants required in prospective exercise trials to statistically power for a reduction in fracture rates is overwhelming.

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Footnotes

  • Competing interests None.