The use of exercise in maintaining bone health throughout the lifespan and ultimately preventing osteoporosis-related fractures has been the focus of considerable research. It is well known that skeletal unloading, such as occurs after spinal cord injury, prolonged bed rest, limb immobilization, and microgravity, precipitates generalize skeletal loss, particularly in bones that bear weight under normal conditions. On the other hand, the relationship between bone loading and bone gain is both highly variable and poorly understood. Skeletal responses to exercise vary as a function of age, reproductive hormone status, nutritional status, and nature of the exercise. In humans, the ultimate goal of an exercise intervention is not only to increase bone mass, but also to reduce the risk of fractures that occur more readily in bones of low mass. Because 90% of hip and 50% of spine fractures occur from a fall, exercise strategies to reduce osteoporosis-related fractures should aim to: 1) improve peak bone mass, 2) minimize bone loss in adulthood, and 3) reduce the risk of falling (Fig. 1).
Drinkwater (2) has emphasized the need to incorporate five training principles into the design of exercises aimed to increase bone mass. They are: specificity, overload, reversibility, initial values, and diminishing returns. That is, an exercise protocol should be designed to load the target bone, or be specific to the measurement site. Additionally, an exercise must overload bone to stimulate it. The issue of overload is problematic as little is known about the loads (e.g., intensities) imposed at given skeletal sites during specific activities. In addition, unlike the muscular and cardiovascular systems, bone has a “lazy zone” within which exercise that may overload and stimulate adaptation in the aforementioned systems, such as a progressive program of jogging, may not stimulate adaptation of bone. Thus, to promote bone gains, an exercise program must include activities that impose bone loads substantially greater than those experienced during activities of normal daily living. Reversibility refers to the fact that gains in bone mass after the imposition of long-term increased loading will likely be lost if the increase in habitual loading ceases. There is some evidence to suggest, however, that although this response is documented in the mature adult skeleton, the growing skeleton may retain gains achieved from increased mechanical loading (4). Initial values refers to the concept that responses from bone to increased loading are greatest when bone mass is initially lower than average. Diminishing returns described the observation that early bone responses to increased mechanical loading are more marked and rapid than ongoing responses.
The most common quantitative measure of bone is bone mineral density (BMD, g·cm−2), assessed by dual-energy x-ray absorptiometry (DXA). Cadaveric studies have shown that BMD predicts more than 80% of the variance in bone strength and thus, to date, has been considered the best noninvasive method to assess skeletal status.
EXERCISE STUDIES ACROSS THE LIFESPAN
In general, cross-sectional studies demonstrate that physically active individuals of all ages have superior skeletal mass than those who are less active. The magnitude of this difference in bone depends upon the mode and intensity of the activity, the age at which it began, and the number of years spent in training.
Exercise and Bone Mass in Children
Studies in children and adolescents of various races generally support significant associations between physical activity and increased bone mass. The effect is clearly demonstrated by the observation that dominant limbs have greater BMD than nondominant limbs, and that athletes loading their dominant limbs preferentially while exercising (e.g., tennis players) develop even greater bilateral disparity. Evidence is accumulating to suggest that exercise confers the greatest long-term benefit when initiated in the prepubertal years, but less is understood about its effect during the peripubertal years. Variations in BMD response to different childhood activities reflect the different loading patterns of each sport and the phenomenon of site specificity.
As exercise interventions for bone have only recently targeted pediatric populations, there are few data available for this cohort. Of those that exist, however, results support cross-sectional observations. Jumping and other weight-bearing activities that overload the skeleton have been found to increase hip and spine bone mineral content (BMC) (Fig. 2) and BMD in prepubescent children (1,3), an effect that can be maintained at the hip after detraining (4) (Fig. 3).
Exercise and Bone Mass in Adults
Although the response of the adult skeleton to exercise has been studied extensively, the difficulties of subject recruitment, randomization, and compliance associated with exercise intervention trials have produced data that are somewhat inconsistent. Additionally, there are few studies in men due to the disproportionate focus on osteoporosis as a disease in women.
Adults engaged in weight-bearing exercise, at intensities of >60% of aerobic capacity, have consistently greater BMD than non-exercisers or those exercising at low aerobic intensities. These differences have been observed in the whole body, spine, and/or proximal femur, pelvis, distal femur, tibia, humerus, calcaneus, and forearm. Broadband ultrasound attenuation and speed of sound transmission in the calcaneus are similarly higher in runners than nonrunners. Given the principle of site specificity, the high BMD of athletes is predictably observed at the skeletal sites loaded during their respective activities.
There is question as to the role of exercise in the prevention of age-related bone loss, although active people who have exercised for many years generally have higher BMD that those who have been less active. Unfortunately, bone mass maintenance due to a lifetime of exercise may not ultimately reduce the risk of fractures (5). That is, in spite of having potentially stronger skeletons than their inactive peers, it is possible that active individuals incur a greater risk of falling (and thus, fracturing) simply as a consequence of moving more.
Certain activities may not apply a sufficient stimulus to bone to force it out of the “lazy zone” previously described to produce an adaptive response. Athletes participating in moderate- to high-intensity impact activities, such as gymnastics, jumping, and power lifting, have greater bone mass than those performing low-intensity or non–weight-bearing activities, such as cycling and swimming (Fig. 4). In fact, often spending more than 20 h·week−1 in a buoyant environment, elite swimmers actually unload their skeletons. Muscle forces on the skeleton during swimming do not appear to offset the concomitant reduced weight bearing that is so crucial to bone mass maintenance.
In non-exercising adults, as in children, the dominant arm exhibits greater total and cortical bone mass than the nondominant arm, and greater differences between right- and left-side limb bone masses are evident when the dominant limb is chronically overloaded (6). The difference is accounted for by increased periosteal area and cortical thickness rather than BMD.
Exercise interventions in young and mature premenopausal women
Exercise-training programs enhance the bone density of young women in a site-specific manner. Both resistance and weight-bearing endurance exercise programs increase spine, hip, and calcaneal BMD of young adult women (13). However, in contrast with the developing skeleton, increased loading must be continued to maintain bone gains (Fig. 5). Only a few studies have addressed the skeletal response to loading in the years just before menopause. Results have indicated that perimenopausal women who exercise will maintain BMD at loaded sites to a greater extent than those who do not (8).
The reduction in circulating estrogen that accompanies menopause represents a powerful confounding factor in studies of exercise effects on bone in this age group. Estrogen withdrawal causes rapid bone loss in the years immediately after menopause; thus, exercise interventions combining both early and late postmenopausal women cannot distinguish the factor imparting the greatest effect on bone.
Resistance training and weight-bearing aerobic exercise in postmenopausal women is generally associated with an increase or maintenance of BMD compared with losses in controls, but not without exception (Fig. 6). Investigations targeting early postmenopausal women report that exercise may be protective from bone loss at the spine and hip, but results are inconsistent.
Activities of low intensity, such as walking, impart very low bone loads. Consequently, walking alone is not an effective strategy for the prevention of osteoporosis in postmenopausal women.
Given the importance of site specificity, it is not surprising that weight-bearing exercise does not increase forearm BMD in postmenopausal women. Forearm loading, however, will increase forearm bone density in osteoporotic postmenopausal women.
Hormone replacement and exercise
The search for alternative approaches to hormone replacement therapy (HRT) for the prevention of bone loss in postmenopausal women has prompted research that examines the efficacy of exercise in comparison with and in combination with HRT. In some cases, exercise enhances the bone maintenance effect of HRT, whereas in others, no interaction between exercise and HRT is observed.
Exercise interventions in young and older adult men
The few existing intervention studies in men indicate the response of the male skeleton to exercise is similar to that of women, but one that is not complicated by an abrupt disruption to reproductive hormones in late adulthood. Young male army recruits frequently show marked increases in bone mass after intensive Basic Training courses, a response reflecting the substantial skeletal overload that occurs during the rigorous physical training. By contrast, walking and moderate-intensity running has been shown to convey little positive benefit to the skeleton in men.
There are few exercise interventions in older men, but of those that exist, site-specific increases in bone density have been reported.
CALCIUM AND EXERCISE
The permissive action of calcium in enhancing the effect of exercise on BMD is somewhat controversial and differences in effect across the lifespan are poorly understood. Some report that the combination of calcium supplementation and exercise is more effective for a bone response in postmenopausal women than calcium supplementation alone (11). An intake of 1000 mg·d−1 of calcium is thought to be necessary to observe such a response.
By contrast to positive reports, a recent cross-sectional study of 422 women found that even though high levels of physical activity and high calcium intake were associated with a higher total body BMC than low activity levels and low calcium intake, there was no significant interaction between exercise and calcium (14). It is reasonable to suggest that exercise provides a greater stimulus to bone than does calcium, but adequate calcium intake is necessary to provide the building blocks for exercise-induced gains in bone mass.
EXERCISE-RELATED GEOMETRIC ADAPTATION
Exercise has the potential to improve bone strength by altering not only bone mineral density, but also bone shape and size, referred to as geometric properties. Increasing cross-sectional area and cross-sectional moment of inertia increase the strength of bone. Athletes who preferentially load their dominant limb exhibit improved geometric parameters (such as increased diaphyseal diameters, cortical wall thickness, and cross-sectional moment of inertia), in addition to superior BMD in that limb compared with the nondominant limb.
HORMONE RESPONSE TO INTENSE EXERCISE
Amenorrhea occurs in some premenopausal women after repeated intense exercise training. The “female athlete triad” describes the combined conditions of excessive dietary restraint, hormonal disturbance, and bone loss in female athletes. Disruption in the hypothalamic-pituitary-thyroid axis from reduced energy availability is the determining factor of exercise-associated amenorrhea (10). Because estrogen levels are reduced, the consequence of exercise-associated amenorrhea may be bone loss. In most cases, the positive effect of exercise on bone cannot offset the negative effects of inadequate energy intake and high-intensity, high-volume exercise training. The exceptions to this rule are gymnasts who, despite a high prevalence of menstrual disturbance, exhibit bone-density values well above normal. In these cases the magnitude and rate of bone loading is so great that it overrides the effect of hormonal disturbance (12). Long distance runners, on the other hand, who load their skeletons at much lower loading rates, are not protected from amenorrhea-related bone loss. Although there are individual differences, the loss of bone mass in amenorrheic distance runners may increase their risk of stress fracture and premature osteoporosis in comparison with amenorrheic runners.
Oral contraceptives may offset bone loss in athletes with menstrual dysfunction; however, there are insufficient data to fully corroborate this effect (7).
Intense training has not been shown to be associated with marked alterations in reproductive hormones in men. Whether hormones potentiate the effect of exercise on bone in men is relatively unexamined.
FALLING AND FRACTURE
Because falls cause more than 90% of hip and 50% of spine fractures, fall prevention should be central to an exercise program for older adults. Muscle weakness, postural stability, and functional mobility are important risk factors for falls (15). As exercise promotes and maintains muscle strength, balance, and mobility it is a highly appropriate strategy for reducing osteoporosis-related fractures.
In general, most literature supports a protective effect of physical activity on the risk of fracture, especially those at the hip (9).
As described above, physical activity has the potential to offset the occurrence of osteoporosis and fragility fractures by: 1) increasing peak bone mass, 2) maintaining or increasing adult bone mass, and 3) reducing the risk and incidence of falls. Because these three factors are age specific, exercise prescription for bone health differs across the lifespan. Not only does younger bone appear to respond better to, and to maintain gains from, a similar activity than does older bone, but a younger skeleton can withstand higher loading magnitudes and rates than an older one.
During youth, to increase peak bone mass, high-impact activities (such as jumping and hopping) should be incorporated into activity patterns from the prepubertal years onwards. In healthy young and middle adulthood, weight-bearing exercise of sufficient magnitude to overload the skeleton (imparting forces of >2.5 body weights at the hip and the spine) should be pursued. For the elderly, exercise programs should emphasize activities that challenge the postural system and use resistance for loading muscle and bone.
A bone-density evaluation is recommended for older and at-risk individuals before initiating a program of impact of high-force exercise, as such activity may be injurious to the osteoporotic skeleton. Osteoporotic individuals, with or without a history of vertebral compression fractures, should not engage in jumping activities or deep forward trunk flexion exercises such as rowing, toe touching, and full sit-ups. Although walking at moderate intensity is not a strong bone stimulus, a lifetime of walking may be beneficial to the skeleton by reducing bone loss in the long term. The maintenance of muscle strength and the coordination associated with regular walking may be highly advantageous in reducing falls related to frailty.
Resistance training programs that promote balance and upper- and lower-body muscle strength may similarly be beneficial by way of reducing fall risk. Any individual undertaking a new program should begin slowly and under supervision, with careful attention to exercise form and appropriate progression.
Physical activity increases peak bone mass and may slow or prevent age-related bone loss. Principles of specificity, overload, reversibility, initial values, and diminishing returns all contribute to the response of bone to exercise. The most osteogenic activities are those that transfer high forces at high loading rates to bone. Such loads are likely to be most effective when introduced early in life, accompanied by adequate calcium consumption and, for hypoestrogenic women, hormone supplementation. High-intensity loading is not recommended for individuals with considerably reduced bone mass. Thus, exercise recommendations for the elderly or osteoporotic focus more on lower-intensity activities designed to reduce falls and fracture.
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