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Physical Activity and
Bone Health
This pronouncement was written for the American College of Sports Medicine by Wendy M. Kohrt, Ph.D., FACSM (Chair);Susan A. Bloomfield, Ph.D., FACSM; Kathleen D. Little, Ph.D.;Miriam E. Nelson, Ph.D., FACSM; and Vanessa R. Yingling, Ph.D.
may be indicated even for those postmenopausal women who are habituallyphysically active. Given the current state of knowledge from multiple small Weight-bearing physical activity has beneficial effects on bone health randomized, controlled trials and large observational studies, the following across the age spectrum. Physical activities that generate relatively high- exercise prescription is recommended to help preserve bone health during intensity loading forces, such as plyometrics, gymnastics, and high-inten- sity resistance training, augment bone mineral accrual in children andadolescents. Further, there is some evidence that exercise-induced gains in weight-bearing endurance activities (tennis; stair climbing; bone mass in children are maintained into adulthood, suggesting that jogging, at least intermittently during walking), activities physical activity habits during childhood may have long-lasting benefits on that involve jumping (volleyball, basketball), and resistance bone health. It is not yet possible to describe in detail an exercise program for children and adolescents that will optimize peak bone mass, because moderate to high, in terms of bone-loading forces quantitative dose-response studies are lacking. However, evidence from weight-bearing endurance activities 3–5 times per week; multiple small randomized, controlled trials suggests that the following exercise prescription will augment bone mineral accrual in children and 30 – 60 min⅐dϪ1 of a combination of weight-bearing endur- ance activities, activities that involve jumping, and resis-tance exercise that targets all major muscle groups impact activities, such as gymnastics, plyometrics, andjumping, and moderate intensity resistance training; partic- It is not currently possible to easily quantify exercise intensity in terms ipation in sports that involve running and jumping (soccer, of bone-loading forces, particularly for weight-bearing endurance activi- basketball) is likely to be of benefit, but scientific evidence ties. However, in general, the magnitude of bone-loading forces increases in parallel with increasing exercise intensity quantified by conventional high, in terms of bone-loading forces; for safety reasons, methods (e.g., percent of maximal heart rate or percent of 1RM).
resistance training should be Ͻ60% of 1-repetition maxi- The general recommendation that adults maintain a relatively high level of weight-bearing physical activity for bone health does not have an upper age limit, but as age increases so, too, does the need for ensuring that 10 –20 min (2 times per day or more may be more effective) physical activities can be performed safely. In light of the rapid and During adulthood, the primary goal of physical activity should be to profound effects of immobilization and bed rest on bone loss, and the poor maintain bone mass. Whether adults can increase bone mineral density prognosis for recovery of mineral after remobilization, even the frailest (BMD) through exercise training remains equivocal. When increases have elderly should remain as physically active as their health permits to pre- been reported, it has been in response to relatively high intensity weight- serve skeletal integrity. Exercise programs for elderly women and men bearing endurance or resistance exercise; gains in BMD do not appear to be should include not only weight-bearing endurance and resistance activities preserved when the exercise is discontinued. Observational studies suggest aimed at preserving bone mass, but also activities designed to improve that the age-related decline in BMD is attenuated, and the relative risk for balance and prevent falls. Maintaining a vigorous level of physical activity fracture is reduced, in people who are physically active, even when the across the lifespan should be viewed as an essential component of the activity is not particularly vigorous. However, there have been no large prescription for achieving and maintaining good bone health.
randomized, controlled trials to confirm these observations, nor have therebeen adequate dose-response studies to determine the volume of physicalactivity required for such benefits. It is important to note that, although INTRODUCTION
physical activity may counteract to some extent the aging-related declinein bone mass, there is currently no strong evidence that even vigorous In Caucasian, postmenopausal women, osteoporosis is de- physical activity attenuates the menopause-related loss of bone mineral in fined as a bone mineral density (BMD) value more than 2.5 women. Thus, pharmacologic therapy for the prevention of osteoporosis standard deviations below the young adult mean value (52),with or without accompanying fractures. Whether the samecriteria should apply to premenopausal women, women ofother races, or men remains to be confirmed. In the U.S. and 0195-9131/04/3611-1985MEDICINE & SCIENCE IN SPORTS & EXERCISE® other developed countries the incidence of osteoporosis is Copyright 2004 by the American College of Sports Medicine increasing at rates faster than would be predicted by the increase in the proportion of aged individuals. Multiple vertebral fractures and, in particular, hip fractures have a Currently, BMD is the best surrogate measure of bone devastating effect on functional abilities and quality of life.
strength in humans and BMD has been estimated to account The mortality rate for elderly individuals in the first year for 60% or more of the variance in bone strength (20,125).
following hip fracture is as high as 15–20% (105). Even However, studies of animals suggest that changes in BMD with no change in current incidence rates, it has been esti- in response to mechanical stress underestimate the effects mated that the number of hip fractures will double to 2.6 on bone strength. For example, 5– 8% increases in BMD million by the year 2025, with a greater percentage increase were associated with increases in bone strength of 64 – 87% (48,116). The size of bone has a significant contribution to Because low BMD greatly elevates the risk of fractures bone strength because the resistance of bone to bending or with minimal trauma, as with a fall to the floor, strategies torsional loading is exponentially related to its diameter; that maximize bone mass and/or reduce the risk of falling furthermore, bone size may continue to increase during have the potential of reducing morbidity and mortality from adulthood (93). Because bone architecture (i.e., geometry) is osteoporotic fractures. Although bone mass can be increased an important determinant of strength (104), evaluation of the through pharmacologic therapy, physical activity is the only effects of mechanical stress on bone should consider not intervention that can potentially both 1) increase bone mass only changes in bone mass, but changes in structural and strength and 2) reduce the risk of falling in older strength and material and geometric properties when possi- populations. There exist other bone health issues associated with exercise, including the risk of stress fractures with The two generally accepted strategies to make the skel- high-volume training and the bone loss associated with eton more resistant to fracture are to 1) maximize the gain amenorrhea. However, the focus of this position stand will in BMD in the first three decades of life and 2) minimize the be on the effectiveness of physical activity to reduce risk for decline in BMD after the age of 40 due to endocrine osteoporotic fracture, without specific reference to nutri- changes, aging, a decline in physical activity, and other factors. Because bone strength and resistance to fracture Well-known principles of exercise training apply to the depend not only on the quantity of bone (estimated by effects of physical activity on bone. For example, overload- BMD) but also bone geometry, methods are being devel- ing forces must be applied to bone to stimulate an adaptive oped that enable the assessment of cross-sectional geometry response, and continued adaptation requires a progressively with existing DXA technology or with peripheral quantita- increasing overload. It is important to emphasize that the tive computed tomography (pQCT) or high-resolution mag- stimulus to bone is literally physical deformation of bone netic resonance imaging (MRI). The microarchitecture of cells, rather than the metabolic or cardiovascular stresses cancellous, or trabecular, bone (i.e., the lattice-work of bone typically associated with exercise (e.g., % V inside vertebral bodies or ends of long bones) is important cal deformation can be measured by strain gauges on the to the mechanical strength of the femoral neck, vertebral bone surface, but is more commonly estimated by such bodies, and other cancellous bone-rich regions. However, surrogate measures as ground-reaction forces engendered microarchitecture of cancellous bone can be assessed at during weight-bearing activities. Muscle contraction forces present in humans only by bone biopsy, sophisticated MRI in the absence of ground-reaction forces (e.g., swimming) analyses, or the most advanced micro-CT devices not yet may also stimulate bone formation, but this is more difficult generally available. Additional valuable information can be to estimate. A factor that is unique to skeletal adaptations to gained from mechanical testing of bone samples from hu- training is the slow turnover of bone tissue. Because it takes man cadavers and from animals subjected to various train- 3– 4 months for one remodeling cycle to complete the se- ing protocols, and from histological and gene expression quence of bone resorption, formation, and mineralization analyses from trained animals. Recent advances in protocols (85), a minimum of 6 – 8 months is required to achieve a that enhance the osteogenic response to mechanical loading new steady-state bone mass that is measurable.
in animals have not yet been evaluated in humans, but are The most common outcome measure used to assess the expected to stimulate new research in this area (116).
effects of physical activity on bone mass in humans is BMD, The purpose of this position stand is to provide recom- which describes the amount of mineral measured per unit mendations for the types of physical activities that are likely area or volume of bone tissue (51). Dual-energy x-ray ab- to promote bone health. The current state-of-knowledge sorptiometry (DXA) is the standard method of measuring regarding physical activity as it relates to 1) increasing peak areal BMD in clinical and research settings. The lumbar bone mass, 2) minimizing age-related bone loss, and 3) spine and proximal femur are the most common sites of preventing injurious falls and fractures will be discussed.
measurement by DXA because they are prone to disablingosteoporotic fractures. Other methods of assessing risk for ANIMAL STUDIES
osteoporosis include computed tomography (CT) measure-ment of spine volumetric BMD, and ultrasonography of the Various animal models have been utilized to study me- calcaneus, which provides an index of bone stiffness. Ul- chanical loading of the skeleton, but this section will focus trasonography is widely available, easy to perform, and does mainly on the commonly used rat model. Multiple factors not involve exposure to ionizing radiation, but should be characterize the physical activities that are likely to influ- ence properties of bone, including the type, intensity, dura- Official Journal of the American College of Sports Medicine tion, and frequency of the bone-loading activity. Studies of changes in bone mass (11). High strain rates also increased animals enable controlled manipulations of these factors to endocortical bone formation rate in an in vivo impact-load- determine their relative contributions to the osteogenic re- ing protocol (27,50). Such observations emphasize the need for further studies of the osteogenic effects of exercises thatgenerate high strain magnitude and rate, such as jumping Type of loading
Mechanical forces have osteogenic effects only if the Duration and frequency of loading
stress to bone is unique, variable, and dynamic in nature.
Static loading of bone (i.e., single, sustained force applica- The seminal work of Rubin and Lanyon (102) using tion) does not trigger the adaptive response that occurs with external loading demonstrated that only a few loading cy- dynamic loading (11). Studies of rats have evaluated the cles (e.g., 36 per day) of relatively high magnitude were osteogenic responses to several types of unique (i.e., not necessary to optimize the bone formation response; increas- usual cage activity) exercise interventions, including run- ing the number of loading cycles by 10-fold had no addi- ning (treadmill and voluntary), swimming, jumping, stand- tional effect. Similarly, in a more physiologic model of ing, climbing, and resistance training. Results have been loading in which rats jumped down from a height of 40 cm, equivocal, demonstrating that mechanical stress can en- as few as 5 jumps per day increased bone mass and strength of the tibia; increasing the number of jumps beyond 10 per (8,26,92,132) bone mass, formation, and/or mechanical day did not yield further benefit (118). It should be noted properties. In general, running and swimming of moderate that, in these studies, the levels of strain likely exceeded intensity have been found to have positive effects on bone those generated during typical human physical activities.
mass and material properties in the cortical and trabecular The interactions between frequency (repetitions per day and regions of the tibia and femur in growing and mature rats sessions per week) and intensity of loading cycles with (8,26,47,121,127,131). However, decreases in bone mass, respect to the resulting osteogenic response in humans is not trabecular thinning, and structural properties have been ob- served in response to exercise that is very intense and/or There is intriguing evidence from recent studies that excessive, particularly in growing animals (26,47,92,132).
applying a given number of loading cycles in multiple daily Activities that simulate resistance training in humans, in- sessions is more osteogenic than applying the same number cluding jumping up to a platform, voluntary tower climbing, of cycles in a single daily session (116). Rat ulnas that were and simulated “squat” exercises, have been found to have loaded 360 times per day in a single session (1ϫ360) for 16 positive effects on both cortical and trabecular bone regions wk absorbed 94% more energy before failing than the con- tralateral unloaded ulnas. However, ulnas that received the Another experimental paradigm that has been used to same 360 daily loading cycles over 4 sessions (4ϫ90) evaluate the osteogenic effects of mechanical stress in ani- absorbed 165% more energy before failing than unloaded mals is controlled in vivo external loading, including com- bones (116). These results suggest that bone cells lose pression of the ulna and four-point bending of the tibia. This sensitivity to mechanical stimulation after a certain number approach has an advantage over physical activity interven- of loading cycles, and that recovery periods are needed to tions in that it enables precise control and quantification of restore sensitivity to loading. It has been estimated that the mechanical loading forces. Studies of external loading complete restoration of sensitivity to loading requires a strongly support favorable adaptations of bone to mechan- recovery time of 8 h in rats, but recovery times as short as ical stress (116). For example, the four-point bending model 0.5–1.0 h have been found to be more osteogenic than no was used in rats to demonstrate that the osteogenic response recovery period (116). It will be important to determine in to loading is markedly enhanced when a given number of humans whether multiple, short daily exercise bouts are daily loading cycles are partitioned into multiple sessions more osteogenic than a single, longer daily exercise session.
separated by rest periods (116). It has not yet been deter-mined whether such findings are relevant to humans.
Other considerations
The ability of the skeleton to respond to mechanical Intensity of loading
loading can be either constrained or enabled by nutritional The primary mechanical variables associated with load or endocrine factors. One example of this is calcium insuf- intensity include strain magnitude and strain rate. Strain is a ficiency, which diminishes the effectiveness of mechanical measurement of the deformation of bone that results from an loading to increase bone mass (66). Another example is external load and is expressed as a ratio of the amount of estrogen status. The independent effects of estrogen on bone deformation to the original length. It has long been recog- metabolism are well described, but recent studies have de- nized that strain magnitude is positively related to the os- termined that the adaptive response of bone cells to me- teogenic response, but accumulating evidence suggests that chanical stress involves the estrogen receptor; blocking the strain rate is also an important factor (11). Increasing strain estrogen receptor impairs the bone formation response to rate, while holding loading frequency and peak strain mag- mechanical stress (133). This observation has led to the nitude constant, was found to be a positive determinant of hypothesis that a down-regulation of estrogen receptors as a Medicine & Science in Sports & Exerciseா consequence of postmenopausal estrogen deficiency de- profound when mechanical forces acting on the skeleton are creases the sensitivity of bone to mechanical loading.
The mechanisms of mechanotransduction in bone (i.e., Further research is needed to better understand the inter- how mechanical forces are translated into metabolic signals) actions of physical activity with genetics, diet, hormones, remain to be elucidated, and the discovery of key elements overuse, and other factors, with respect to the influence on in the mechanistic pathways will likely reveal factors, po- bone health. However, due to a paucity of evidence to date, tentially modifiable, that influence the osteogenic response to loading. As an example, it has been observed that pros-taglandins and nitric oxide are produced by bone cells in Role of physical activity in maximizing bone mass
response to mechanical loading, and that blocking their in children and adolescents
production impairs the bone formation response (16,115).
The translation of such information generated from studies A primary factor associated with risk for osteoporosis is of animals and cultured bone cells will be critical in finding the peak bone mass developed during childhood and the strategies to maximize the osteogenic effects of physical early adult years. Cross-sectional data suggest that trabec- ular bone loss begins as early as the third decade, whereascortical bone increases or remains constant until the fifthdecade (74,100). One longitudinal study found that HUMAN STUDIES
both cortical and trabecular bone mass continued to In humans, physical activity appears to play an important increase slightly in healthy young women well into the third role in maximizing bone mass during childhood and the early adult years, maintaining bone mass through the fifth It has been observed that bone mass is higher in children decade, attenuating bone loss with aging, and reducing falls who are physically active than in those who are less active and fractures in the elderly. The benefits of physical activity (108), and higher in children who participate in activities on bone health have typically been judged by measuring that generate high impact forces (e.g., gymnastics and bal- associations of physical activity level with bone mass and, let) than in those who engage in activities that impart lower in fewer studies, incidence of fractures, or by evaluating impact forces (e.g., walking) or are not weight bearing (e.g., changes in bone mass that occur in response to a change in swimming) (12,19,58). Recent studies have focused on physical activity level or to a specific exercise training jumping and other high-impact activities based on the the- program. In evaluating the osteogenic effects of exercise ory that high-intensity forces, imposed rapidly, produce training programs, the following principles should be noted: greater gains in bone mass than low- to moderate-intensity Specificity. Only skeletal sites exposed to a change in
forces (29,70,72,78,83,96). Ground-reaction forces during daily loading forces undergo adaptation.
jumping can reach 6 – 8 times body weight and some gym- Overload. An adaptive response occurs only when the
nastics maneuvers generate forces that are 10 –15 times loading stimulus exceeds usual loading conditions; contin- body weight; in contrast, ground-reaction forces during ued adaptation requires a progressively increasing overload.
walking or running are 1–2 times body weight (79). Most of Reversibility. The benefits of exercise on bone may not
the intervention studies of children were implemented as persist if the exercise is markedly reduced. However, the part of school programs and lasted between 7 and 20 months rate at which bone is lost when an exercise program is (29,70,72,78,83,96). These studies uniformly found that discontinued, and whether this is different in young vs older children who participated in the experimental high-impact individuals, is not well understood.
jumping and calisthenics programs increased bone mass to The associations of physical activity and specific types of a greater extent than children who participated in usual exercise with bone mass have been assessed in a variety of activities. One study that added weight lifting to other high- research paradigms. As reviewed previously (51,123), the impact loading exercises found robust increases in bone majority of studies have been cross-sectional, comparing mass of the hip, spine, and total body (83). Based on this nonathletes with athletes who participate in a variety of evidence, it is recommended that physical activity for chil- sports, or comparing people who report being sedentary dren should include activities that generate relatively high with those who report varying levels of physical activity.
ground-reaction forces, such as jumping, skipping, and run- Because of the numerous confounding factors inherent to ning and, possibly, strengthening exercises.
cross-sectional studies, these will be discussed only briefly.
Peak bone mineral accrual rate has been reported to occur The response of bone to changes in physical activity and at puberty (2), with 26% of adult total body bone mineral exercise training has also been assessed, including prospec- accrued within a 2-yr period of this time (3). Thus, the tive studies (e.g., athletes followed through peak and off- peri-pubertal period may represent a relatively short win- season training cycles) and controlled intervention studies in dow of time in which to maximize peak bone mass. Cross- which physical activity is increased (e.g., exercise training) sectional studies indicate that male and female adolescent or decreased (e.g., bed rest). Perhaps the most compelling athletes have higher, site-specific BMD when compared evidence that mechanical loading is essential to bone integ- with nonathletic adolescents (123). The effect is most pro- rity comes from studies of bed rest, space flight, and spinal nounced in athletes who participate in sports that generate cord injury, which demonstrate that bone loss is rapid and high-intensity ground- or joint-reaction forces (e.g., gym- Official Journal of the American College of Sports Medicine nastics, weight lifting) and less pronounced in athletes who portant to determine the influence of exercise on bone participate in sports that generate lower-intensity loading geometry in children and adolescents.
There have been few exercise intervention studies of Role of physical activity in young adults
adolescents, all involving girls only, with contradictory re-sults. No significant changes in BMD were found in re- Because peak bone mass is thought to be attained by the sponse to 6 months of resistance training (7), 9 months of end of the third decade, the early adult years may be the final resistance training and plyometrics with weighted vests opportunity for its augmentation. Numerous cross-sectional (129), or 9 months of step aerobics and plyometrics (44). In studies of male and female athletes representing a variety of contrast, significant increases in BMD occurred in response sports suggest that athletes have higher, site-specific BMD to 3 yr of artistic gymnastics (65), or 15 months of resistance values when compared with nonathletes (123). BMD values training (89). The most obvious difference between the tend to be highest in athletes who participate in sports that studies that elicited an effect of exercise and those that failed involve high-intensity loading forces, such as gymnastics, to do so was the duration of the intervention. However, these weight lifting, and body building, and lowest in athletes who studies involved a very small number of participants and participate in non–weight bearing sports such as swimming.
must be interpreted cautiously. There have been no well- As noted previously, inherent limitations of cross-sectional controlled studies that isolated the effects of exercise train- studies include confounding variables such as genetics, self- ing duration on the bone response, independent of changes selection, diet, hormones, and other factors.
A handful of prospective, controlled studies of athletes Three studies have attempted to determine at what point have monitored changes in bone mass through periods of in the peri-pubertal period the skeleton is most responsive to training or detraining. Bilateral differences in arm BMC of the benefits of physical activity or exercise training. One national level male tennis players (13–25%) were signifi-cantly greater than in controls (1–5%) and persisted after 4 study determined the effect of 9 months of step aerobics and yr of retirement (63). Studies of runners, rowers, power plyometrics on bone mineral content (BMC) in premenar- athletes, and gymnasts, ranging in duration from 7 months to cheal and postmenarcheal girls; control subjects were 2 yr all showed significant increases (1–5%) in either BMC matched on menarche status. BMC increased in response to or BMD of skeletal regions loaded by the specific type of exercise in premenarcheal girls only (44). Another study exercise performed during periods of training (123). In assessed the effect of 7 months of plyometrics on BMC and competitive gymnasts followed for 2 yr (111), BMD in- BMD in prepubertal (Tanner stage I) and early pubertal creased during the competitive seasons (2– 4%) and de- (Tanner stages II and III) girls. Significant bone gains were creased during the off-seasons (1%).
observed in the early pubertal, but not the prepubertal, girls A number of intervention studies ranging in duration when compared with controls (71). A cross-sectional study from 6 to 36 months have evaluated the effects of exercises evaluated humeral BMD of both the dominant and non- that generate relatively high ground-reaction and/or joint- dominant arms of female junior tennis players matched with reaction forces (e.g., resistance training, plyometrics) on controls for Tanner stage of maturity (39). Bilateral differ- bone mass of previously sedentary women. The majority of ences in BMD were similar in athletes and controls at these studies found significant increases in femoral neck Tanner stage I (9.4 yr), but became progressively larger in and/or lumbar spine BMD (1–5%) (4,5,28,43,68,77, athletes at Tanner stages II (10.8 yr), III (12.6 yr), and IV 112,128). In two of three studies of resistance training that (13.5 yr) with a plateau at stage V (15.5 yr). Based on these failed to elicit a significant effect on BMD, exercise inten- observations, bone appears to be most responsive to me- sity was only low to moderate (i.e., 60% or less of 1-repe- chanical stress during Tanner stages II through IV, corre- tition maximum, 1RM) (34,107). Exercise intensity was sponding to the 2-yr window that has been identified (3) for high in the third study (i.e., 80% 1RM; 5 sets; 10 repetitions; peak bone mineral accrual around the time of puberty.
4 d·wkϪ1) (122), but only the unilateral leg press exercise There remains a need for further research to elucidate the was performed and this exercise may have lacked site- best type and duration of exercise to augment bone accrual specificity for adaptation of the spine and femoral neck and the time during the growth period when loading is most because it was performed in a seated position (109). Two effective. The evidence to date supports the same prescrip- studies found an unexpected decrease in BMD in response tion noted previously for children (i.e., relatively high im- to relatively high-impact exercise. In one (101), there was pact and strengthening activities, such as plyometrics, gym- no change in femoral neck BMD but a 4% decrease in nastics, soccer, volleyball, and resistance training). These lumbar spine BMD after 9 months of resistance training; activities appear to be most effective in promoting bone exercise intensity was moderate (i.e., 70% 1RM). In the mineral accrual when started before or in the early pubertal other (124), there was a significant increase in total body period. Further, because measures of bone geometry may BMC (1–2%), a nonsignificant increase in spine BMD emerge as important determinants of bone strength that are (1%), and a significant decrease in femoral neck BMD independent of BMD (96), and because it seems plausible (1.5%) in response to 2 yr of resistance training and rope that geometric factors could be particularly responsive to skipping; however, exercise compliance was poor (i.e., mechanical stress during periods of growth, it will be im- 45%). Thus, although there is evidence that exercise training Medicine & Science in Sports & Exerciseா can increase BMD in young adult women, a number of the interaction between use of hormone therapy and phys- factors such as intensity of loading forces, site-specificity of ical activity with respect to relative risk for hip fracture. Hip the exercise, and adherence to the program may be impor- fracture risk was reduced by 60 –70% in women on hormone tant determinants of the relative effectiveness.
therapy, regardless of physical activity level, when com- Exercise training that generates high-intensity loading pared with sedentary women not on hormone therapy.
forces (i.e., high strain magnitude) may also induce changes Among women not on hormone therapy, those in the highest in body composition (i.e., fat and fat-free mass) and mus- quintile of physical activity (Ͼ24 MET⅐h⅐wkϪ1) also had a cular strength. This has stimulated interest in the potential 67% reduction in hip fracture risk, suggesting that a high additive and interactive effects of changes in body compo- level of physical activity may prevent fractures even if it sition and strength with the direct effects of mechanical does not attenuate bone loss. Fat-free mass remains a stron- loading on BMD. Significant correlations of body mass, fat ger determinant of bone mass with aging than either total mass, fat-free mass, and strength with total and regional mass or fat mass, although fat mass may also be an inde- BMD have been found in several studies, with these factors pendent determinant (1,6). Thus, physical activities that help accounting for up to 50% of the variance in BMD (109,113).
preserve muscle mass (e.g., resistance exercise) may also be Weight lifters typically have high levels of fat-free mass and strength compared with other athletes and BMD also tends The effect of exercise intervention on bone mass of post- to be highest in these athletes. For exercises, such as weight menopausal women has received considerable attention lifting, that introduce loading forces to the skeleton primar- over the past three decades; exercise programs have in- ily through joint-reaction forces (i.e., muscle contractions) cluded brisk walking, jogging, stair climbing/descending, rather than ground-reaction forces, it seems likely that in- rowing, weight lifting, and/or jumping exercises. The gen- creases in bone mass will occur only if the exercise is of eral conclusion from meta-analyses of published studies is sufficient intensity to cause an increase in muscle mass.
that a variety of types of exercise can be effective in pre- Although physical activities that involve high-intensity serving bone mass of older women (54,55).
skeletal loading are recommended to optimize and maintain Walking exercise programs of up to 1 yr have yielded bone mass in young adults, the benefits may not be realized only modest effects (88), if any (13,88), on the preservation in the presence of hormonal or dietary deficiencies or an of bone mass. This is not surprising as walking does not overuse syndrome. The Female Athlete Triad, consisting of generate high-intensity loading forces, nor does it represent disordered eating, amenorrhea, and osteoporosis, is an ex- a unique stimulus to bone in most individuals. These find- ample of the ineffectiveness of exercise to fully counteract ings do not rule out the possibility that habitual walking for the deleterious effects of other factors on bone health; this is many years helps to preserve bone. Studies that included reviewed in an ACSM Position Stand on this topic (94).
activities with higher intensity loading forces, such as stair Calcium and other nutritional deficiencies that can limit the climbing and jogging, generally found a more positive skel- osteogenic effects of exercise have been reviewed previ- ously (67), as have overuse syndromes such as stress frac- Exercise intervention trials that included high-intensity tures resulting from extreme, repetitive loading forces (10).
progressive resistance training have found increases in hipand spine BMD in estrogen-deficient women (22,56,57,60,82,87) and in women on hormone therapy (HT) (35,82).
Role of physical activity in middle-aged and older
Moderate-intensity resistance training has not been found to generate the same increases in hip BMD as high-intensity Bone mass decreases by about 0.5% per year or more training (56,57). In one study, the increase in BMD was after the age of 40, regardless of sex or ethnicity. In this linearly related to the total amount of weight lifted in a context, it is important to recognize that benefits of exercise progressive resistance exercise training program (22).
in middle-aged and older people may be reflected by an The osteogenic response to jumping exercise (i.e., per- attenuation in the rate of bone loss, rather than an increase forming vertical jumps from a standing position) appears to in bone mass. The rate of loss varies by skeletal region and be less robust in postmenopausal women than in children is likely influenced by such factors as genetics, nutrition, and young adults. Jumping exercise that increased hip BMD hormonal status, and habitual physical activity, making it of premenopausal women was not effective in postmeno- difficult to determine the extent to which the decline in bone pausal women not on HT, even when the duration of the mass is an inevitable consequence of the aging process. In exercise program was extended (5). Although not signifi- women, estrogen withdrawal at the menopause results in cant, the response of postmenopausal women on HT was rapid bone loss that is distinct from the slower age-related intermediate to that of the pre- and postmenopausal women bone loss. Comparisons of pre- and postmenopausal athletes not on HT. It should be noted that the exercise stimulus in suggest that even very vigorous levels of physical activity the study was constant, rather than progressive as would do not prevent the menopause-induced loss of bone mineral typically be prescribed. In a 5-yr study of a small group of (32,41,59,81,103). There have been no intervention studies postmenopausal women, exercisers who wore weighted of perimenopausal women to determine whether exercise vests averaging 5 kg during jumping activity preserved hip can attenuate the loss of bone during the menopausal tran- BMD to a greater extent than control subjects (110). There sition. However, the Nurses’ Health Study (24) examined is preliminary evidence that combining exercise with Official Journal of the American College of Sports Medicine bisphosphonate therapy may be effective in preventing os- and long period of observation that would be required.
There is encouraging evidence from a study conducted on a Recent findings that estrogen receptor antagonists impair small sample of postmenopausal women that a 2-yr trial of the response of bone cells to mechanical stress (15) have back strengthening exercises reduced the incidence of ver- raised the possibility that a down-regulation of estrogen tebral fractures over the subsequent 8 yr (106). However, receptors as a consequence of postmenopausal estrogen little other evidence exists from prospective trials that phys- deficiency decreases the sensitivity of bone to mechanical ical activity reduces the incidence of vertebral or wrist loading (49). Indeed, there is evidence that exercises that generate high-intensity loading forces are more effective in There is considerable evidence from epidemiologic stud- increasing BMD in postmenopausal women on HT than in ies that physical inactivity is a risk factor for hip fracture.
women not on HT (61,62,82,90), although this is not a The incidence of hip fracture has been found to be 20 – 40% uniform finding (42). It is also not clear whether the effects lower in individuals who report being physically active than of mechanical stress and HT are independent, or whether in those who report being sedentary (37,75). Elderly women HT modulates the response of bone to mechanical stress.
and men who were chronically inactive (i.e., rare stair The vast majority of osteoporosis prevention research has climbing, gardening, or other weight-bearing activities) focused on women because the incidence of osteoporotic were more than twice as likely to sustain a hip fracture as fractures does not increase markedly in men until the eighth those who were physically active, even after adjusting for or ninth decade (21). Research on the effectiveness of phys- differences in body mass index, smoking, alcohol intake, ical activity to preserve bone health of men is therefore and dependence in daily activities (18). A prospective study sparse, but is becoming increasingly important due to the of more than 30,000 Danish men and women found that the incidence of hip fracture in active people who became A strong association between BMD and jogging was sedentary was twice as high as in those who remained observed in 4254 men, aged 20 –59 yr (86). Men who jogged physically active (45). In the Finnish Twin Cohort, men who nine or more times per month had higher BMD levels than reported participation in vigorous physical activity had a men who jogged less frequently. In a 5-yr prospective study 62% lower relative risk of hip fracture than men who indi- of middle-aged and older runners (81), the rate of bone loss cated they did not participate in vigorous physical activity was attenuated in runners compared with controls. Among (64). The Nurses’ Health Study of more than 61,000 post- the runners, decreases in BMD were most pronounced in menopausal women suggested that the relative risk of hip men who substantially decreased their running volume. The fracture was reduced by 6% for every 3 MET⅐h⅐wkϪ1 of general conclusion from a meta-analysis of published exer- physical activity, which is roughly equivalent to 1 h of cise intervention studies was that exercise can improve or walking per week (24). Interestingly, women who reported walking at least 4 h⅐wkϪ1 had a 41% lower risk of hip Several studies have evaluated the effects of resistance fracture compared with sedentary peers who walked less training on bone mass in older men (9,73,76,80,130). The than 1 h⅐wkϪ1. This suggests that even low-intensity weight- duration of exercise ranged from 3 to 24 months and exer- bearing activity, such as walking, may be beneficial in cise intensity was moderate to high. All but one (76) of the lowering fracture risk, even though minimal changes in studies found beneficial effects of resistance training on BMD, most commonly at the femur; the study that did not Regular physical activity may help to prevent fractures by find a benefit used a moderate exercise intensity. In general, preserving bone mass and/or by reducing the incidence of the improvements in BMD in response to exercise were of injurious falls. Many factors contribute to falling, including the same relative magnitude as has been observed in diminished postural control, poor vision, reduced muscle women, although much larger increases were observed in strength, reduced lower limb range of motion, and cognitive male heart transplant patients who performed 6 months of impairment, as well as such extrinsic factors as psychotropic resistance exercise training (9). Thus, the types of exercise medications and tripping hazards. Exercise interventions programs that help to preserve bone mass in older women will be effective in reducing falls only if they are directed to individuals in whom the cause of falling involves factorsthat are amenable to improvement with exercise (e.g., poormuscle strength, balance, or range of motion). Reviews and Physical activity and fracture risk
meta-analyses of randomized trials (14,30,37) suggest that Osteoporotic fractures occur with minimal trauma in exercise trials that included balance, leg strength, flexibility, bones weakened because of low BMD or unfavorable ge- and/or endurance training effectively reduced risk of falling ometry (e.g., length or angle of the neck region of the proximal femur). The most common sites of osteoporotic It must be noted that some studies have found little or no fractures are the distal radius, spine, and the neck and effect of exercise interventions on the incidence of falls trochanteric regions of the femur. There have been no ran- (69,84). A recent Cochrane database review concluded that domized, controlled trials of the effectiveness of exercise to exercise alone does not reduce fall risk in elderly women reduce fractures, and such a trial would be extremely chal- and men (33). One reason forwarded for the lack of a lenging to conduct, in part because of the large sample size positive effect was that studies frequently targeted very frail Medicine & Science in Sports & Exerciseா nursing home residents, who likely had multiple risk factors ing; participation in sports that involve running and jumping for falling that would not be expected to be ameliorated by (soccer, basketball) is likely to be of benefit, but scientific exercise (e.g., poor vision). Further, if the exercise intensity is too low (common in studies of the frail elderly), only Intensity: high, in terms of bone-loading forces; for
minimal gains in muscle strength that might help reduce safety reasons, resistance training should be Յ60% of 1RM falling risk are achieved. Lastly, it must be recognized that Frequency: at least 3 d⅐wkϪ1
the opportunity for falling probably increases as people Duration: 10 –20 min (2 times per day or more may be
become more physically active, particularly in community- During adulthood, the primary goal of physical activity The type of exercise regimen most likely to reduce falls should be to maintain bone mass. Whether adults can in- remains unclear (14), because studies with positive and crease BMD significantly through exercise training remains negative findings overlap a great deal in the type of activity equivocal. When increases have been reported, it has been in utilized (i.e., oriented to strength, endurance, balance, or response to relatively high intensity weight-bearing endur- flexibility), duration of exercise, and frequency of training ance or resistance exercise; gains in BMD do not appear to sessions (51). It appears that balance training is a critical be preserved when the exercise is discontinued. Observa- component of these programs and should be included in tional studies suggest that the age-related decline in BMD is exercise interventions for older individuals at risk of falling.
attenuated, and the relative risk for fracture is reduced, in Improving muscle strength has been posited as potentially people who are physically active, even when the activity is one of the most effective means of reducing falls and frac- not particularly vigorous. However, there have been no ture incidence in the elderly because of its beneficial effects large randomized, controlled trials to confirm these obser- on multiple risk factors for fracture, such as low BMD, slow vations, nor have there been adequate dose-response studies walking speed, low levels of energy-absorbing soft tissue, to determine the volume of physical activity required for and immobility (75). There is further evidence that the gains such benefits. Animal research has demonstrated that me- in functional abilities after a course of resistance training chanical loading generates improvements in bone strength lead to an increase in voluntary physical activity in older (i.e., resistance to fracture) that are disproportionately larger adults (46) as well as in the very elderly living in nursing than the increases in bone mass. This supports the concept homes (25). The capacity of even frail elderly to exercise at that physical activity can reduce fracture risk even in the relatively high intensities may be habitually underestimated, absence of changes in BMD. Confirmation of this in humans though the feasibility of establishing community programs will require large randomized, controlled trials of the effects that utilize the intensive training that has been found to of physical activity on fracture incidence, although further increase muscle strength and improve functional ability (25) advancements in technology to enable the in vivo assess- is likely limited by the challenges of implementing such ment of bone strength will provide insight regarding programs outside a research setting.
whether this occurs. Evidence from multiple small random-ized, controlled trials of the effectiveness of exercise toincrease or maintain BMD suggests that the bone health of CONCLUSIONS
adults will be favorably influenced by the maintenance of a Weight-bearing physical activity has beneficial effects on high level of daily physical activity, as recommended by the bone health across the age spectrum. There is evidence that U.S. Surgeon General (117), if the activity is weight-bearing physical activities that generate relatively high-intensity in nature. It is important to note that, although physical loading forces, such as plyometrics, gymnastics, and high- activity may counteract to some extent the aging-related intensity resistance training, augment bone mineral accrual decline in bone mass, there is currently no strong evidence in children and adolescents. This is compatible with the that even vigorous physical activity attenuates the meno- findings from studies of animals that the osteogenic re- pause-related loss of bone mineral in women. Thus, phar- sponse to mechanical stress is maximized by dynamic load- macologic therapy for the prevention of osteoporosis may ing forces that engender a high strain magnitude and rate.
be indicated even for those postmenopausal women who are Further, there is some evidence that exercise-induced gains habitually physically active. Given the current state of in bone mass in children are maintained into adulthood, knowledge from multiple small randomized, controlled tri- suggesting that physical activity habits during childhood als and epidemiological studies, the following exercise pre- may have long-lasting benefits on bone health. It is not yet scription is recommended to help preserve bone health possible to describe in detail an exercise program for chil- dren and adolescents that will optimize peak bone mass, Mode: weight-bearing endurance activities (tennis; stair
because quantitative dose-response studies are lacking.
climbing; jogging, at least intermittently during walking), However, evidence from multiple small randomized, con- activities that involve jumping (volleyball, basketball), and trolled trials suggests that the following exercise prescrip- tion will augment bone mineral accrual in children and Intensity: moderate to high, in terms of bone-loading
Mode: impact activities, such as gymnastics, plyomet-
Frequency: weight-bearing endurance activities 3–5
rics, and jumping, and moderate intensity resistance train- times per week; resistance exercise 2–3 times per week Official Journal of the American College of Sports Medicine Duration: 30 – 60 min⅐dϪ1 of a combination of weight-
sistance activities aimed at preserving bone mass, but also bearing endurance activities, activities that involve jumping, activities designed to improve balance and prevent falls.
and resistance exercise that targets all major muscle groups Maintaining a vigorous level of physical activity across It is not currently possible to easily quantify exercise the lifespan should be viewed as an essential component of intensity in terms of bone-loading forces, particularly for the prescription for achieving and maintaining optimal bone weight-bearing endurance activities. However, in general, health. Further research will be required to define the type the magnitude of bone-loading forces increases in parallel and quantity of physical activity that will be most effective with increasing exercise intensity quantified by conven- in developing and maintaining skeletal integrity and mini- tional methods (e.g., percent of maximal heart rate or per- The general recommendation that adults maintain a rela- ACKNOWLEDGMENT
tively high level of weight-bearing physical activity forbone health does not have an upper age limit, but as age This pronouncement was reviewed for the American increases so, too, does the need for ensuring that physical College of Sports Medicine by members-at-large; the activities can be performed safely. In light of the rapid and Pronouncements Committee; and by Debra Bemben, Ph.D., profound effects of immobilization and bed rest on bone FACSM; Patricia Fehling, Ph.D., FACSM; Scott Going, loss, and the poor prognosis for recovery of mineral after Ph.D.; Heather McKay, Ph.D.; Charlotte Sanborn, Ph.D., remobilization, even the frailest elderly should remain as FACSM; and Christine Snow, Ph.D., FACSM.
physically active as their health permits to preserve skeletal This Position Stand replaces the 1995 ACSM Position integrity. Exercise programs for elderly women and men Stand, “Osteoporosis and Exercise,” Med. Sci. Sports Exerc. should include not only weight-bearing endurance and re- REFERENCES
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