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Bone mass and exercise
Bone Mass and Exercise C. H.
CHESNUT
III,
M.D.,
Seattle, Washington
The overall role of exercise as an integral part of osteoporosis prevention and treatment remains unclear and controversial. Comparatively well accepted are the facts that disuse results in bone mass loss, that sedentary individuals in general have less bone mass than exercising individuals (from cross-sectional study data), that exercise may produce a modest increase in bone mass (from longitudinal study data), and that exercise cannot compensate for estrogen loss. However, numerous questions regarding exercise and the skeleton remain to be answered, such as how the apparent osteogenic effect of exercise is mediated, what is the relationship of exercise in reducing fractures, how to reconcile the discrepancy between exercise-induced bone mass gain (lesser) and disuse bone loss (greater). At present, it seems reasonable to recommend avoidance of a sedentary existence, and participation in a moderate exercise program, for individuals seeking to prevent or treat osteoporosis, recognizing that much of the benefit may be in the resultant increase in muscle strength, in coordination, and in flexibility associated with such a program.
From the Osteoporosis
Nuclear
5A-345
Medicine
Research Center, University
RC-70, University
November
30, 1993
of Washington
of Washington Medical Cen-
Medical Center, Seattle,
The American Journal of Medicine
T
he value of exercise in preventing and treating osteoporosis remains unclear and controversial [l-4]. Whereas a number of observations regarding physical activity and the skeleton may be accepted as incontrovertible, a plethora of unanswered questions and/or untested hypotheses remain; nevertheless, a number of pragmatic recommendations can be made for individuals who are concerned about osteoporosis. Which observations regarding exercise and bone appear well validated? l Without weight bearing (mechanical loading, gravitational force), bone mass loss will occur at axial and appendicular skeletal sites [5-‘71. Extensive animal studies and studies in human bed rest volunteers and space flight participants confirm this observation. l Active individuals possess a greater bone mass than inactive individuals, at least as confirmed by cross-sectional studies. Figure 1, a compilation of cross-sectional studies in females ~50 or >50 years of age, demonstrates higher lumbar bone mineral density (BMD) in exercising women compared to sedentary individuals. l Sedentary individuals can increase bone mass slightly by becoming more active, as confirmed in longitudinal studies (Figure 1). l Exercise cannot entirely compensate for decreased endogenous estrogen levels in either the pre- or postmenopausal women [8,9]. However, qualifications must be made of even these comparatively well-accepted facts. For instance, cross-sectional studies can demonstrate only an association, and not causation, between bone mass and activity, and not all studies have confirmed such an exercise-bone mass association in all women. As an example of the latter observation, Kirk et a2 [lo] detected no difference in lumbar spine BMD between exercising women (master runners) and sedentary women aged 55-65. Data from longitudinal studies exploring the relationship between bone mass and exercise over time must also be qualified: indeed, there are relatively few rigorously defined prospective longitudinal studies, and not all of these show a beneficial effect. Two studies [11,12] have shown a negative or no effect of bone mineral density from weight-lifting programs, and Mazess and Barden [13] have noted no association between moderate activity levels and
Volume 95 (SUPPI 5A)
CONSENSUS
spine, hip, radius, or humeral bone mineral density over 2 years. However, Reeker et al [14] did note a significant effect of activity on lumbar BMD over a similar 2-year period, as well as a significant interaction with calcium. Also, as noted in Figure 1, the difference in BMD in active and sedentary women is obviously much larger in cross-sectional than in longitudinal trials. This discrepancy might be due to the years of training activity in the sense that prospective studies are typically completed within 1-2 years, while cross-sectional studies may involve athletic women who have been active for many years prior to their bone mass measurement. Also, the selection of the activities for prospective studies may introduce bias; many studies do not allow for a progressive increase in skeletal loading. For instance, a recent study [15] noted no significant increase in spinal BMD in women completing a l-year walking program; such a walking program may not have provided a progressive increase in skeletal loading, in the sense that the women presumably walked prior to study participation. The magnitude of the effect in longitudinal studies may also be biased by utilization of sedentary individuals who enter the study with a lower bone mass level, optimizing the chance of a significant increase in BMD. Both cross-sectional studies and prospective longitudinal trials often suffer from a lack of skeletal site specificity (i.e., measuring a bone mass site discordant from the site subject to loading/weight bearing). For instance, one study [16] noted no effect on radial bone mineral density from a walking program. Overall, as noted in Figure 2, in studies examining the relationship of exercise and BMD, only approximately 5% of the variability in bone mineral density can be explained by exercise. Therefore, in spite of a number of observations regarding exercise and bone mass being relatively well accepted, the exact relationship between exercise and the skeleton remains unclear. To elucidate this relationship further, a number of fundamental questions regarding exercise and the skeleton need to be explored, and hopefully answered, over the next few years: 1. It is generally accepted that the effect of increased or decreased loading is modulated by hormonal and nutritional (and possibly electrophysiological) effects; what is the exact mechanism of the osteogenic response to loading and unloading? 2. What is the relationship between activity and hip bone mass, and between activity and skeletal fracture? Although bone mass seems to respond to exercise, there are no prospective data to show that exercise protects against fracture.
% Difference
X-SEC #R=lS
CONFERENCE
ON OSTEOPOROSIS
/ CHESNUT
in Lumbar BMD
L #R=4
X-SEC #R=3
L RR=10
Figure 1. Effect of exercise on lumbar bone mrneral density (BMD). Cross-sectional (X-SEC) and longitudinal (L) studies; #R = number of studies assessed. (Adapted from [3], with permission).
3. What is the role of exercise in protecting against bone mass loss in males? 4. How is the discrepancy explained between the greater bone mass loss associated with immobilization/disuse/inactivity and the lesser bone mass gain associated with increased activity? A l-2% improvement in bone mass may occur within 12 months of increased activity, with 3-4% losses with immobilization for 1 month. 5. What is the age specificity of exercise programs (i.e., is the exercise model for teenage women appropriate for postmenopausal women)? Quite obviously, exercise-program compliance for a teenage woman may be quite different from that for a postmenopausal woman, and adapting such a program to achieve satisfactory compliance should be based on firm data demonstrating potential benefit for the skeleton.
Relationship of physical activity and BMD r R2 Ages 18-26 0.175 0.03 0.01 Ages 17m38 0.10 0.09 0.01 x age 57.6 0.23 0.05 Ages 21-95 L
Figure 2. Relationship of physical activity and bone mineral density @MD). r = the association (correlation) between physical activity and BMD in each of four studies, and R2 = the variable in BMD contributed by physical activity. (Personal communication B.L. Drinkwater, 1993.)
November 30, 1993
The American Journal of Medicine
Volume 95 (suppl 5A)
5A-35s
CONSENSUS
CONFERENCE
ON OSTEOPOROSIS/
CHESNUT
6. In women, is there a genetic potential for peak REFERENCES bone mass attainment that can be realized by dra- 1. Drinkwater EL. Exercise in the prevention of osteoporosis. Osteoporosis Int 1993; matically increasedlevels of exercise, or are most 3 (Suppl 1): S169-71. B. Exercise in the prevention of osteoporosis. In: Christiansen C, Riis normally exercising young women already at their 2.B, Drinkwater eds. ,Proceedings 1993. Fourth International Symposium on Osteoporosis and training “ceiling,” with little additionalbenefit to be Consensus Development Conference, Copenhagen: Handelstrykkeriet Aalborg ApS; gained by such an increase in activity? 1993: 105-8. Drinkwater BL. Physical fitness, activity, and osteoporosis. In: Bouchard, eds. Given, then, the controversy regarding the role 3.Physical Activity, Fitness, and Health Proceedings, 1992. Champagne, IL: Human of exercise in skeletal health, what can be recom- Kinetics Publishers, 1993, (in press). mended in terms of exercise for the patient or 4. Marcus R, Drinkwater B, Dalsky G, et al. Osteoporosis and exercise in woman. Sci Sports Exert 1993; 24 (Suppl); S301-7. health care professional trying to prevent and/or 5.MedKrolner B, Toft B, Nielsen SP, Tondevold E. Physical exercise as prophylaxis treat osteoporosis?While the most beneficial type, against involutional vertebral bone loss: a controlled trial. Clin Sci 1983; 64; 541-6. duration, and intensity of exercise for the individ- 6. Donaldson CL, Hulley SE, Vogel JM, et al. Effect of prolonged bed rest on bone ual subject has yet to be determined, avoidanceof mineral. Metabolism 1970; 19; 1071-84. Vogel JM, Whittle MW, Smith MC, Rambaut PC. Bone mineral measurement, inactivity and participation in a reasonable(moder- 7.experiment MO78 In: Biomedical Results from Skylab, National Aeronautics and ate) exercise program can (and should)be encour- Space Administration. Washington, DC: GPO, 19T 183-90. aged.The cost- and risk-benefit ratios for exercise 8. Drinkwater BL, Nilson K, Chesnut CH, eta/. Bone mineral content of amenorrheic are positive; exercise programs are generally safe and eumenorrheic athletes. N Engl J Med 1984; 311: 277-81. 9. Prince R, Smith M, Dick IM, et al. Prevention of osteoporosis: a comparative (in moderation), inexpensive, and logistically sim- study of exercise, calcium supplementation, and hormone-replacement therapy. N ple to complete. In addition, beneficial effects on Engl J Med 1991; 325: 1189-95. strength, coordination, and flexibility may be an 10. Kirk S, Sharp CF, Elbaum N, et al. Effect of long-distance running on bone mass additional skeletal benefit of exercise, particularly in women. J Bone Miner Res 1989; 4: 515-22. Gleeson PB, Protas EJ, LeBlanc A, et al. Effects of weight lifting on bone mineral in the elderly woman (i.e., improved coordination 11. density in premenopausal women. J Bone Miner Res 1990; 5: 153-8. and muscular strength may prevent falls). 12. Rockwell JC, Sorenson AM, Baker S, ef al. Weight training decreases vertebral Thus, while the value of exercisefor the skeleton bone density in premenopausal women; a prospective study. J Clin Endocrinol Metab 1990; 71: 988-93. remains incompletely defined,the assetsof an exer- 13. RB, Barden HS. Bone density in pre-menopausal women: effect of age, cise program would seemto outweigh its liabilities. dietaryMazess intake, physical activity, smoking, and birth-control pills. Am J Clin Nutr 1991; In fact, for osteoporosisprevention and treatment, 53; 132-42. in terms of exercise a secular variant of Pascal’s 14. Reeker RR, Davies KM, Hinders SM, et al. Bone gain in young adult women. JAMA 1992; 268: 2403-B. wager [17] might seem prudent: 15. Nelson ME, Fisher EC, Dilmaninan FA, et al. A one-year walking program and Let us weigh the gain and the loss in wagering that God is. Let us estimate these two chances. If you gain, you gain all; if you lose, you lose nothing. Wager, then, without hesitation that He is.
5A-36s
November
30, 1993
The American Journal of Medicine
increased calcium in postmenopausal women: effects on bone. Am J Clin Nutr 1991; 53: 1304-11. 16. Sandler RB, Cauley JA, Horn DL, et al. The effects of walking on the crosssectional dimensions of the radius in postmenopausal women. Calcif Tissue lnt 1987; 41: 65-9. 17. Pascal B. Pensees, 1670.
Volume 95 (suppl 5A)
CHESNUT
III,
M.D.,
Seattle, Washington
The overall role of exercise as an integral part of osteoporosis prevention and treatment remains unclear and controversial. Comparatively well accepted are the facts that disuse results in bone mass loss, that sedentary individuals in general have less bone mass than exercising individuals (from cross-sectional study data), that exercise may produce a modest increase in bone mass (from longitudinal study data), and that exercise cannot compensate for estrogen loss. However, numerous questions regarding exercise and the skeleton remain to be answered, such as how the apparent osteogenic effect of exercise is mediated, what is the relationship of exercise in reducing fractures, how to reconcile the discrepancy between exercise-induced bone mass gain (lesser) and disuse bone loss (greater). At present, it seems reasonable to recommend avoidance of a sedentary existence, and participation in a moderate exercise program, for individuals seeking to prevent or treat osteoporosis, recognizing that much of the benefit may be in the resultant increase in muscle strength, in coordination, and in flexibility associated with such a program.
From the Osteoporosis
Nuclear
5A-345
Medicine
Research Center, University
RC-70, University
November
30, 1993
of Washington
of Washington Medical Cen-
Medical Center, Seattle,
The American Journal of Medicine
T
he value of exercise in preventing and treating osteoporosis remains unclear and controversial [l-4]. Whereas a number of observations regarding physical activity and the skeleton may be accepted as incontrovertible, a plethora of unanswered questions and/or untested hypotheses remain; nevertheless, a number of pragmatic recommendations can be made for individuals who are concerned about osteoporosis. Which observations regarding exercise and bone appear well validated? l Without weight bearing (mechanical loading, gravitational force), bone mass loss will occur at axial and appendicular skeletal sites [5-‘71. Extensive animal studies and studies in human bed rest volunteers and space flight participants confirm this observation. l Active individuals possess a greater bone mass than inactive individuals, at least as confirmed by cross-sectional studies. Figure 1, a compilation of cross-sectional studies in females ~50 or >50 years of age, demonstrates higher lumbar bone mineral density (BMD) in exercising women compared to sedentary individuals. l Sedentary individuals can increase bone mass slightly by becoming more active, as confirmed in longitudinal studies (Figure 1). l Exercise cannot entirely compensate for decreased endogenous estrogen levels in either the pre- or postmenopausal women [8,9]. However, qualifications must be made of even these comparatively well-accepted facts. For instance, cross-sectional studies can demonstrate only an association, and not causation, between bone mass and activity, and not all studies have confirmed such an exercise-bone mass association in all women. As an example of the latter observation, Kirk et a2 [lo] detected no difference in lumbar spine BMD between exercising women (master runners) and sedentary women aged 55-65. Data from longitudinal studies exploring the relationship between bone mass and exercise over time must also be qualified: indeed, there are relatively few rigorously defined prospective longitudinal studies, and not all of these show a beneficial effect. Two studies [11,12] have shown a negative or no effect of bone mineral density from weight-lifting programs, and Mazess and Barden [13] have noted no association between moderate activity levels and
Volume 95 (SUPPI 5A)
CONSENSUS
spine, hip, radius, or humeral bone mineral density over 2 years. However, Reeker et al [14] did note a significant effect of activity on lumbar BMD over a similar 2-year period, as well as a significant interaction with calcium. Also, as noted in Figure 1, the difference in BMD in active and sedentary women is obviously much larger in cross-sectional than in longitudinal trials. This discrepancy might be due to the years of training activity in the sense that prospective studies are typically completed within 1-2 years, while cross-sectional studies may involve athletic women who have been active for many years prior to their bone mass measurement. Also, the selection of the activities for prospective studies may introduce bias; many studies do not allow for a progressive increase in skeletal loading. For instance, a recent study [15] noted no significant increase in spinal BMD in women completing a l-year walking program; such a walking program may not have provided a progressive increase in skeletal loading, in the sense that the women presumably walked prior to study participation. The magnitude of the effect in longitudinal studies may also be biased by utilization of sedentary individuals who enter the study with a lower bone mass level, optimizing the chance of a significant increase in BMD. Both cross-sectional studies and prospective longitudinal trials often suffer from a lack of skeletal site specificity (i.e., measuring a bone mass site discordant from the site subject to loading/weight bearing). For instance, one study [16] noted no effect on radial bone mineral density from a walking program. Overall, as noted in Figure 2, in studies examining the relationship of exercise and BMD, only approximately 5% of the variability in bone mineral density can be explained by exercise. Therefore, in spite of a number of observations regarding exercise and bone mass being relatively well accepted, the exact relationship between exercise and the skeleton remains unclear. To elucidate this relationship further, a number of fundamental questions regarding exercise and the skeleton need to be explored, and hopefully answered, over the next few years: 1. It is generally accepted that the effect of increased or decreased loading is modulated by hormonal and nutritional (and possibly electrophysiological) effects; what is the exact mechanism of the osteogenic response to loading and unloading? 2. What is the relationship between activity and hip bone mass, and between activity and skeletal fracture? Although bone mass seems to respond to exercise, there are no prospective data to show that exercise protects against fracture.
% Difference
X-SEC #R=lS
CONFERENCE
ON OSTEOPOROSIS
/ CHESNUT
in Lumbar BMD
L #R=4
X-SEC #R=3
L RR=10
Figure 1. Effect of exercise on lumbar bone mrneral density (BMD). Cross-sectional (X-SEC) and longitudinal (L) studies; #R = number of studies assessed. (Adapted from [3], with permission).
3. What is the role of exercise in protecting against bone mass loss in males? 4. How is the discrepancy explained between the greater bone mass loss associated with immobilization/disuse/inactivity and the lesser bone mass gain associated with increased activity? A l-2% improvement in bone mass may occur within 12 months of increased activity, with 3-4% losses with immobilization for 1 month. 5. What is the age specificity of exercise programs (i.e., is the exercise model for teenage women appropriate for postmenopausal women)? Quite obviously, exercise-program compliance for a teenage woman may be quite different from that for a postmenopausal woman, and adapting such a program to achieve satisfactory compliance should be based on firm data demonstrating potential benefit for the skeleton.
Relationship of physical activity and BMD r R2 Ages 18-26 0.175 0.03 0.01 Ages 17m38 0.10 0.09 0.01 x age 57.6 0.23 0.05 Ages 21-95 L
Figure 2. Relationship of physical activity and bone mineral density @MD). r = the association (correlation) between physical activity and BMD in each of four studies, and R2 = the variable in BMD contributed by physical activity. (Personal communication B.L. Drinkwater, 1993.)
November 30, 1993
The American Journal of Medicine
Volume 95 (suppl 5A)
5A-35s
CONSENSUS
CONFERENCE
ON OSTEOPOROSIS/
CHESNUT
6. In women, is there a genetic potential for peak REFERENCES bone mass attainment that can be realized by dra- 1. Drinkwater EL. Exercise in the prevention of osteoporosis. Osteoporosis Int 1993; matically increasedlevels of exercise, or are most 3 (Suppl 1): S169-71. B. Exercise in the prevention of osteoporosis. In: Christiansen C, Riis normally exercising young women already at their 2.B, Drinkwater eds. ,Proceedings 1993. Fourth International Symposium on Osteoporosis and training “ceiling,” with little additionalbenefit to be Consensus Development Conference, Copenhagen: Handelstrykkeriet Aalborg ApS; gained by such an increase in activity? 1993: 105-8. Drinkwater BL. Physical fitness, activity, and osteoporosis. In: Bouchard, eds. Given, then, the controversy regarding the role 3.Physical Activity, Fitness, and Health Proceedings, 1992. Champagne, IL: Human of exercise in skeletal health, what can be recom- Kinetics Publishers, 1993, (in press). mended in terms of exercise for the patient or 4. Marcus R, Drinkwater B, Dalsky G, et al. Osteoporosis and exercise in woman. Sci Sports Exert 1993; 24 (Suppl); S301-7. health care professional trying to prevent and/or 5.MedKrolner B, Toft B, Nielsen SP, Tondevold E. Physical exercise as prophylaxis treat osteoporosis?While the most beneficial type, against involutional vertebral bone loss: a controlled trial. Clin Sci 1983; 64; 541-6. duration, and intensity of exercise for the individ- 6. Donaldson CL, Hulley SE, Vogel JM, et al. Effect of prolonged bed rest on bone ual subject has yet to be determined, avoidanceof mineral. Metabolism 1970; 19; 1071-84. Vogel JM, Whittle MW, Smith MC, Rambaut PC. Bone mineral measurement, inactivity and participation in a reasonable(moder- 7.experiment MO78 In: Biomedical Results from Skylab, National Aeronautics and ate) exercise program can (and should)be encour- Space Administration. Washington, DC: GPO, 19T 183-90. aged.The cost- and risk-benefit ratios for exercise 8. Drinkwater BL, Nilson K, Chesnut CH, eta/. Bone mineral content of amenorrheic are positive; exercise programs are generally safe and eumenorrheic athletes. N Engl J Med 1984; 311: 277-81. 9. Prince R, Smith M, Dick IM, et al. Prevention of osteoporosis: a comparative (in moderation), inexpensive, and logistically sim- study of exercise, calcium supplementation, and hormone-replacement therapy. N ple to complete. In addition, beneficial effects on Engl J Med 1991; 325: 1189-95. strength, coordination, and flexibility may be an 10. Kirk S, Sharp CF, Elbaum N, et al. Effect of long-distance running on bone mass additional skeletal benefit of exercise, particularly in women. J Bone Miner Res 1989; 4: 515-22. Gleeson PB, Protas EJ, LeBlanc A, et al. Effects of weight lifting on bone mineral in the elderly woman (i.e., improved coordination 11. density in premenopausal women. J Bone Miner Res 1990; 5: 153-8. and muscular strength may prevent falls). 12. Rockwell JC, Sorenson AM, Baker S, ef al. Weight training decreases vertebral Thus, while the value of exercisefor the skeleton bone density in premenopausal women; a prospective study. J Clin Endocrinol Metab 1990; 71: 988-93. remains incompletely defined,the assetsof an exer- 13. RB, Barden HS. Bone density in pre-menopausal women: effect of age, cise program would seemto outweigh its liabilities. dietaryMazess intake, physical activity, smoking, and birth-control pills. Am J Clin Nutr 1991; In fact, for osteoporosisprevention and treatment, 53; 132-42. in terms of exercise a secular variant of Pascal’s 14. Reeker RR, Davies KM, Hinders SM, et al. Bone gain in young adult women. JAMA 1992; 268: 2403-B. wager [17] might seem prudent: 15. Nelson ME, Fisher EC, Dilmaninan FA, et al. A one-year walking program and Let us weigh the gain and the loss in wagering that God is. Let us estimate these two chances. If you gain, you gain all; if you lose, you lose nothing. Wager, then, without hesitation that He is.
5A-36s
November
30, 1993
The American Journal of Medicine
increased calcium in postmenopausal women: effects on bone. Am J Clin Nutr 1991; 53: 1304-11. 16. Sandler RB, Cauley JA, Horn DL, et al. The effects of walking on the crosssectional dimensions of the radius in postmenopausal women. Calcif Tissue lnt 1987; 41: 65-9. 17. Pascal B. Pensees, 1670.
Volume 95 (suppl 5A)