Medicine & Science in Sports & Exercise:
Clinical Sciences: Symposium: Resistance Training For Health And Disease
The effects of progressive resistance training on bone density: a review
LAYNE, JENNIFER E.; NELSON, MIRIAM E.
Section Editor(s): Pollock, Michael L.
Nutrition, Exercise Physiology and Sarcopenia Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, Boston, MA 02111
Submitted for publication June 1997.
Accepted for publication February 1998.
The authors wish to express their gratitude to Andrea Nuernberger and Erin Gunselman for their help in researching the material for this manuscript.
Conflict of interest: This work has been supported by federal funds from the U.S. Department of Agriculture, and Agricultural Research Service Contract 53-3K06-5-10 and the Brookdale National Fellowship. The contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture or the American College of Sports Medicine, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. government or the American College of Sports Medicine. The authors have no professional relationships with companies or manufacturers that will benefit from the results of the present manuscript.
Address for correspondence: Jennifer E. Layne, M.S., NEPS Laboratory, JM-USDA-HNRCA, 711 Washington Street, Boston, MA 02111.
The effects of progressive resistance training on bone density: a review. Med. Sci. Sports Exerc., Vol. 31, No. 1, pp. 25-30, 1999. Osteoporosis is a major public health problem that is characterized by low bone mass and increased susceptibility to fractures, primarily of the hip, spine, and wrist. It is estimated to cause 1.5 million fractures annually in the United States in people aged 50 yr and older. Physical activity, particularly weight-bearing exercise, is thought to provide the mechanical stimuli or "loading" important for the maintenance and improvement of bone health, whereas physical inactivity has been implicated in bone loss and its associated health costs. Both aerobic and resistance training exercise can provide weight-bearing stimulus to bone, yet research indicates that resistance training may have a more profound site specific effect than aerobic exercise. Over the past 10 years, nearly two dozen cross-sectional and longitudinal studies have shown a direct and positive relationship between the effects of resistance training and bone density. Conversely, a handful of other studies have reported little or no effect on bone density. However, these results may be partially attributable to the study design, intensity and duration of the exercise protocol, and the bone density measurement techniques used. High-intensity resistance training, in contrast to traditional pharmacological and nutritional approaches for improving bone health in older adults, has the added benefit of influencing multiple risk factors for osteoporosis including improved strength and balance and increased muscle mass.
Progressive resistance training by nonathletic populations, including the elderly, is a relatively new practice. Historically "weight lifting" or "strength training" has been limited to young, athletic individuals seeking to improve performance as a component of a sports training program. As a result, strength training research has concentrated on this population. However, the benefits gained from resistance training, specifically improved muscle strength, agility, and resilience, extend beyond the playing field to the performance of daily activities. Over the past decade, numerous studies have focused on bone and resistance training. In older populations, the effects of resistance training may make a difference in being able to climb stairs, carry groceries, or rise from a chair. In addition, resistance training may have a significant impact in maintaining bone health. Recently, progressive resistance training principles have been applied to a large and growing population of older men and women for whom the relationship of muscle strength and balance is critical in maintaining functional independence and resisting falls and for decreasing risk factors associated with osteoporosis. Several studies have shown that resistance training can greatly increase physical strength in elderly people and may have a positive effect on bone (1,7,8,10,20). This paper will review the results of both cross-sectional and longitudinal research reported over the past 10 years examining the effects of resistance training on bone in adult men and women.
Wolff's law states that stress or mechanical loading applied to the bone via the muscle and tendons has a direct effect on bone formation and remodeling (2). A review of recent cross-sectional studies examining this principle is provided in Table 1. Two of these studies (4,16) have shown that male weight lifters have greater bone mineral density (BMD) than nonathletes. Karlsson et al. (16) proposed that this effect is site-specific, based upon the higher total body BMD (TBBMD) and higher BMD in all sites measured (spine, hip, tibia, and forearm) except for the skull of both active and retired weight lifters aged 16-54 yr, when compared with a control group. Several other studies (13,31,33) have compared the bone density of male weight lifters to other athletes to determine whether the effect on bone is sport-specific. Hamdy et al. (13) compared the bone density of weight lifters, runners, recreational athletes, and cross-trainers measured by dual photon absorptiometry and reported that the upper arm BMD was highest in the weight lifters and cross-trainers (who performed upper body weight training as part of their program) when compared with runners who did not include upper body training. These results also support the theory that the effects of resistance training on bone are site-specific. No differences were noted in vertebral and lower body bone density between the four exercise groups as each group of athletes performed some type of weight-bearing exercise. Similarly, Smith et al. (31) reported that the rowers who weight trained had a significantly greater TBBMD, total spine, lumbar spine, and pelvic BMD measured by dual energy x-ray absorptiometry when compared with either triathletes or a control group. Arm bone density was also significantly greater in the weight lifters compared with that of the control group.
Cross-sectional investigations can be suggestive of the relationships between bone and strength training exercises and can provide information derived from observation of relatively large samples. However, these studies compare independent samples and therefore are not able to establish a causal relationship between the variables of interest. In addition, a methodological criticism of cross-sectional studies using weight lifters as subjects is that these studies do not control for the possible effect of anabolic steroid use and its potential influence on bone density. Fiore et al. (9) reported significantly greater BMC and BMD of the distal radius in body-builders versus matched controls. No significant differences in BMC and BMD were seen between 8 body-builders who took androgens and 10 who were drug-free in this study examining the effect of self-administered anabolic steroid use on bone formation. The results of this study should be interpreted cautiously as it was not a randomized, controlled trial, and the administration of steroids was not monitored.
A cross-sectional study of active older men aged 70-81 yr with a long-term training history in either endurance training, resistance training, or speed training indicated that the three groups of athletes had greater bone mineral content (BMC) at the calcaneous measured by SPA and weight-adjusted BMC than an aged-matched population sample (33). This result may be a general effect of weight-bearing exercise on the calcaneous.
Cross-sectional studies utilizing female athletes also indicate that resistance training is positively associated with bone density (5,14,15). A comparison of trained competitive weight lifters, orienteers, cross-country skiers, and cyclists (total N = 105) and an aged-matched control group (N = 25) indicated a higher mean weight-adjusted BMD in female weight lifters in all sites except the femoral neck and calcaneus when compared with the control group (14). Moreover, the weight lifter's BMD was also significantly greater than the other exercise groups in the lumbar spine, distal femur, patella, and distal radius (14). Interestingly, the weight lifters had trained fewer years than the other athletes, yet they had the highest values in BMD. Another study (15) comparing female weight lifters, runners, and swimmers found that the weight lifters had greater mean BMC at all sites in comparison with runners, swimmers and a control group. Davee et al. (5) also reported that women who combined aerobic and muscle building exercises had a higher lumbar BMD when compared to control and aerobic exercise groups not utilizing a resistance training program.
The majority of longitudinal studies have been performed in women due to the critical importance of maintaining bone health and preventing osteoporosis in this population. A review of recent longitudinal studies is provided in Table 2. Interpretation of longitudinal trials examining the impact of resistance training on bone requires a critical examination of the study designs to fully understand and compare results of different studies. Randomized study designs reduce self-selection in group assignment, which is particularly important in exercise trials where individuals may be more or less predisposed to participate in physical activity.
The effects of a recent long-term randomized controlled prospective study of high intensity resistance training in young women indicated that regional BMD at the femoral and trochanteric sites can be increased by resistance training exercise (17). TBBMD did not change significantly over the 18 months of this trial despite these regional changes and significant increases in maximal and isokinetic strength. Lohman et al. (17) speculate that increases in strength and lean tissue may be greater than increases in BMD in premenopausal women and that in young women there may be a site-specific redistribution of bone mineral rather than a total body increase in BMC. Similarly, Snow-Harter et al. (32) noted significant increases in lumbar BMD in young women completing either a progressive aerobic training program (jogging) or a progressive resistance training program, when compared with a control group. The resistance training group showed significant strength increases when compared with the aerobic trained women; however, the increases in bone density were not significantly different between the two exercise groups (32). This result is consistent with the site-specific principles of mechanical loading as both groups of women performed weight-bearing exercise stressing the lower body and spine. Differences might not necessarily be expected between exercise groups due to the short duration of the protocol and the physiologic limits of bone formation and remodeling.
Gleeson et al. (11) reported positive and significant increases in both muscle strength and lumbar BMD in premenopausal women ranging from 23-46 yr of age following a 1-yr low-intensity resistance training program when compared with a nonexercising control group. Group assignment was not randomized; however, none of the subjects had previously participated in a resistance training program. In addition, this trial was one of four longitudinal investigations that included calcium supplementation of 500 mg·d−1 in both the experimental and control groups (17,19,21,25).
Conversely, resistance training has been reported to have either no effect or a negative impact on bone in two studies in premenopausal women (28,34). Vuori et al. (34) found that unilateral resistance training did not have significant impact on BMD or BMC in physically active young women except at the patella. However, there was a trend towards increased BMD and BMC at several sites in the trained limb. In another study (28), lumbar spine BMD decreased in an exercise group completing an intensive weight training regimen and remained unchanged in the control group. This study is difficult to interpret because of a nonrandomized design and baseline physical differences between the women in the control and resistance training groups. The women in the control group had greater body weight and body fat, which is typically associated with higher BMD, when compared with the resistance trained women who had lower body weight.
The effects of resistance training and bone density have also been reported in older populations (19,20,22,24,25). A commonality of these studies is a moderate- to high-intensity resistance training protocol and significant gains in strength. Our laboratory has completed a 1-yr randomized controlled trial of high-intensity resistance training in postmenopausal women (20). The results of the study demonstrated that women in a 2 d·wk−1 resistance training program gained an average of 1% in BMD of the femoral neck and lumbar spine whereas the control group lost 2.5% and 1.8% at these sites, respectively. In addition, the resistance-trained women tended to maintain TBBMC of the skeleton whereas the women in the control group had a 1.2% decline in TBBMC. Furthermore, the resistance-trained women had a 35-76% increase strength, 14% improvement in dynamic balance, and a 1.2-kg increase in total body muscle mass and a 27% increase in physical activity unrelated to the intervention whereas the control group showed declines in all of these parameters. The overall findings of our study indicate that resistance training in postmenopausal women can decrease the risk for osteoporosis by simultaneously influencing multiple risk factors for osteoporotic fractures.
In a study of surgically postmenopausal women receiving estrogen replacement therapy, Notelovitz et al. (22) found that a resistance training group increased their bone density at multiple sites, whereas the control group maintained their bone density. This study clearly demonstrates the benefits of resistance training on the skeleton and has important implications for women receiving only hormone replacement therapy to improve bone density.
Strength training has also been shown to be an effective osteogenic agent for glucocorticoid-induced bone loss. Braith and colleagues reported that the significant decrease in lumbar spine BMD secondary to heart transplant surgery and antirejection drug therapy can be mitigated by postoperative strength training in middle-aged male patients (1). In a prospective randomized controlled trial, eight patients who participated in resistance training were able to recapture almost all of their presurgical total body, femoral neck, and lumbar spine BMD as measured by dual energy x-ray absorptiometry whereas eight male transplant recipients in the control group continued to lose bone (1). These results suggest that resistance training exercise may be an effective strategy for preventing secondary bone loss due to other medical conditions.
In contrast to the postoperative population, Nichols et al. (21) investigated the impact of a high-intensity resistance training program on healthy, very active older women, previously exercising at least three times a week for the 6 months before the study, and reported that resistance training had no significant effect on BMD. However, the pretraining hip BMD of these women was very high, 105% of aged reported norms, possibly influenced by their previous exercise participation, and was unlikely to show additional gains (21). Also of interest, calcium intake varied initially between subjects and was normalized at 800 mg·d−1 through dietary counseling or supplementation (21). In another study of elderly males and females performing a 42 wk high-intensity resistance training program, no change was seen in BMD; however, other results from this study were highly significant and may be attributed to the resistance training program (18). The resistance-trained group showed great increases in strength, maximum cycle ergometry test, treadmill endurance, and stair climbing test, which have a direct impact on quality of life for these older individuals and which may decrease the risk for osteoporotic fractures.
In another recent study, Pruitt et al. (25) also reported no significant differences in lumbar spine or total hip BMD as a result of either high-intensity resistance training, low-intensity resistance training, or a control group of woman aged 65-70 yr. However, these subject had higher than average baseline spinal BMD, ranging from 107% to 126% of aged-matched normative values, in a similar manner as the subjects in the study reported by Nichols et al (21). In addition, the majority of the woman in the resistance training groups had been taking hormone replacement therapy for at least 1 yr before the enrollment in the study and were taking a calcium and or vitamin D supplement. As noted by the investigators, the combination of these factors indicate a relatively low risk of accelerated bone loss and compromised skeletal status.
Three studies involving less intense resistance training programs have also found that resistance training has a positive impact on bone through either maintenance or formation in postmenopausal women (26,27,29). However, it has not been shown that low-intensity or home-based resistance training is an effective stimulator of bone formation in women by several others investigators (3,23,30).
The research completed to date indicates that resistance training is positively associated with high BMD in both young and older adults and that the effect of resistive exercise is relatively site specific to the working muscles and the bones to which they attach (1,4,5,11,13-16,19,20,22,24,26,27,29,31,32,34). Although aerobic exercise and weight bearing physical activity are important in maintaining overall health and healthy bone, resistance training exercise seems to have a more potent impact on bone density (12). The positive effect on bone is most convincingly demonstrated by randomized, controlled trials using a high-intensity resistance training protocols. This indicates that progressive resistance training may have significant clinical application as a prevention and treatment for osteoporosis and other degenerative bone diseases in a wide range of individuals. Resistance training may help to achieve the highest possible peak bone mass in premenopausal woman and may aid in maintaining or increasing bone in postmenopausal women. The frail elderly may also benefit from progressive resistance training to help preserve bone density in addition to increasing muscular strength and potentially improving agility and balance. There are many interesting directions for future research in this area. There is certainly a need for additional randomized controlled trials of progressive resistance training possibly in conjunction with other novel exercise modalities and calcium and vitamin D supplementation (6). Furthermore, the potential mechanisms responsible for the positive changes in bone due to these interventions warrants further investigation.
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OSTEOPOROSIS; FRACTURES; WEIGHT BEARING; EXERCISE; AGING
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