Men with low bone mass are much less likely than their female counterparts to receive treatment. But research suggests that resistance exercise is a safe and effective way to improve bone mineral density in men and, in turn, reduce the risk of fracture and related complications.
By Pamela S. Hinton, PhD
Osteoporosis, which is defined1 as “low bone mass and micro-architectural deterioration of bone tissue, leading to enhanced bone fragility and a consequent increase in fracture risk,” currently affects more than 200 million people worldwide.2 The World Health Organization defines osteoporosis as a bone mineral density (BMD) that is two and a half standard deviations (SD) or more below the average value for a young adult (T-score < -2.5).3 Osteopenia is characterized as low bone mass, and is defined as a BMD that is between one and two and a half SDs below the young adult mean (T-score between -1 and -2.5).3
Low BMD is associated with increased risk of nontraumatic fracture; fracture risk is increased 1.5 to three-fold or greater for each SD decrease in BMD.4 Each year, more than 4.5 million people in the US and Europe will suffer a fragility fracture.3 Due to the growth of the aging population and the rise in life expectancy in recent years, the incidence of osteoporosis and related fracture is expected to increase.5
Osteoporosis affects men
Osteoporosis affects more than two million men in the US, and nearly 16 million more have low bone mass.6 Men account for approximately 40% of the nine million new osteoporotic fractures that occur annually,7 and the lifetime fracture risk in men aged 60 years and older is estimated to be as high as 25%.8 Compared with women, men have a significantly greater risk for complications after a hip fracture, including increased morbidity, mortality, loss of independence, and rate of institutionalization,9,10 yet treatment rates are much lower in men than in women.11
Recent estimates from the National Osteoporosis Foundation guidelines indicate that one third of white men older than 65 years, and more than half older than 75 years, should be recommended pharmacologic treatment for osteoporosis.12 Yet, even after suffering an osteoporosis-related fracture, more than 90% of men remain undiagnosed and untreated.13,14 Postfracture, men are less likely than women to receive follow-up care,15 including calcium and vitamin D supplementation16 and prescription of antiresorptive pharmacotherapy.11
Physical inactivity is a modifiable risk factor for osteoporosis, and increasing physical activity at any point throughout the lifespan positively affects bone health,17-22 while reductions in physical activity can result in bone loss.23,24 Cross-sectional and longitudinal studies have shown the skeletal benefits of physical activity during adolescence and young adulthood persist into middle age and older adulthood.25,26 In addition to increasing BMD, bone loading during adulthood increases bone size, cortical area, and strength,27 and reduces hip fracture risk later in life.20
Exercise can affect bone through multiple mechanisms, including muscle contraction forces, gravitational loading, and endocrine/paracrine effects. During physical activity, bone is subjected to mechanical forces exerted by muscle contraction and gravitational loading. At the cellular level, bone cells (osteocytes) perceive these mechanical forces as cell deformation, changes in extracellular fluid shear stress, pressure gradients, and electric fields.28 The osteocytes communicate with osteoblasts and osteoclasts to modulate bone formation and resorption, thereby changing the bone’s geometry and material properties.29
It is well accepted that bone adapts to the mechanical demands to which it is subjected, and muscle contractions contribute a portion of those demands.30,31 The importance of skeletal muscle contraction forces (ie, joint reaction forces) to bone mass is supported by the parallel changes in bone mass and muscle strength throughout the lifespan.30,32 Similarly, in states of muscular disuse that result in muscle atrophy (eg, disease, inactivity, or paralysis), muscle contraction forces are severely reduced, and site-specific reductions in bone mass and bone strength occur.31
Site-specific relationships between skeletal muscle mass and BMD demonstrate the importance of muscle contraction to the preservation of bone mass. Studies of tennis players demonstrate that a player’s dominant arm has greater muscle and bone mass than their nondominant arm.32 In the lower extremity, the bones of the nondominant limb have greater bone density due to greater motor neuron excitability and activity of stabilizing muscles of the nondominant side.33 Cross-sectional studies have shown positive site-specific associations between repetitive muscle contraction and regional BMD, such that resistance training of the upper body is associated with greater BMD of the arms.34 Likewise, changes in skeletal mass following strength training are positively associated with changes in BMD.35 Thus, there is considerable evidence that muscle contraction forces are important for bone strength.
The American College of Sports Medicine recommends weightbearing endurance activities, including those that involve jumping and jogging, three to five times per week, and resistance exercise two to three times per week to preserve bone health during adulthood.36 Resistance training is also recommended by the National Strength and Conditioning Association to increase BMD or to prevent age-associated reductions in BMD.37 The Surgeon General’s Report on Bone Health also recommends progressive resistance training, as well as daily jump-training and participation in weightbearing recreational activities for individuals who can tolerate high-impact activity.1
The majority of clinical trials of resistance training have been conducted in women. Exercise that exerts high muscle-contraction or ground-reaction forces on the skeleton, such as high-intensity resistance training or structured jump-training, respectively, is associated with increased BMD in pre- and postmenopausal women.38-40 However, very few controlled trials have examined the effects of resistance training on bone mass in men.22,41-48
Generally, these studies reported positive effects of resistance training on BMD. Kukuljan et al found that 12 months of progressive resistance training and impact exercise (three days per week) was associated with increased BMD at the femoral neck and lumbar spine by 1.8% and 1.5%, respectively, in men aged 50 to 79 years with normal to below-average BMD at baseline.42 Whole-body BMD increased by about 1.2% after 12 weeks of resistance training in elderly men and in women with an average age of about 60 years.48 Ryan et al also reported a 2.8% increase in femoral neck BMD after four months of resistance training in men with an average age around 60 years,46 and Menkes et al observed significant increases in lumbar spine (2%) and femoral neck (3.8%) BMD in men aged 55 to 60 years.45 In a study of men and women aged 55 to 74 years, some of whom were osteopenic or osteoporotic, Bemben et al found that 40 weeks of resistance training significantly increased BMD of the spine, trochanter, and total hip by ≤1%.41 However, because these studies included men and women, elderly men, or a mixed study population of men who had either normal or low BMD, or because the intervention included a combined exercise protocol (ie, resistance training plus high-impact activity), the effectiveness of resistance training for increasing BMD in men with existing low bone mass could not be determined.
To answer this clinically relevant question, we conducted a clinical trial to determine the effects of 12 months of periodic progressive resistance training on BMD in apparently healthy men (mean age, 44 ± 2 years; median age, 44 years) with osteopenia of the hip or spine.49 This study was conducted in accordance with the Declaration of Helsinki and was approved by the local Institutional Review Board. Informed written consent was obtained from each study participant.
Apparently, healthy physically active (four or more hours of leisure time physical activity/week for the past 24 months) men aged 25 to 60 years with low BMD of the lumbar spine or hip (T-score between -2.5 and -1 SD) were eligible to participate in the study. Exclusion criteria: use of medications or supplements that affect bone metabolism or prevent exercise; a previous or current medical condition affecting bone health; osteoporosis of the lumbar spine and/or hip (T-score < -2.5 SD); cardiovascular disease; metal implants; current smoker (ie, within the past six months); current regular participation in high-intensity resistance training and/or plyometrics; reversed sleep/wake cycle (ie, sleep during the day and work at night); and consumption of more than three alcoholic drinks per day.
The participants completed two resistance training sessions per week under the supervision of study personnel. The resistance training intervention included exercises that load the hip and spine: squats, bent-over-row, modified dead lift, military press, lunges, and calf raises. Participants were instructed to perform the eccentric phase of each lift in two to three seconds and to perform the concentric contraction “explosively.” Prior to and every six weeks during the intervention, we performed maximal strength testing.50
To minimize risk of injury and to account for strength adaptations as a result of strength training improvements, the intervention also used a progressive intensity design based on a six-week cycle followed by a rest week; a total of eight cycles were completed. During the six-week cycle, the intensity progressively increased every two weeks based on the strength measured at the end of each cycle.
- Weeks one to two were light intensity, consisting of one warm-up set of 10 repetitions at 20% of the 1-repetition maximum (1RM) and three sets of 10 repetitions at 50% of the 1RM.
- Weeks three and four were moderate intensity, with one warm-up set of 10 repetitions at 20% of the 1RM, two sets of 10 repetitions at 60% of the 1RM, and one set of six to eight repetitions at 70% to 75% of the 1RM.
- Weeks five to six were high intensity, starting with one warm-up set of 10 repetitions at 20% of the 1RM, followed by two sets of 10 repetitions at 60% of the 1RM, and one set of three to five repetitions at 80% to 90% of the 1RM.
At the end of the 12-month intervention, participants significantly improved their muscular strength, as evidenced by increases in 1RM for the squat, lunge, modified deadlift, calf raise, military press, and bent-over row of 79%, 114%, 64%, 79%, 52%, and 44%, respectively. Bone mineral density of the whole body, total hip, and lumbar spine, which was measured using dual-energy X-ray absorptiometry, also significantly increased after 12 months of resistance training. There was a positive relationship between percent changes in squat 1RM and in left leg BMD (r = .605, p= .042). The increases in BMD observed in the present study were associated with favorable alterations in serum bone turnover markers; specifically, there was a significant reduction in bone resorption and an increase in bone formation.
Biological and clinical significance
The biological and clinical significance of these results can be appreciated only if one considers that bone loss occurs with normal aging. Young adult and middle-aged men lose BMD at rates of about .4% to 1.5% per year.51-53 The results are also important because they suggest that a time-efficient (two to three days per week) resistance training intervention can improve BMD in otherwise healthy men. We previously observed that physically active adult men with osteopenia, similar to those in the present study, lost hip BMD at a rate of .8% per year,54 consistent with the literature consensus that bone loss occurs with aging. Therefore, the increases in BMD observed in this and previous exercise-intervention studies, though relatively small (.6% to 1.3%), are biologically significant, in that exercise reversed the bone loss that occurs with normal aging.
The increases in BMD observed following exercise interventions likely have clinical significance, as small increases in BMD result in much larger gains in bone strength. For example, increasing BMD by 5% increased bone strength by 65% in an animal model,55 and, in women with postmenopausal osteoporosis, a 1% increase in spine BMD reduced fracture risk by 8%.56 Similar to the increase in bone formation and decrease in bone resorption observed in our study, others have reported increases in bone formation markers relative to resorption following high-intensity resistance training in older men.47,57,58 These data suggest exercise might counteract age-related bone loss in men, which has been attributed primarily to a deficit in bone formation relative to bone resorption.59
Feasibility of resistance training
From a practical perspective, it is worth noting that, in our study, the time and equipment required to complete the resistance training each week was minimal, ranging from 60 minutes during a “light” week to 120 minutes for a “heavy” week. If participants missed a session, they were required to make it up. While the training in our study was supervised, it could be done at home without supervision.
These observations, coupled with evidence of long-term compliance with voluntary unsupervised high-impact exercise interventions in premenopausal women,60 suggests exercise-based interventions might be effective in the real world.
This conclusion is strengthened when one considers the alternative of pharmacologic treatment. Although antiresorptive medications are a Food and Drug Administration-approved treatment for osteoporosis in men,61 less than 10% of men with osteoporotic fractures are treated with bisphosphonates. Enthusiasm for use of these medications in men appears to be limited by the relative lack of long-term safety and efficacy studies in men, the especially poor treatment compliance in men,62 and data suggesting poor cost-effectiveness of bisphosphonate treatment in men.63 Drug treatments for osteoporosis have low rates of compliance and persistence, and most patients who stop taking their osteoporosis medication do not restart.64
To evaluate safety of the resistance training intervention, we assessed the self-reported pain and fatigue associated with the exercise at each training session. On average, the participants rated the intensity of the pain caused by the training as a score of 10 or less out of 100, with 100 being the most intense pain imaginable. In addition, the pain ratings decreased from the baseline assessment at six and 12 months. Participants also rated fatigue associated with the interventions as less than 30 out of 100, with 100 being the most fatigue imaginable, at all time points. In addition, there were no injuries reported during any of the approximately 1800 supervised training sessions.
Thus, the resistance training was well tolerated by the participants and appears to have a minimal risk of injury or discomfort, which predicts both good compliance and practical application. Other studies have reported that older adults with low bone mass can safely perform maximal strength training (squats)65 or jumping.66,67 Moreover, a recent review by a panel of experts strongly recommends multicomponent exercise that includes resistance training for individuals with osteoporosis. Osteoporosis Canada, the National Osteoporosis Foundation, and Osteoporosis Australia’s Medical and Scientific Advisory Committee endorsed the recommendation that individuals with osteoporosis engage in resistance training that targets all major muscle groups at least twice per week.68
In summary, the existing evidence suggests that resistance training interventions are safe and effectively increase BMD in men with low bone mass. These results have clinical implications, as exercise may be the appropriate “prescription” for some individuals with low bone mass.
Pamela S. Hinton, PhD, earned in her doctorate in nutrition sciences from the University of Wisconsin-Madison and is currently an associate professor in the Department of Nutrition & Exercise Physiology at the University of Missouri-Columbia.
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