Update 2010
Selections from thesis published 1997
DISCUSSION OF SELECTED LITERATURE
Introduction
Fitness includes all muscles and bones, and much more, located inside your skin. Contrary to popular media-induced opinion, physical fitness has little to do with squeezing your body into attractive and revealing exercise garments. It is about the apparatus inside of your skin. Bones are the framework that gives shape to your body. The total amount of bone in your body is known as bone mass. Bone mass, bone density, and bone strength are all ways of describing your bone architecture. Bone material, tightly crowded into bone formation, is known as bone density or strength. Strength determines how strongly your bones resist breaking.
Your bones are busy throughout life. New bone is formed; old bone is withdrawn. Eventually less new bone is formed but old bone continues to be withdrawn. So, like a bank account with more withdrawals than deposits, the bones become less dense.
Bone density is measured in grams per centimeter. In general, greater than one gram per centimeter is considered healthy for spine or femur. (See author note after references.)
As bones become more fragile, the spine, hip, and forearm are most susceptible to fracture. Recent research focusing on exercise to maintain bone density is discussed in the following paragraphs.
Exercise
Kohrt et al (2004), for the American College of Sports Medicine, prepared a position stand declaring that weight-bearing physical activity has beneficial effects on bone health across the age spectrum. The position stand includes separate exercise prescriptions likely to promote bone health of children and adolescents, young healthy individuals, and middle age and older adults.
The stages of life and bone health are first a time of bone accrual, then bone maintenance, and finally attenuating or preventing the removal of bone tissue by resporption. At various life stages, different exercise patterns are suggested for enhancing bone mineral density (BMD). BMD is estimated to account for 60% or more of variance in bone strength.
Children and adolescents can use high-intensity loading and high-intensity resistance training to augment bone mineral accrual.
In adults, focused activity is expected to maintain bone mass; however when the activity is discontinued, the benefits are not preserved. The recommendation to preserve bone health in adults uses weight bearing, endurance, and weight lifting activity.
Finally, as stated in the position stand, “Even the frailest elderly should be as physically active as health permits to preserve skeletal integrity.” This meta-analysis of published studies substantiated that a variety of types of exercise can be effective in preserving bone mass of older adults. Chronically inactive elderly individuals are more than twice as likely to fracture a hip.
Walking without sufficient high intensity loading is only moderately effective in preserving bone mass. It is well known that weightlessness at any age, such as bed rest or space flight, induces rapid and profound bone loss.
Greendale et al. (2003) obtained baseline data from the study of Women’s Health Across the Nation for over 3,000 female participants aged 42-52 years and of African-American, Caucasian, Chinese, Hispanic, and Japanese ancestry in seven cities in the United States. Activity, food intake, and other data were obtained by recall questionnaire. The values between ethnicities were substantially similar. Researchers studied the relationship of the sport, home, work, and active living domains of physical activity of these women.
They found that higher sport activity was statistically significantly associated with greater bone mineral density at the lumbar spine, femoral neck, and total hip, and more home physical activity was associated with greater bone mineral density at the spine and femoral neck. The finding that home physical activity benefits bone suggests that nonrecreational activity may be important to bone maintenance for women. Neither work physical activity nor active living related to bone mineral density at any bone site.
Muscle force
Robling (2009) arrives at the tentative conclusion that muscle forces contribute the most effective mechanism to determine whole-bone strength. It is accepted that bone adapts to mechanical demands. A clear delineation of the most effective type of demands has potentially therapeutic value. Robling (2009) states the obvious that new therapies and exercise-related approaches to bone health can be streamlined to account for discoveries. His brief survey revealed a consistent and significantly positive association between muscle strength and mass and bone mass.
In sub-adult tennis players, muscle and bone mass in the playing arm is significantly increased over the non-playing arm. However, additional analyses show a statistically significant side-to-side difference (20%) in bone rigidity. He reports that others have found that in disease states, bone mass is typically not over-adapted for muscle mass. When the size of muscle lessens, so does the bone, but the reverse does not occur.
Robling concludes that muscle forces are capable of providing a sufficient stimulus to drive bone adaptation, and do normally provide a significant amount of force. It is likely that the origin of primary mechanical stimulus is less important then the overall stimulus. Mechanical signals must be of enough magnitude, imposed at significant rates and dynamics for bone adaptation to occur.
Judex and Carlson (2009) reviewed literature on the inherent relationship between the effect of gravity and muscle forces as signals to bone. Gravity may have a major role in affecting weight-bearing bone. These researchers found that muscle loading is likely not the predominant stimulus for bone mass change, primarily because it is not true in both increasing and decreasing bone mass. If muscle activity were the primary stimulus for bone mass change, there would be a close association between loss of muscle and loss of bone tissue. Muscle loss continues for approximately 1.5 years after paraplegia, yet bone loss continues for several additional years.
The discussion and investigations continue as to whether muscle forces or gravity or other causes are a prime stimulus for bone formation. The source may be less important than the force of the stimulus.
Rest Between Training Loads
Sirinivasin et al (2002) report finding that in animal models the insertion of 10 seconds of rest between each moderate weight loading led to 10 times the bone formation as in the same consistent moderate weight loading without rest intervals. They theorize that important fluid flow at the osteocytes during the rest period augments osteogenic potential of low-magnitude loading. If additional research supports this analysis, it could positively impact exercise prescriptions for older adults who could sustain sufficient bone loading to attain stable or increasing bone mass.
An unpublished small pilot study employing yoga postures and sufficient time for each pose appeared to indicate that bone-forming proteins seemed to synthesize well after 10 seconds of stimulating pressure. It is already incorporated into certain physical routines suggested in publicly available formats for attenuating or reversing bone loss. A larger study is on-going.
Resistance training
A quantitative review of 56 studies by Spence and Humphries (2002) indicated that the effect of resistance training (weight lifting) on bone strength was significant but small at L2-L4 spine, femoral neck, and total body. Interestingly, the review showed larger increases in bone density in postmenopausal women than in premenopausal women. The reviewers concluded that due to small increases in bone strength in women of all ages, resistance training alone may not be the most effective way to promote bone growth or slow bone loss.
Energy imbalance
The related components of disordered eating, ovarian suppression, and osteoporosis often occur in women involved in sports that emphasize a low body mass. Marked weight loss is often accompanied by significant reduction of bone mass. Energy deficit elicits a cascade of endocrine-metabolic aberrations.
The opposite is energy excess. Increases in spinal bone mineral density (BMD) may occur with weight gain in women. In anorexic women, refeeding accompanies increase in bone formation markers and gradual reduction of bone resorption markers, even before significant weight gain.
In a review to examine the possible link between energy balance and bone turnover, Zanker and Cooke (2004) found evidence of a relationship between reduced bone formation and an abrupt short-term energy deficit.
Any individual, of either sex, may be at risk of skeletal problems if their energy demands are not balanced with appropriate nutrition for the energy demands of their activity. Bone turnover culminating in a reduced bone mass, whether during growth or maturity, is described as “skeletal problems”.
During the 1980s and 1990s evidence accumulated that it is an energy deficit, rather than exercise specifically, that is responsible for the BMD dysfunction of some active women. The reviewers also evaluated the evidence that underlies the hypothesis that an energy deficit is instrumental in the disturbance of bone turnover observed in physically active men.
Zanker and Cooke (2004) concluded that exercise-associated imbalances of bone remodeling are linked to an energy deficit, and they pose a serious threat to long-term health because the capacity to regain lost bone and to increase BMD in adulthood may be limited, the prevention of these imbalances is of paramount importance.
Body Fat & Bone Strength Relationship
Studies have found a complex relationship between body fat and bone strength as determined by BMD or BMC. Zhao et al (2007) found several variations in their review. Possibly greater fat mass imposes greater load on bone causing increases in bone to accommodate the demand. Researchers have found that fat tissue secretes biologically active molecules as well as storing energy. These molecules may be involved in bone metabolism. Some studies support the concept that insulin may be a regulator of bone metabolism; other studies indicate that insulin may contribute to the bone protective effects of obesity. Observations by other researchers are interpreted to show that the effect of fat on bone may be site-specific. The relationship of fat mass to bone activity and bone strength indicates need for substantial additional research.
Resistance Training Effectiveness
Cussler et al. (2003) examined the relationship between weight lifted in progressive training and the change in bone mineral density (BMD) as part of the Bone Estrogen Strength Training (BEST) study. One hundred forty calcium-replete women, ages 44 to 66 years, 50% of them on hormone replacement therapy, participated in the randomized, one year trial. The purpose of the study was to define more precisely the type and amount of exercise needed to stimulate bone formation. Earlier animal studies indicated there may be a linear relationship of weight lifted to bone change. Subjects were recruited by direct mail according to zip code, medical clinics, community organizations, and media advertisement. Telephone screenings were followed by small group meetings. Inclusion criteria included body mass index greater than 19.0 and less than 32.9, nonsmoking, and no history of osteoporotic fracture. At baseline, standing height and weight were measured. Regional and total body BMD were measured by dual energy x-ray absorptiometry.
The subjects randomized to the exercise intervention were asked to train 3 days each week, on non-consecutive days. Sessions lasted 60-75 minutes and included stretching, balance, and weight-bearing activities for warmup, weightlifting, an additional weight-bearing circuit of moderate impact activities and stair-climbing/step boxes with weighted vests. Three times weekly they performed 2 sets of 6 to 8 repetitions, at 70-80% of l-RM, in eight core exercises focused on major muscle groups. Trainers coached women to perform 4-second extensions and equally long releases. Muscle strength was measured every two months and weights were increased to maintain loads of 70-80% of 1-RM. At both baseline and end of study, two measurements of BMD were taken approximately one week apart. This study found an increase in femur trochanter (FT) BMD that was positively related to total weight lifted after adjusting for age, baseline factors, hormone replacement therapy status, weight change, cohort, and fitness. Weighted squats showed the strongest gain, while back extension showed the weakest. Weight lifted in weighted march significantly related to total BMD. No significant relationship was found between weight lifted and BMD in the femur neck or lumbar spine. There was evidence of linear relationship between BMD and total and exercise specific that reinforces the positive association in postmenopausal women. The researchers noted that because performance in one exercise may depend on success in others, a well-balanced strength-training program provides the most sensible approach to an osteoporosis prevention program A one-year study, as this was, is often sufficient to indicate probable trends; however, a longer study with a larger number of participants would be useful.
A later study known as the Strong Healthy Empowered (SHE) group, performed by Warren et al. (2008), followed the published guidelines of US Department of Health and Human Services on BMC and areal bone mineral content (aBMC) in the proximal femur and lumbar spine in premenopausal women. One hundred forty overweight, sedentary women aged 25-44 were randomized to progressive strength training or standard care for two years. The exercise group participated in a twice-weekly strength training program.
The researchers concluded that strength training had no effect on BMD after two years of training. Femoral neck BMC decreased 1.5% in the standard care group and remained unchanged in the strength training group. They mention that there is a lack of consensus in randomized studies and a lack of consistency between cross-sectional studies and randomized trials. Direct comparisons are difficult due to differing research designs.
Summary
Research results and reviews discuss many affectors of bone mineral density. Exercise, muscle force, rest between training loads, resistance training, energy imbalance, amount of body fat, and various training loads have each been shown to affect bone strength to some degree. Some are more effective; some are marginally effective. None have been shown to be the one superior method of building bone after it has been resorbed.
REFERENCES
Cussler, E. C., Lohman, T. G., Going, S. B., Houtkooper, L. B., Metcalfe, L. L., Flint-Wagner, H. G., Harris, R. B., Teixeira, P. J. (2003). Weight lifted in strength training predicts bone change in postmenopausal women. Medicine and Science in Sports and Exercise, 35, 1, 10-17.
Judex, S., & Carlson, K. J. (2009). Is bone’s response to mechanical signals dominated by gravitational loading? Medicine and Science in Sports and Exercise, 41, 11, 2037-2043.
Kohrt, W. M.,
Robling, A. G., (2009). Is bone’s response to mechanical signals dominated by muscle forces? Medicine and Science in Sports and Exercise, 41, 11, 2044-2049.
Spence, J. C., Humphries, B. (2002). The effect of resistance training on bone strength in women: a quantitative review. Medicine and Science in Sports and Exercise, 34, 5, p S 109.
Srinivasan, S., Weimer, D. A., Agans, S. C., Bain, S. D., Gross, T. S. (2002). Low-magnitude mechanical loading becomes osteogenic when rest is inserted between each load cycle. Journal of Bone Mineral Research, 17, 9, 1613-1620.
Warren, M., Petit, M. A., Hannan, P. J., Schmitz, K. H. (2008). Strength training effects on bone mineral content and density in premenopausal women. Medicine and Science in Sports and Exercise, 40, 7, 1282-1288.
Zanker, C. L., & Cooke, C. B, (2004). Energy balance, bone turnover, and skeletal health in physically active individuals. Medicine and Science in Sports and Exercise, 36, 8, 1372-1381.
Zhao, L., Jiang, H., Papasian, C. J., Maulik, D., Drees, B., Hamilton, J., Deng, J. (2007). Review. Correlation of obesity and osteoporosis: effect of fat mass on the determination of osteoporosis. Published online September 3, 2007. Journal of Bone and Mineral Research, 23, 1, (2008).
Author comment: Bone density measured in ”grams per centimeter squared” as reported in research literature is the average value of pixels (g.cm2) within the defined region that exceed a defined threshold (to exclude nonbone pixels.) Beck, Thomas J. et al. Medicine and Science in Sports and Exercise, 43, 1, pg 85.
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