Influence of physical activity on the regulation of bone density

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Whalen, R. T.^1,2; Carter, D. R.^1,2; Steele, C. R.²

Influence of physical activity on the regulation of bone density

J Biomech. 1988;21(10):825-837

Affiliations

¹Rehabilitation Research and Development Center, Veterans Administration Medical Center, Palo Alto, CA, U.S.A.

²Department of Mechanical Engineering, Design Division, Stanford University, Stanford, CA, U.S.A.
Abstract

Using a mathematical model which relates bone density to daily stress histories, the influence of physical activities on the apparent density of the calcaneal cancellous bone was investigated. Assuming that the mechanical bone maintenance stimulus is constant for all bone tissue, bone apparent density was calculated by a linear superposition of the mechanical stimulus provided by different daily physical activities. An empirical weighting factor, m, accounted for possible differences in the relative importance of load magnitude and number of cycles in each activity. By considering hypothetical variations in body weight and occupational activity levels, the range of probable m values was established. The model was then applied to the results of two previous running studies in which calcaneal density was measured to obtain an estimate of the stress exponent parameter, m. The results indicate that stress magnitudes (or joint forces) have a greater influence on bone mass than the number of loading cycles. We demonstrate that by carefully considering the magnitudes of imposed skeletal forces and the number of loading cycles, it may be possible to design exercise programs to achieve predictable changes in bone mass.
Links

DOI: 10.1016/0021-9290(88)90015-2

PubMed: 3225269

WoS: A1988Q581200005
History

Received: 1986-10-08

Revised: 1987-10-26

Cited Works (23)

Year	Entry
1980	Mann RA, Hagy J. Biomechanics of walking, running, and sprinting. Am J Sports Med. September 1980;8(5):345-350.
1972	Chamay A, Tschantz P. Mechanical influences in bone remodeling: experimental research on Wolff's law. J Biomech. March 1972;5(2):173-180.
1977	Andriacchi TP, Ogle IJA, Galante JO. Walking speed as a basis for normal and abnormal gait measurements. J Biomech. 1977;10(4):261-268.
1985	Dickinson JA, Cook SD, Leinhardt TM. The measurement of shock waves following heel strike while running. J Biomech. 1985;18(6):415-422.
1984	Röhrle H, Scholten R, Sigolotto C, Sollbach W, Kellner H. Joint forces in the human pelvis-leg skeleton during walking. J Biomech. 1984;17(6):409-424.
1981	Woo SL-Y. The relationships of changes in stress levels on long bone remodeling. In: Cowin SC, ed. Mechanical Properties of Bone. The Joint ASME-ASCE Applied Mechnics, Fluids Engineering and Bioengineering Conference; June 22-24, 1981; Boulder, CO. New York, NY: American Society of Mechical Engineers; 1981:107-129.
1981	Woo SL-Y, Kuei SC, Amiel D, Gomez MA, Hayes WC, White FC, Akeson WH. The effect of prolonged physical training on the properties of long bone: a study of Wolff's Law. J Bone Joint Surg. June 1981;63A(5):780-787.
1964	Wright DG, Desai SM, Henderson WH. Action of the subtalar and ankle-joint complex during the stance phase of walking. J Bone Joint Surg. March 1964;46A(2):361-382.
1985	McBroom RJ, Hayes WC, Edwards WT, Goldberg RP, White AA III. Prediction of vertebral body compressive fracture using quantitative computed tomography. J Bone Joint Surg. 1985;67A(8):1206-1214.
1976	Cappozzo A, Figura F, Marchetti M, Pedotti A. The interplay of muscular and external forces in human ambulation. J Biomech. 1976;9(1):35-43.
1984	Lanyon LE, Rubin CT. Static vs dynamic loads as an influence on bone remodelling. J Biomech. 1984;17(12):897-905.
1975	Cappozzo A, Leo T, Pedotti A. A general computing method for the analysis of human locomotion. J Biomech. September 1975;8(5):307-320.
1980	Gordon D, Winter DA. Mechanical energy generation, absorption and transfer amongst segments during walking. J Biomech. 1980;13(10):845-854.
1985	Rubin CT, Lanyon LE. Regulation of bone mass by mechanical strain magnitude. Calcif Tiss Int. 1985;37(4):411-417.
1984	Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg. March 1984;66A(3):397-402.
1987	Carter DR, Fyhrie DP, Whalen RT. Trabecular bone density and loading history: regulation of connective tissue biology by mechanical energy. J Biomech. 1987;20(8):785-794.
1984	Carter DR. Mechanical loading histories and cortical bone remodeling. Calcif Tiss Int. March 1984;36(suppl 1):S19-S24.
1980	Cavanagh PR, Lafortune MA. Ground reaction forces in distance running. J Biomech. 1980;13(5):397-406.
1980	Light LH, McLellan GE, Klenerman L. Skeletal transients on heel strike in normal walking with different footwear. J Biomech. 1980;13(6):477-480.
1977	Jones HH, Priest JD, Hayes WC, Tichenor CC, Nagel DA. Humeral hypertrophy in response to exercise. J Bone Joint Surg. March 1977;59A(2):204-208.
1970	Donaldson CL, Hulley SB, Vogel JM, Hattner RS, Bayers JH, McMillan DE. Effect of prolonged bed rest on bone mineral. Metabolism. December 1970;19(12):1071-1084.
1981	Hayes WC, Snyder B. Toward a quantitative formulation of Wolff's Law in trabecular bone. In: Cowin SC, ed. Mechanical Properties of Bone. The Joint ASME-ASCE Applied Mechnics, Fluids Engineering and Bioengineering Conference; June 22-24, 1981; Boulder, CO. New York, NY: American Society of Mechical Engineers; 1981:43-68.
1983	Winter DA. Moments of force and mechanical power in jogging. J Biomech. 1983;16(1):91-97.

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Year	Entry
2011	Rantalainen T, Kłodowski A. Estimating lower limb skeletal loading. In: Klika V, ed. Theoretical Biomechanics. InTech; 2011:243-266.
1990	Carter DR, Wong M. Mechanical stresses in joint morphogenesis and maintenance. In: Mow VC, Ratcliffe A, Woo SL-Y, eds. Biomechanics of Diarthrodial Joints. Vol 2. New York, NY: Springer-Verlag; 1990:155-174.
1998	Martin RB, Burr DB, Sharkey NA. Skeletal Tissue Mechanics. New York, NY: Springer-Verlag; 1998.
1990	Wong M, Carter DR. A theoretical model of endochondral ossification and bone architectural construction in long bone ontogeny. Anat Embryol. July 1990;181(6):523-532.
1994	Frost HM. Wolff's law and bone's structural adaptations to mechanical usage: an overview for clinicians. Angle Orthod. June 1994;64(3):175-188.
1991	Bertram JEA, Swartz SM. The “law of bone transformation”: a case of crying Wolff? Biol Rev. August 1991;66(3):245-273.
1993	van der Meulen MCH, Beaupré GS, Carter DR. Mechanobiologic influences in long bone cross-sectional growth. Bone. July–August 1993;14(4):635-642.
1996	Carter DR, Van der Meulen MCH, Beaupré GS. Mechanical factors in bone growth and development. Bone. January 1996;18(1)(suppl 1):S5-S10.
1993	Forwood MR, Burr DB. Physical activity and bone mass: exercises in futility? Bone Miner. May 1993;21(2):89-112.
2001	Garcia JM, Martínez MA, Doblaré M. An anisotropic internal-external bone adaptation model based on a combination of CAO and continuum damage mechanics technologies. Comput Methods Biomech Biomed Eng. 2001;4(4):355-377.
2019	Georgiou L, Kivell TL, Pahr DH, Buck LT, Skinner MM. Trabecular architecture of the great ape and human femoral head. J Anat. May 2019;234(5):679-693.
1990	Orr TE, Beaupré GS, Carter DR, Schurman DJ. Computer predictions of bone remodeling around porous-coated implants. J Arthoplast. September 1990;5(3):191-200.
1989	Carter DR, Orr TE, Fyhrie DP. Relationships between loading history and femoral cancellous bone architecture. J Biomech. 1989;22(3):231-244.
1991	Carter DR, Wong M, Orr TE. Musculoskeletal ontogeny, phylogeny, and functional adaptation. J Biomech. 1991;24(suppl 1):3-16.
1995	Mikić B, Carter DR. Bone strain gage data and theoretical models of functional adaptation. J Biomech. April 1995;28(4):465-469.
1996	Pattin CA, Caler WE, Carter DR. Cyclic mechanical property degradation during fatigue loading of cortical bone. J Biomech. January 1996;29(1):69-79.
1997	Adams DJ, Spirt AA, Brown TD, Fritton SP, Rubin CT, Brand RA. Testing the daily stress stimulus theory of bone adaptation with natural and experimentally controlled strain histories. J Biomech. July 1997;30(7):671-678.
2000	Fritton SP, McLeod KJ, Rubin CT. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. J Biomech. March 2000;33(3):317-325.
2001	Hazelwood SJ, Martin RB, Rashid MM, Rodrigo JJ. A mechanistic model for internal bone remodeling exhibits different dynamic responses in disuse and overload. J Biomech. March 2001;34(3):299-308.
2010	Cavanagh PR, Genc KO, Gopalakrishnan R, Kuklis MM, Maender CC, Rice AJ. Foot forces during typical days on the international space station. J Biomech. August 10, 2010;43(11):2182-2188.
1992	Snow-Harter C, Bouxsein ML, Lewis BT, Carter DR, Marcus R. Effects of resistance and endurance exercise on bone mineral status of young women: a randomized exercise intervention trial. J Bone Miner Res. July 1992;7(7):761-769.
1998	Swartz SM, Parker A, Huo C. Theoretical and empirical scaling patterns and topological homology in bone trabeculae. J Exp Biol. February 1998;201(4):573-590.
1990	Beaupré GS, Orr TE, Carter DR. An approach for time‐dependent bone modeling and remodeling: theoretical development. J Orthop Res. September 1990;8(5):651-661.
1990	Beaupré GS, Orr TE, Carter DR. An approach for time‐dependent bone modeling and remodeling—application: a preliminary remodeling simulation. J Orthop Res. September 1990;8(5):662-670.
1998	Qin Y, Rubin CT, McLeod KJ. Nonlinear dependence of loading intensity and cycle number in the maintenance of bone mass and morphology. J Orthop Res. July 1998;16(4):482-489.
2000	Giddings VL, Beaupré GS, Whalen RT, Carter DR. Calcaneal loading during walking and running. Med Sci Sports Exer. March 2000;32(3):627-634.
2020	Lin C. Effects of Marathon Training on Male and Female Femoral Stress Fracture Risk [Master's thesis]. California Polytechnic State University; November 2020.
2011	Genc KO. The Effects of Altered Gravity Environments on the Mechanobiology of Bone: From Bedrest to Spaceflight [PhD thesis]. Cleveland, OH: Case Western Reserve University; August 2011.
2007	Young CM. Do in-Line Dance, Progressively Loaded Squats and Foot Stomping Affect the Parameters of Fracture Risk in Postmenopausal Women? [Master's thesis]. Brisbane, Australia: Griffith University; 2007.
2009	Edwards WB. Internal Structural Loading of the Lower Extremity During Running: Implications for Skeletal Injury [PhD thesis]. Iowa State University; 2009.
1997	Heinonen A. Exercise as an Osteogenic Stimulus [PhD thesis]. University of Jyväskylä; 1997.
2003	Bona M. A Contact Algorithm for Density-Based Load Estimation [PhD thesis]. Lawrence, KS: University of Kansas; 2003.
2019	Frazer LL. Subchondral Bone Cysts Filling the Void [PhD thesis]. Lawrence, KS: University of Kansas; 2019.
2014	Ellman R. Skeletal Adaptation to Reduced Mechanical Loading [PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; September 2014.
2004	Tovar A. Bone Remodeling as a Hybrid Cellular Automaton Optimization Process [PhD thesis]. University of Notre Dame; December 2004.
1998	D'Andrea SE. Lower Limb Response to Impact in Simulated Microgravity and 1G [PhD thesis]. The Ohio State University; 1998.
1997	McCrory JL. A Biomechanical Comparison of 1-G and Fully Loaded Simulated Zero-Gravity Locomotion [PhD thesis]. State College, PA: Pennsylvania State University; May 1997.
2003	Peterman MM. A Strain Map of the Human Distal Tibia During the Stance Phase of Walking, from Dynamic Cadaver Experiments and Finite Element Analysis Simulations [PhD thesis]. State College, PA: Pennsylvania State University; August 2003.
2002	Wang X. Simulation for Bone Adaptive Remodeling: A Stochastic Approach With Application on Spine Fusion [PhD thesis]. Queen's University; May 2002.
1990	Orr TE. The Role of Mechanical Stresses in Bone Remodeling [PhD thesis]. Stanford University; September 1990.
1990	Wong M. The Role of Mechanical Loading Histories in Skeletal Morphogenesis [PhD thesis]. Stanford University; June 1990.
1992	Bouxsein ML. Physical Activity and Bone Density [PhD thesis]. Stanford University; August 1992.
1993	van der Meulen MCH. The Influence of Mechanics on Long Bone Development and Adaptation [PhD thesis]. Stanford University; June 1993.
1994	Jacobs CR. Numerical Simulation of Bone Adaptation to Mechanical Loading [PhD thesis]. Stanford University; June 1994.
1997	Stevens SS. Mechanical Regulation of Articular Cartilage Development, Maintenance and Degeneration [PhD thesis]. Stanford University; August 1997.
1998	Giddings VL. Computer Simulations of Calcaneal Loading and Bone Adaptation [PhD thesis]. Stanford University; June 1998.
1997	Qin Y-X. Fluid Flow, Matrix Strain and Loading Frequency as Interdependent Control Parameters in Skeletal Adaptation [PhD thesis]. Stony Brook, NY: State University of New York at Stony Brook; May 1997.
2011	Vijayaraghavan S. Duration of Reambulation Phases as a Modulator of the Detrimental Impact of Multiple Disuse Exposures on the Skeleton [Master's thesis]. Stony Brook, NY: Stony Brook University; August 2011.
2006	Rouhi G. Theoretical Aspects of Bone Remodeling and Resorption Processes [PhD thesis]. Calgary, AB: University of Calgary; March 2006.
2003	Nyman JS. Simulations of Bone Adaptation to Total Knee Arthroplasty and Bisphosphonates Through Remodeling Stimulated by Microdamage and Disuse [PhD thesis]. Davis, University of California; 2003.
2002	Walsh AJL. Tissue Remodeling in the Intervertebral Disc: Response to Dynamic Loading and Growth Factors [PhD thesis]. San Francisco, University of California; 2002.
1996	Adams DJ. Mechanical Factors Initiating Appositional Bone Formation [PhD thesis]. University of Iowa; May 1996.
2007	Christiansen BA. Vibrational Stimulation of Bone Formation in Mice [PhD thesis]. St. Louis, MO: Washington University in St. Louis; December 2007.