Mechanical factors in bone growth and development

wbldb

Carter, D. R.¹; Van der Meulen, M. C. H.¹; Beaupré, G. S.¹

Mechanical factors in bone growth and development

Bone. January 1996;18(1)(suppl 1):S5-S10

©1996 Elsevier Science Inc.

Affiliations

¹Department of Mechanical Engineering, Biomechanical Engineering Program, Stanford University, Stanford, CA

²Rehabilitation Research & Development Center, Veterans Affairs Health System, Palo Alto, CA, USA
Abstract and keywords

Mechanobiologic factors strongly influence skeletal ossification and regulate changes in bone geometry and apparent density during ontogeny. We have developed computer models that implement a simple mathematical rule relating cyclic tissue stresses to bone apposition and resorption. Beginning at the fetal stages of the femoral anlage, these models successfully predict the appositional bone growth and modeling observed in the development of the diaphyseal cross section. The same basic mechanobiologic rule can also predict the architectural construction of the proximal cancellous bone formed in regions of endochondral ossification. Geometry and density changes in adult diaphyseal cancellous bone as a result of changes in physical activity can be simulated by invoking the same rule used during development. Future clinical and experimental work is needed to provide more quantitative data for mechanobiologic rules and elucidate the interactions between chemical and mechanical factors influencing bone biology.

Keywords: Bone; Bone development; Bone adaptation; Mechanical adaptation; Mathematical modeling; Morphogenesis
Links

DOI: 10.1016/8756-3282(95)00373-8

PubMed: 8717541

WoS: A1996TT81200002

Cited Works (29)

Year	Entry
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.
1977	Martin RB, Atkinson PJ. Age and sex-related changes in the structure and strength of the human femoral shaft. J Biomech. 1977;10(4):223-231.
1986	Biewener AA, Swartz SM, Bertram JEA. Bone modeling during growth: dynamic strain equilibrium in the chick tibiotarsus. Calcif Tiss Int. November 1986;39(6):390-395.
1989	Keller TS, Spengler DM. Regulation of bone stress and strain in the immature and mature rat femur. J Biomech. 1989;22(11-12):1115-1127.
1978	Uhthoff HK, Jaworski ZF. Bone loss in response to long-term immobilisation. J Bone Joint Surg. August 1978;60B(3):420-429.
1990	Orr TE. The Role of Mechanical Stresses in Bone Remodeling [PhD thesis]. Stanford University; September 1990.
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.
1983	Urist MR, DeLange RJ, Finerman GA. Bone cell differentiation and growth factors. Science. May 13, 1983;220(4598):680-686.
1995	Mikić B, Carter DR. Bone strain gage data and theoretical models of functional adaptation. J Biomech. April 1995;28(4):465-469.
1992	Gross TS, McLeod KJ, Rubin CT. Characterizing bone strain distributions in vivo using three triple rosette strain gages. J Biomech. September 1992;25(9):1081-1087.
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.
1991	Carter DR, Wong M, Orr TE. Musculoskeletal ontogeny, phylogeny, and functional adaptation. J Biomech. 1991;24(suppl 1):3-16.
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.
1991	Biewener AA. Musculoskeletal design in relation to body size. J Biomech. 1991;24(suppl 1):19-29.
1987	Frost HM. Bone “mass” and the “mechanostat”: a proposal. Anat Rec. September 1987;219(1):1-9.
1988	Dalsky GP, Stocke KS, Ehsani AA, Slatopolsky E, Lee WC, Birge SJ Jr. Weight-bearing exercise training and lumbar bone mineral content in postmenopausal women. Ann Intern Med. June 1988;108(6):824-828.
1982	Ruff CB, Hayes WC. Subperiosteal expansion and cortical remodeling of the human femur and tibia with aging. Science. September 3, 1982;217(4563):945-948.
1988	Whalen RT, Carter DR, Steele CR. Influence of physical activity on the regulation of bone density. J Biomech. 1988;21(10):825-837.
1985	Cowin SC, Hart RT, Balser JR, Kohn DH. Functional adaptation in long bones: establishing in vivo values for surface remodeling rate coefficients. J Biomech. 1985;18(9):665-684.
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.
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.
1978	Morey ER, Baylink DJ. Inhibition of bone formation during space flight. Science. September 22, 1978;201(4361):1138-1141.
1992	Weinans H, Huiskes R, Grootenboer HJ. The behavior of adaptive bone-remodeling simulation models. J Biomech. December 1992;25(12):1425-1441.
1987	Carter DR, Orr TE, Fyhrie DP, Schurmant DJ. Influences of mechanical stress on prenatal and postnatal skeletal development. Clin Orthop Relat Res. June 1987;219:237-250.
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.
1987	Huiskes R, Weinans H, Grootenboer HJ, Dalstra M, Fudala B, Slooff TJ. Adaptive bone-remodeling theory applied to prosthetic-design analysis. J Biomech. 1987;20(11-12):1135-1150.
1964	Smith RW Jr, Walker RR. Femoral expansion in aging women: implications for osteoporosis and fractures. Science. July 10, 1964;145(3628):156-157.
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.
1984	Rubin CT, Lanyon LE. Dynamic strain similarity in vertebrates: an alternative to allometric limb bone scaling. J Theo Biol. March 21, 1984;107(2):321-327.

Cited By (35)

Year	Entry
2012	Forman JL, del Pozo de Dios E, Symeonidis I, Duart J, Kerrigan JR, Salzar RS, Balasubramanian S, Segui‐Gomez M, Kent RW. Fracture tolerance related to skeletal development and aging throughout life: 3‐point bending of human femurs. In: Proceedings of the 2012 International IRCOBI Conference on the Biomechanics of Injury. September 12-14, 2012; Dublin, Ireland.524-539.
2019	Marques M, Belinha J, Oliveira AF, Manzanares-Céspedes MC, Jorge RN. Combining radial point interpolation meshless method with a new homogenization technique for trabecular bone multiscale structural analyses. Acta Bioeng Biomech. 2019;21(2):101-113.
2020	Marques M, Belinha J, Oliveira AF, Manzanares Cespedes MC, Natal Jorge RM. A 3D trabecular bone homogenization technique. Acta Bioeng Biomech. 2020;22(3):139-152.
2005	Fritton JC, Myers ER, Wright TM, van der Meulen MCH. Loading induces site-specific increases in mineral content assessed by microcomputed tomography of the mouse tibia. Bone. June 2005;36(6):1030-1038.
1997	Prendergast PJ, Huiskes R, Søballe K. Biophysical stimuli on cells during tissue differentiation at implant interfaces. J Biomech. June 1997;30(6):539-548.
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.
2020	Alonso MG, Bertolino G, Yawny A. Mechanobiological based long bone growth model for the design of limb deformities correction devices. J Biomech. August 26, 2020;109:109905.
1997	Morris FL, Naughton GA, Gibbs JL, Carlson JS, Wark JD. Prospective ten-month exercise intervention in premenarcheal girls: positive effects on bone and lean mass. J Bone Miner Res. September 1997;12(9):1453-1462.
2001	Beck TJ, Oreskovic TL, Stone KL, Ruff CB, Ensrud K, Nevitt MC, Genant HK, Cummings SR. Structural adaptation to changing skeletal load in the progression toward hip fragility: the study of osteoporotic fractures. J Bone Miner Res. June 2001;16(6):1108-1119.
2018	Kersh ME, Martelli S, Zebaze R, Seeman E, Pandy MG. Mechanical loading of the femoral neck in human locomotion. J Bone Miner Res. November 2018;33(11):1999-2006.
2011	Erkmen E, Meriç G, Kurt A, Tunç Y, Eser A. Biomechanical comparison of implant retained fixed partial dentures with fiber reinforced composite versus conventional metal frameworks: a 3d fea study. J Mech Behav Biomed Mater. January 2011;4(1):107-116.
2016	McDermott AM, Mason DE, Lin AS, Guldberg RE, Boerckel JD. Influence of structural load-bearing scaffolds on mechanical load- and BMP-2-mediated bone regeneration. J Mech Behav Biomed Mater. September 2016;62:169-181.
2001	Le AX, Miclau T, Hu D, Helms JA. Molecular aspects of healing in stabilized and non-stabilized fractures. J Orthop Res. January 2001;19(1):78-84.
2012	Boerckel JD, Kolambkar YM, Stevens HY, Lin ASP, Dupont KM, Guldberg RE. Effects of in vivo mechanical loading on large bone defect regeneration. J Orthop Res. July 2012;30(7):1067-1075.
2024	Szabo E. Insights Into the Mechanical Behavior of Maturing Cortical Bone: A Porcine Model [PhD thesis]. Cleveland, OH: Case Western Reserve University; May 2024.
2006	Fritton JC. Mechanical Loading Induced Adaptation of the Mouse Tibia [PhD thesis]. Ithaca, NY: Cornell University; January 2006.
2005	Ho EY. Engineering Bioactive Polymers for the Next Generation of Bone Repair [PhD thesis]. Drexel University; April 2005.
2011	Boerckel JD. Mechanical Regulation of Bone Regeneration and Vascular Growth in Vivo [PhD thesis]. Atlanta, GA: Georgia Institute of Technology; August 2011.
2020	Lewandowski K. Numerical Investigation of Bone Adaptation to Exercise and Fracture in Thoroughbred Racehorses [PhD thesis]. Glasgow, UK: University of Glasgow; February 2020.
2010	Chennimalai Kumar N. Numerical Modeling of Cortical Bone Adaptation Due to Mechanical Loading Using the Finite Element Method [PhD thesis]. University of Illinois at Urbana-Champaign; 2010.
2009	Carriero A. Modelling Gait Abnormalities and Bone Deformities in Children With Cerebral Palsy [PhD thesis]. Imperial College London; May 2009.
2012	Garofalo EM. Environmental and Genetic Effects on Growth of the Human Skeleton: A Bioarchaeological Investigation [PhD thesis]. Johns Hopkins University; December 2012.
2002	Hudson JA. The Ontogeny of Transverse Femoral Geometry and Bone Modeling in the Ward Skeletal Population [PhD thesis]. Kent State University; August 2002.
1998	Robling AG. Histomorphometric Assessment of Mechanical Loading History from Human Skeletal Remains: The Relation Between Micromorphology and Macromorphology At the Femoral Midshaft [PhD thesis]. University of Missouri; December 1998.
2021	Fawcett EB. Effect of Brachial Plexus Birth Injury on Postnatal Glenohumeral Bone and Muscle [PhD thesis]. North Carolina State University; 2021.
2019	McDermott AM. Mechanical Regulation of Progenitor Cell Differentiation During Endochondral Ossification [PhD thesis]. University of Notre Dame; July 2019.
2012	Kelly N. An Experimental and Computational Investigation of the Inelastic Behaviour of Trabecular Bone [PhD thesis]. Galway, Ireland: National University of Ireland Galway; September 2012.
2010	Lin H. Biomechanical Modeling of Vertebral Mechanobiological Growth and of the Deformation Process in Adolescent Idiopathic Scoliosis [PhD thesis]. École polytechnique de Montréal; June 2010.
2019	Mustafy T. The Short and Long Term Effects of in Vivo Cyclic Axial Compression Applied During Puberty on Bone Growth, Morphometry and Biomechanics [PhD thesis]. École polytechnique de Montréal; July 2019.
2022	Beloglowka K. Ex Vivo Mechanical Testing and FEA Modelling of Bovine Trabecular Bone [Master's thesis]. Queen's University; September 2022.
2017	Gabel LEC. Bone Strength Accrual Across Adolescent Growth and the Influences of Physical Activity and Sedentary Time [PhD thesis]. Vancouver, BC: University of British Columbia; April 2017.
1999	Judex S. The Effect of Exercise-Induced Mechanical Stimuli on Cortical Bone [PhD thesis]. Calgary, AB: University of Calgary; 1999.
2006	Rouhi G. Theoretical Aspects of Bone Remodeling and Resorption Processes [PhD thesis]. Calgary, AB: University of Calgary; March 2006.
2000	Nauman EA. The Analytical Design of a Hybrid Bone Substitute [PhD thesis]. Berkeley, CA: Berkeley, University of California; Spring 2000.
2007	Wallace JM III. Investigating the Inbred Strain-Specific Response to Biglycan-Deficiency and Exercise: A Study in Genetically-Mediated Skeletal Adaptation [PhD thesis]. University of Michigan; 2007.