Trabecular bone remodeling: an experimental model

wbldb

Goldstein, Steven A.¹; Matthews, Larry S.¹; Kuhn, Janet L.¹; Hollister, Scott J.¹

Trabecular bone remodeling: an experimental model

J Biomech. 1991;24(suppl 1):135-150

Affiliations

¹The Orthopaedic Research Laboratories, The University of Michigan, Section of Orthopaedic Surgey, Department of Surgery, Ann Arbor, MI 48109, U.S.A.
Abstract

An experimental model, capable of inducing controlled stress fields to the distal femoral metaphyses of large dogs, is presented. This model utilized an implantable hydraulic device incorporating five loading cylinders and platens in direct contact with an exposed plane of trabecular bone. A microprocessor controls the loading characteristics, and finite element models were created to calculate the induced stress and strain fields. The trabecular remodeling response is measured using serial in vivo computed tomography, in vitro microcomputed tomography, and histologic analysis. The results of the experiment indicate that significant remodeling can be induced by the activated implant. An increase in trabecular orientation toward the loaded platens was observed, and a statistically significant decrease in connectivity was documented. The greatest effect was associated with a change in the loading rate. A fast rise time (70 ms) loading waveform induced significant bone ingrowth at the implant interface when compared to a slow rise time waveform (700 ms), and demonstrated high correlations with the calculated stress fields as remodeling approached an equilibrium state.
Links

DOI: 10.1016/0021-9290(91)90384-Y

PubMed: 1791174

WoS: A1991HB54500013

Cited Works (28)

Year	Entry
1979	Parfitt AM. Quantum concept of bone remodeling and turnover: implications for the pathogenesis of osteoporosis. Calcif Tiss Int. 1979;28(1):1-5.
1984	Parfitt AM. The cellular basis of bone remodeling: the quantum concept reexamined in light of recent advances in the cell biology of bone. Calcif Tiss Int. March 1984;36(suppl 1):S37-S45.
1974	Lanyon LE. Experimental support for the trajectorial theory of bone structure. J Bone Joint Surg. 1974;56B(1):160-166.
1972	Chamay A, Tschantz P. Mechanical influences in bone remodeling: experimental research on Wolff's law. J Biomech. March 1972;5(2):173-180.
1979	Goodship AE, Lanyon LE, McFie H. Functional adaptation of bone to increased stress: an experimental study. J Bone Joint Surg. June 1979;61A(4):539-546.
1990	Fyhrie DP, Carter DR. Femoral head apparent density distribution predicted from bone stresses. J Biomech. 1990;23(1):1-10.
1892	Wolff J. Das Gesetz der Transformation der Knochen. Berlin: Hirschwald; 1892.
1990	Kuhn JL, Goldstein SA, Feldkamp LA, Goulet RW, Jesion G. Evaluation of a microcomputed tomography system to study trabecular bone structure. J Orthop Res. 1990;8(6):833-842.
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.
1985	Burr DB, Martin RB, Schaffler MB, Radin EL. Bone remodeling in response to in vivo fatigue microdamage. J Biomech. 1985;18(3):189-200.
1964	Frost HM. The Laws of Bone Structure. Springfield, IL: Charles C. Thomas; 1964.
1983	Frost HM. The regional acceleratory phenomenon: a review. Henry Ford Hosp Med J. 1983;31(1):3-9.
1983	Frost HM. A determinant of bone architecture: the minimum effective strain. Clin Orthop Relat Res. August 1983;175:286-292.
1984	Harrigan TP, Mann RW. Characterization of microstructural anisotropy in orthotropic materials using a second rank tensor. J Mater Sci. March 1984;19(3):761-767.
1987	Lanyon LE. Functional strain in bone tissue as an objective, and controlling stimulus for adaptive bone remodelling. J Biomech. 1987;20(11-12):1083-1093.
1969	Seireg A, Kempke W. Behavior of in vivo bone under cyclic loading. J Biomech. October 1969;2(4):455-461.
1979	Churches AE, Howlett CR, Waldron KJ, Ward GW. The response of living bone to controlled time-varying loading: method and preliminary results. J Biomech. 1979;12(1):35-45.
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.
1976	Lanyon LE, Baggott DG. Mechanical function as an influence on the structure and form of bone. J Bone Joint Surg. November 1976;58B(4):436-443.
1982	Martin RB, Burr DB. A hypothetical mechanism for the stimulation of osteonal remodelling by fatigue damage. J Biomech. 1982;15(3):137-139.
1989	Feldkamp LA, Goldstein SA, Parfitt MA, Jesion G, Kleerekoper M. The direct examination of three‐dimensional bone architecture in vitro by computed tomography. J Bone Miner Res. 1989;4(1):3-11.
1986	Fyhrie DP, Carter DR. A unifying principle relating stress to trabecular bone morphology. J Orthop Res. 1986;4(3):304-317.
1984	Carter DR. Mechanical loading histories and cortical bone remodeling. Calcif Tiss Int. March 1984;36(suppl 1):S19-S24.
1984	Hart RT, Davy DT, Heiple KG. Mathematical modeling and numerical solutions for functionally dependent bone remodeling. Calcif Tiss Int. March 1984;36(suppl 1):S104-S109.
1986	Cowin SC. Wolff’s law of trabecular architecture at remodeling equilibrium. J Biomech Eng. February 1986;108(1):83-88.
1985	Cowin SC. The relationship between the elasticity tensor and the fabric tensor. Mech Mater. 1985;4(2):137-147.
1987	Cheal EJ, Snyder BD, Nunamaker DM, Hayes WC. Trabecular bone remodeling around smooth and porous implants in an equine patellar model. J Biomech. 1987;20(11-12):1121-1134.
1984	Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg. March 1984;66A(3):397-402.

Cited By (42)

Year	Entry
2000	Ding M. Age variations in the properties of human tibial trabecular bone and cartilage. Acta Orthop Scand. 2000;71(suppl 292):1-45.
2001	Fajardo RJ, Müller R. Three‐dimensional analysis of nonhuman primate trabecular architecture using micro‐computed tomography. Am J Phys Anthropol. 2001;115(4):327-336.
2012	Christen P, van Rietbergen B, Lambers FM, Müller R, Ito K. Bone morphology allows estimation of loading history in a murine model of bone adaptation. Biomech Model Mechanobiol. March 2012;11(3-4):483-492.
2006	van der Meulen MCH, Morgan TG, Yang X, Baldini TH, Myers ER, Wright TM, Bostrom MPG. Cancellous bone adaptation to in vivo loading in a rabbit model. Bone. June 2006;38(6):871-877.
2009	Mueller TL, Stauber M, Kohler T, Eckstein F, Müller R, van Lenthe GH. Non-invasive bone competence analysis by high-resolution pQCT: an in vitro reproducibility study on structural and mechanical properties at the human radius. Bone. February 2009;44(2):364-371.
2010	Lynch ME, Main RP, Xu Q, Walsh DJ, Schaffler MB, Wright TM, van der Meulen MCH. Cancellous bone adaptation to tibial compression is not sex dependent in growing mice. J Appl Physiol. September 2010;109(3):685-691.
1997	Turner CH, Annet V, Pidaparti RMV. A uniform strain criterion for trabecular bone adaptation: do continuum-level strain gradients drive adaptation? J Biomech. June 1997;30(6):555-563.
1998	Herzog W, Diet S, Suter E, Mayzus P, Leonard TR, Müller C, Wu JZ, Epstein M. Material and functional properties of articular cartilage and patellofemoral contact mechanics in an experimental model of osteoarthritis. J Biomech. December 1998;31(12):1137-1145.
2000	Weinans H, Sumner DR, Igloria R, Natarajan RN. Sensitivity of periprosthetic stress-shielding to load and the bone density–modulus relationship in subject-specific finite element models. J Biomech. July 2000;33(7):809-817.
2002	van der Meulen MC, Huiskes R. Why mechanobiology? a survey article. J Biomech. April 2002;35(4):401-414.
2003	Qin Y-X, Kaplan T, Saldanha A, Rubin C. Fluid pressure gradients, arising from oscillations in intramedullary pressure, is correlated with the formation of bone and inhibition of intracortical porosity. J Biomech. October 2003;36(10):1427-1437.
1993	Huiskes R, Hollister SJ. From structure to process, from organ to cell: recent developments of FE-analysis in orthopaedic biomechanics. J Biomech Eng. November 1993;115(4B):520-527.
1995	Luo G, Cowin SC, Sadegh AM, Arramon YP. Implementation of strain rate as a bone remodeling stimulus. J Biomech Eng. August 1995;117(3):329-338.
2001	Adachi T, Tsubota K-i, Tomita Y, Hollister SJ. Trabecular surface remodeling simulation for cancellous bone using microstructural voxel finite element models. J Biomech Eng. October 2001;123(5):403-409.
1997	Ding M, Dalstra M, Danielsen CC, Kabel J, Hvid I, Linde F. Age variations in the properties of human tibial trabecular bone. J Bone Joint Surg. November 1997;79B(6):995-1002.
1995	Rubin CT, Gross TS, McLeod KJ, Bain SD. Morphologie stages in lamellar bone formation stimulated by a potent mechanical stimulus. J Bone Miner Res. March 1995;10(3):488-495.
1996	Hipp JA, Jansujwicz A, Simmons CA, Snyder BD. Trabecular bone morphology from micro-magnetic resonance imaging. J Bone Miner Res. February 1996;11(2):286-292.
1997	Gross TS, Edwards JL, Mcleod KJ, Rubin CT. Strain gradients correlate with sites of periosteal bone formation. J Bone Miner Res. June 1997;12(6):982-988.
1999	McAllister TN, Frangos JA. Steady and transient fluid shear stress stimulate NO release in osteoblasts through distinct biochemical pathways. J Bone Miner Res. June 1999;14(6):930-936.
1999	Taylor WR. A Computer Based Technique for Predicting Changes in Bone Properties With Applications in Pre-Clinical Testing of Hip Implants [PhD thesis]. University of Bath; 1999.
2011	Kummari SR. Experimental and Computational Evaluation of Microscopic Tissue Damage and Remodeling Cavities in Trabecular Bone [PhD thesis]. Cleveland, OH: Case Western Reserve University; May 2011.
2003	Kim CH. In Vivo Trabecular Bone Response to Mechanical Loading and Parathyroid Hormone Stimulation [PhD thesis]. Columbia University; 2003.
2009	Chan M. Mechanobiology of 3D Co-Culture Trabecular Explant Model [PhD thesis]. Columbia University; 2009.
2010	Lynch ME. Cancellous Bone Adaptation to Non-Invasive Mechanical Loading in the Murine Tibia [PhD thesis]. Ithaca, NY: Cornell University; August 2010.
2017	Cresswell EN. Spatial Regulation of Bone Formation in Functional Adaptation of Cancellous Bone [PhD thesis]. Ithaca, NY: Cornell University; May 2017.
2010	Müller T. Bioimaging and Biomechanics of Bone Competence and Implant Stability [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2010.
2019	Watson S. LIFTMOR: Lifting Intervention for Training Muscle and Osteoporosis Rehabilitation [PhD thesis]. Brisbane, Australia: Griffith University; January 2019.
2002	Follet H. Caractérisation Biomécanique Et Modélisation 3D Par Imagerie X Et IRM Haute Résolution De L’os Spongieux Humain: Evaluation Du Risque Fracturaire [PhD thesis]. Institut national des sciences appliquées de Lyon (INSA Lyon); 2002.
2004	Tovar A. Bone Remodeling as a Hybrid Cellular Automaton Optimization Process [PhD thesis]. Notre Dame, IN: University of Notre Dame; December 2004.
2013	Verbruggen SW. Mechanobiological Origins of Osteoporosis [PhD thesis]. National University of Ireland Galway; September 2013.
1995	DeVries S. A Three-Dimensional Finite Element Stress Analysis of the Glenoid With and Without a Total Shoulder Arthroplasty Component [Master's thesis]. Queen's University; July 1995.
2010	Boyle CH. Computational Study of Wolff's Law Utilizing Design Space Topology Optimization: A New Method for Hip Prosthesis Design [Master's thesis]. Queen's University; August 2010.
2013	Christen P. Deciphering the Secret Message Within Bone Microstructure [PhD thesis]. Eindhoven University of Technology; 2013.
1994	Fritton SP. Computational Simulation of Trabecular Bone Adaptation [PhD thesis]. Tulane University; January 1994.
2018	Synek A. Predicting Habitual Activities from Bone Architecture Using a Biomechanical Approach [PhD thesis]. Vienna University of Technology; 2018.
2006	Macdonald HM. Effectiveness of a School-Based Physical Activity Intervention for Increasing Bone Strength in Children: Action Schools! British Columbia [PhD thesis]. Vancouver, BC: University of British Columbia; July 2006.
1995	Guldberg RE. Mechanical Adaptation of Trabecular Bone Formation in Vivo [PhD thesis]. University of Michigan; 1995.
1995	Tseng K-F. Investigating the Structure-Function Relationships of Long Bone: An Approach Using Growth Hormone Mouse Models [PhD thesis]. University of Michigan; 1995.
1997	Richards M. Strain Environment Effects on New Bone Formation and Precursor Tissue Differentiation During Distraction [PhD thesis]. University of Michigan; 1997.
2000	Borodkin JL. The Influence of Interface Micromechanics on the Biological Fixation of Porous-Coated Implants [PhD thesis]. University of Michigan; 2000.
2008	Waldorff EI. Effects of Aging and Disuse on Bone Remodeling in Response to Microdamage [PhD thesis]. University of Michigan; 2008.
1996	Beck BR. The Relationship of Streaming Potential Magnitude to Strain and Periosteal Modeling [PhD thesis]. Eugene, OR: University of Oregon; December 1996.