Age variations in the properties of human tibial trabecular bone

wbldb

Ding, Ming¹; Dalstra, Michel¹; Danielsen, Carl C.²; Kabel, Jesper¹; Hvid, Ivan¹; Linde, Frank¹

Age variations in the properties of human tibial trabecular bone

J Bone Joint Surg. November 1997;79B(6):995-1002

Affiliations

¹Orthopaedic Research Laboratory, Aarhus University Hospital (AKH), Kommunehospital, Building 1A, DK-8000, Aarhus C, Denmark

²Department of Connective Tissue Biology, Institute of Anatomy, University of Aarhus, DK-8000 Aarhus C, Denmark.
Abstract

We tested in compression specimens of human proximal tibial trabecular bone from 31 normal donors aged from 16 to 83 years and determined the mechanical properties, density and mineral and collagen content.

Young's modulus and ultimate stress were highest between 40 and 50 years, whereas ultimate strain and failure energy showed maxima at younger ages. These age-related variations (except for failure energy) were non-linear.

Tissue density and mineral concentration were constant throughout life, whereas apparent density (the amount of bone) varied with ultimate stress. Collagen density (the amount of collagen) varied with failure energy. Collagen concentration was maximal at younger ages but varied little with age.

Our results suggest that the decrease in mechanical properties of trabecular bone such as Young's modulus and ultimate stress is mainly a consequence of the loss of trabecular bone substance, rather than a decrease in the quality of the substance itself. Linear regression analysis showed that collagen density was consistently the single best predictor of failure energy, and collagen concentration was the only predictor of ultimate strain.
Links

DOI: 10.1302/0301-620X.79B6.7538

PubMed: 9393920

WoS: A1997YL20900024
History

Received: 1996-12-23

Accepted: 1997-05-29

Cited Works (30)

Year	Entry
1966	Weaver JK, Chalmers J. Cancellous bone: its strength and changes with aging and an evaluation of some methods for measuring its mineral content, I: age changes in cancellous bone. J Bone Joint Surg. March 1966;48A(2):289-298.
1985	Hvid I, Hansen SL. Trabecular bone strength patterns at the proximal tibial epiphysis. J Orthop Res. 1985;3(4):464-472.
1982	Armstrong CG, Mow VC. Variations in the intrinsic mechanical properties of human articular cartilage with age, degeneration, and water content. J Bone Joint Surg. 1982;64A(1):88-94.
1991	Goldstein SA, Matthews LS, Kuhn JL, Hollister SJ. Trabecular bone remodeling: an experimental model. J Biomech. 1991;24(suppl 1):135-150.
1990	Skerry TM, Suswillo R, El Haj AJ, Ali NN, Dodds RA, Lanyon LE. Load-induced proteoglycan orientation in bone tissuein vivo and in vitro. Calcif Tiss Int. May 1990;46(5):318-326.
1993	Dalstra M, Huiskes R, Odgaard A, van Erning L. Mechanical and textural properties of pelvic trabecular bone. J Biomech. April–May 1993;26(4-5):523-535.
1985	Panjabi MM, Krag M, Summers D, Videman T. Biomechanical time-tolerance of fresh cadaveric human spine specimens. J Orthop Res. 1985;3(3):292-300.
1989	Linde F, Hvid I, Pongsoipetch B. Energy absorptive properties of human trabecular bone specimens during axial compression. J Orthop Res. May 1989;7(3):432-439.
1993	Linde F, Sørensen HCF. The effect of different storage methods on the mechanical properties of trabecular bone. J Biomech. 1993;26(10):1249-1252.
1994	Linde F. Elastic and viscoelastic properties of trabecular bone by a compression testing approach. Dan Med Bull. April 1994;41(2):119-138.
1987	Mosekilde L, Mosekilde L, Danielsen CC. Biomechanical competence of vertebral trabecular bone in relation to ash density and age in normal individuals. Bone. 1987;8(2):79-85.
1992	Linde F, Hvid I, Madsen F. The effect of specimen geometry on the mechanical behaviour of trabecular bone specimens. J Biomech. 1992;25(4):359-368.
1977	Carter DR, Hayes WC. The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg. 1977;59A(7):954-962.
1975	Currey JD, Butler G. The mechanical properties of bone tissue in children. J Bone Joint Surg. September 1975;57A(6):810-814.
1989	Linde F, Hvid I. The effect of constraint on the mechanical behaviour of trabecular bone specimens. J Biomech. 1989;22(5):485-490.
1988	Linde F, Gøthgen CB, Hvid I, Pongsoipetch B, Bentzen S. Mechanical properties of trabecular bone by a non‐destructive compression testing approach. Eng Med. 1988;17(1):23-29.
1981	Riggs BL, Wahner HW, Dunn WL, Mazess RB, Offord KP, Melton LJ III. Differential changes in bone mineral density of the appendicular and axial skeleton with aging: relationship to spinal osteoporosis. J Clin Invest. February 1981;67(2):328-335.
1987	Goldstein SA. The mechanical properties of trabecular bone: dependence on anatomic location and function. J Biomech. 1987;20(11-12):1055-1061.
1990	Sharp DJ, Tanner KE, Bonfield W. Measurement of the density of trabecular bone. J Biomech. 1990;23(8):853-857.
1989	Hvid I, Bentzen SM, Linde F, Mosekilde L, Pongsoipetch B. X-ray quantitative computed tomography: the relations to physical properties of proximal tibial trabecular bone specimens. J Biomech. 1989;22(8-9):837-844.
1993	McCalden RW, McGeough JA, Barker MB, Court-Brown CM. Age-related changes in the tensile properties of cortical bone: the relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg. 1993;75A(8):1193-1205.
1976	Lindahl O. Mechanical properties of dried defatted spongy bone. Acta Orthop Scand. 1976;47(1):11-19.
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.
1964	Gong JK, Arnold JS, Cohn SH. Composition of trabecular and cortical bone. Anat Rec. 1964;149(3):325-331.
1967	Bell GH, Dunbar O, Beck JS, Gibb A. Variations in strength of vertebrae with age and their relation to osteoporosis. Calcif Tiss Res. 1967;1(1):75-86.
1975	Burstein AH, Zika JM, Heiple KG, Klein L. Contribution of collagen and mineral to the elastic-plastic properties of bone. J Bone Joint Surg. October 1975;57A(7):956-961.
1991	Linde F, Nørgaard P, Hvid I, Odgaard A, Søballe K. Mechanical properties of trabecular bone: dependency on strain rate. J Biomech. 1991;24(9):803-809.
1979	Currey JD. Changes in the impact energy absorption of bone with age. J Biomech. 1979;12(6):459-469.
1976	Burstein AH, Reilly DT, Martens M. Aging of bone tissue: mechanical properties. J Bone Joint Surg. 1976;58A(1):82-86.
1993	Keaveny TM, Hayes WC. A 20-year perspective on the mechanical properties of trabecular bone. J Biomech Eng. November 1993;115(4B):534-542.

Cited By (52)

Year	Entry
2001	Keaveny TM. Strength of trabecular bone. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:16-1–16-42.
2001	Zhang L, Yang KH, Dwarampudi R, Omori K, Li T, Chang K, Hardy WN, Khalil TB, King AI. Recent advances in brain injury research: a new human head model development and validation. Stapp Car Crash J. 2001;45:369-394. SAE 2001-22-0017.
2004	Kent R, Lessley D, Sherwood C. Thoracic response to dynamic, non-impact loading from a hub, distributed belt, diagonal belt, and double diagonal belts. Stapp Car Crash J. 2004;48:495-519. SAE 2004-22-0022.
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	Keaveny TM, Morgan EF, Niebur GL, Yeh OC. Biomechanics of trabecular bone. Annu Rev Biomed Eng. 2001;3:307-333.
1999	Yeh OC, Keaveny TM. Biomechanical effects of intraspecimen variations in trabecular architecture: a three-dimensional finite element study. Bone. August 1999;25(2):223-228.
2000	Ding M, Hvid I. Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone. March 2000;26(3):291-295.
2000	Day JS, Ding M, Odgaard A, Sumner DR, Hvid I, Weinans H. Parallel plate model for trabecular bone exhibits volume fraction-dependent bias. Bone. November 2000;27(5):715-720.
2002	Hu JH, Ding M, Søballe K, Bechtold JE, Danielsen CC, Day JS, Hvid I. Effects of short-term alendronate treatment on the three-dimensional microstructural, physical, and mechanical properties of dog trabecular bone. Bone. November 2002;31(5):591-597.
2004	Akkus O, Adar F, Schaffler MB. Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone. Bone. March 2004;34(4):443-453.
2007	Perilli E, Baleani M, Öhman C, Baruffaldi F, Viceconti M. Structural parameters and mechanical strength of cancellous bone in the femoral head in osteoarthritis do not depend on age. Bone. November 2007;41(5):760-768.
2018	Zhao S, Arnold M, Ma S, Abel RL, Cobb JP, Hansen U, Boughton O. Standardizing compression testing for measuring the stiffness of human bone. Bone Joint Res. August 2018;7(8):524-538.
2003	Ding M, Day JS, Burr DB, Mashiba T, Hirano T, Weinans H, Sumner DR, Hvid I. Canine cancellous bone microarchitecture after one year of high-dose bisphosphonates. Calcif Tiss Int. June 2003;72(6):737-744.
2003	Giesen EBW, Ding M, Dalstra M, van Eijden TMGJ. Architectural measures of the cancellous bone of the mandibular condyle identified by principal components analysis. Calcif Tiss Int. 2003;73(3):225-231.
2005	Busa B, Miller LM, Rubin CT, Qin Y-X, Judex S. Rapid establishment of chemical and mechanical properties during lamellar bone formation. Calcif Tiss Int. December 2005;77(6):386-394.
1999	Ding M, Odgaard A, Hvid I. Accuracy of cancellous bone volume fraction measured by micro-CT scanning. J Biomech. 1999;32(3):323-326.
2023	Albert DL, Katzenberger MJ, Hunter RL, Agnew AM, Kemper AR. Effects of loading rate, age, and morphology on the material properties of human rib trabecular bone. J Biomech. July 2023;156:111670.
2001	Arthur Moore TL, Gibson LJ. Modeling modulus reduction in bovine trabecular bone damaged in compressio. J Biomech Eng. December 2001;123(6):613-622.
2015	Oftadeh R, Perez-Viloria M, Villa-Camacho JC, Vaziri A, Nazarian A. Biomechanics and mechanobiology of trabecular bone: a review. J Biomech Eng. January 2015;137(1):010802.
2002	Ding M, Odgaard A, Danielsen CC, Hvid I. Mutual associations among microstructural, physical and mechanical properties of human cancellous bone. J Bone Joint Surg. August 2002;84B(6):900-907.
1999	Boskey AL, Wright TM, Blank RD. Collagen and bone strength. J Bone Miner Res. March 1999;14(3):330-335.
2003	Akkus O, Polyakova‐Akkus A, Adar F, Schaffler MB. Aging of microstructural compartments in human compact bone. J Bone Miner Res. June 2003;18(6):1012-1019.
2009	Gourion‐Arsiquaud S, Burket JC, Havill LM, DiCarlo E, Doty SB, Mendelsohn R, van der Meulen MCH, Boskey AL. Spatial variation in osteonal bone properties relative to tissue and animal age. J Bone Miner Res. July 2009;24(7):1271-1281.
2015	Grassi L, Isaksson H. Extracting accurate strain measurements in bone mechanics: a critical review of current methods. J Mech Behav Biomed Mater. October 2015;50:43-54.
2017	Sandino C, McErlain DD, Schipilow J, Boyd SK. Mechanical stimuli of trabecular bone in osteoporosis: a numerical simulation by finite element analysis of microarchitecture. J Mech Behav Biomed Mater. February 2017;66:19-27.
2020	Hart NH, Newton RU, Tan2 J, Rantalainen T, Chivers P, Siafarikas A, Nimphius S. Biological basis of bone strength: anatomy, physiology and measurement. J Musculoskel Neuron Interact. September 2020;20(3):347-371.
2000	Guo XE, Goldstein SA. Vertebral trabecular bone microscopic tissue elastic modulus and hardness do not change in ovariectomized rats. J Orthop Res. March 2000;18(2):333-336.
2002	Ding M, Odgaard A, Linde F, Hvid I. Age-related variations in the microstructure of human tibial cancellous bone. J Orthop Res. May 2002;20(3):615-621.
2021	Ding M, Overgaard S. 3-D microarchitectural properties and rod- and plate-like trabecular morphometric properties of femur head cancellous bones in patients with rheumatoid arthritis, osteoarthritis, and osteoporosis. J Orthop Translat. May 2021;28:159-168.
2020	Ketata H, Kharrat M, Dammak M. Modeling age-related changes in the mechanical behavior of the fracture-fixated human tibia bone during healing. Med Eng Phys. July 2020;81:77-85.
2005	Viano DC, Casson IR, Pellman EJ, Zhang L, King AI, Yang KH. Concussion in professional football: brain responses by finite element analysis: part 9. Neurosurgery. November 2005;57(5):891-916.
2007	Clark EM. An Investigation Into the Role of Bone Mass and Other Factors in Determining Fracture Risk in Children [PhD thesis]. Bristol, UK: University of Bristol; 2007.
2012	Slyfield CR Jr. The Biomechanics of Bone Turnover [PhD thesis]. Ithaca, NY: Cornell University; January 2012.
2005	Cook RB. Non-Invasively Assessed Skeletal Bone Status and Its Relationship to the Biomechanical Properties and Condition of Cancellous Bone [PhD thesis]. Cranfield, UK: Cranfield University; December 18, 2005.
2011	Donaldson FE. On Incorporating Bone Microstructure in Macro-Finite-Element Models [PhD thesis]. Edinburgh, UK: University of Edinburgh; March 2011.
2012	Hamed E. Multiscale Modeling of Elastic Moduli and Strength of Bone [PhD thesis]. University of Illinois at Urbana-Champaign; 2012.
2016	Currier EJ. Predicting Peak Load of the Femoral Neck Using Structural Parameters [Master's thesis]. University of Illinois at Urbana-Champaign; 2016.
2023	Moshage SG. Non-Invasive Determinants of Juvenile Equine Bone Strength for Assessing Exercise Interventions [PhD thesis]. University of Illinois at Urbana-Champaign; 2023.
2016	Grassi L. Femoral Strength Prediction Using Finite Element Models: Validation of Models Based on CT and Reconstructed DXA Images Against Full-Field Strain Measurements [PhD thesis]. Lund, Sweden: Lund University; 2016.
2007	Akhtar R. Micromechanical Behaviour of Bone [PhD thesis]. University of Manchester; 2007.
2001	Arthur Moore TL. Microdamage Accumulation in Bovine Trabecular Bone [PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; June 2001.
2015	Oftadeh R. Hierarchical Analysis and Multiscale Modelling of Cellular Structures: From Meta Materials to Bone Structure [PhD thesis]. Northeastern University; December 2015.
2010	Garo A. Modélisation du corps vertébral en chargement dynamique: Intégration de l'effet de l'âge [Vertebral Body Modeling in Dynamic Loading: Integration of Age Effects] [PhD thesis]. École polytechnique de Montréal; December 2010.
2013	Schumacher Y. Comparison of Two Loading Surface Preparation Methods on Rat Vertebral Bodies for Compression Testing [Master's thesis]. Queen's University; September 2013.
2005	Gushue DL. Frontal Plane Knee Joint Biomechanics: Implications in Experimental Animal Models and Childhood Obesity [PhD thesis]. University of Rochester; 2005.
2009	Lancianese SL. Modeling the Effect of Obesity and Related Biomechanical Risk Factors on the Onset of Knee Osteoarthritis [PhD thesis]. University of Rochester; 2009.
2004	Mittra ES. Assessment of Trabecular Bone Quality Using Microstructure, Micro-Mechanics and Micro-Finite Element Modeling [PhD thesis]. Stony Brook, NY: Stony Brook University; May 2004.
2010	Johnston JD. Development of a Non-Invasive Imaging Technique for Characterizing Subchondral Bone Density and Stiffness [PhD thesis]. Vancouver, BC: University of British Columbia; December 2010.
2020	Patton DM. Changes in Femoral Structure and Function Following Anterior Cruciate Ligament Injury and With Aging [PhD thesis]. University of Michigan; 2020.
2010	Schwen LO. Composite Finite Elements for Trabecular Bone Microstructures [PhD thesis]. Bonn, Germany: Rheinische Friedrich-Wilhelms-Universität Bonn; July 2010.
2010	Reyes MJ. Age-Related Influence of Bone Remodeling on Local Tissue Properties of Human Cortical Bone [PhD thesis]. San Antionio, TX: University of Texas at San Antonio; December 2010.
2009	García-Rodríguez S. Mechanical Behavior of Trabecular Bone [PhD thesis]. University of Wisconsin – Madison; 2009.