Age-related variations in the microstructure of human tibial cancellous bone

wbldb

Ding, Ming¹; Odgaard, Anders¹; Linde, Frank¹; Hvid, Ivan¹

Age-related variations in the microstructure of human tibial cancellous bone

J Orthop Res. May 2002;20(3):615-621

Affiliations

¹Orthopaedic Research Laboratory, Department of Orthopaedics, Aarhus University Hospital, Building 1 A, Norrebrogade 44, 8000 Aarhus C, Denmark
Abstract

A thorough understanding of the microstructure of cancellous bone is crucial for diagnosis, prophylaxis, and treatment of age-related skeletal diseases. Until now, little has been known about age-related variations in the microstructure of peripheral cancellous bone. This study quantified age-related changes in the three-dimensional (3D) microstructure of human tibial cancellous bone. One hundred and sixty cylindrical cancellous bone specimens were produced from 40 normal proximal tibiae from 40 donors, aged 16–85 years. These specimens were micro-computed tomography (micro-CT) scanned, and microstructural properties were determined. The specimens were then tested in compression to obtain Young's modulus.

The degree of anisotropy, mean marrow space volume, and bone surface-to-volume ratio increased significantly with age. Bone volume fraction, mean trabecular volume, and bone surface density decreased significantly with age. Connectivity did not have a general relationship with age. Bone volume fraction together with anisotropy best predicted Young's modulus. Age-related changes in the microstructural properties had the same trends for both medial and lateral condyles of the tibia. The observed increase of anisotropy and constant connectivity suggest a bone remodeling mechanism that may reorient trabecular volume orientation in aging tibial cancellous bone. The aging trabeculae align more strongly to the primary direction - parallel to the tibial longitudinal loading axis.
Links

DOI: 10.1016/S0736-0266(01)00132-2

PubMed: 12038639

WoS: 000175621300030
History

Online: 2006-01-01

Cited Works (26)

Year	Entry
1985	Hvid I, Hansen SL. Trabecular bone strength patterns at the proximal tibial epiphysis. J Orthop Res. 1985;3(4):464-472.
1993	Goldstein SA, Goulet R, McCubbrey D. Measurement and significance of three-dimensional architecture to the mechanical integrity of trabecular bone. Calcif Tiss Int. February 1993;53(suppl 1):S127-S133.
1989	Mosekilde L. Sex differences in age-related loss of vertebral trabecular bone mass and structure—biomechanical consequences. Bone. 1989;10(6):425-432.
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.
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.
1999	Kabel J, Odgaard A, van Rietbergen B, Huiskes R. Connectivity and the elastic properties of cancellous bone. Bone. 1999;24(2):115-120.
1993	Martin B. Aging and strength of bone as a structural material. Calcif Tiss Int. February 1993;53(suppl 1):S34-S40.
1985	Kleerekoper M, Villanueva AR, Stanciu J, Rao DS, Parfitt AM. The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif Tiss Int. 1985;37(6):594-597.
1994	Goulet RW, Goldstein SA, Ciarelli MJ, Kuhn JL, Brown MB, Feldkamp LA. The relationship between the structural and orthogonal compressive properties of trabecular bone. J Biomech. April 1994;27(4):375-389.
1987	Aaron JE, Makins NB, Sagreiya K. The microanatomy of trabecular bone loss in normal aging men and women. Clin Orthop Relat Res. February 1987;215:260-271.
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.
1991	Ciarelli MJ, Goldstein SA, Kuhn JL, Cody DD, Brown MB. Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography. J Orthop Res. May 1991;9(5):674-682.
1998	Kinney JH, Ladd AJC. The relationship between three-dimensional connectivity and the elastic properties of trabecular bone. J Bone Miner Res. May 1998;13(5):839-845.
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.
1990	Hodgskinson R, Currey JD. The effect of variation in structure on the Young's modulus of cancellous bone: a comparison of human and non-human material. Proc Inst Mech Eng Part H-J Eng Med. 1990;204(2):115-121.
1983	Parfitt AM, Mathews CH, Villanueva AR, Kleerekoper M, Frame B, Rao DS. Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis: implications for the microanatomic and cellular mechanisms of bone loss. J Clin Invest. October 1983;72(4):1396-1409.
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.
1990	Turner CH, Cowin SC, Rho JY, Ashman RB, Rice JC. The fabric dependence of the orthotropic elastic constants of cancellous bone. J Biomech. 1990;23(6):549-561.
1988	Mosekilde L. Age-related changes in vertebral trabecular bone architecture—assessed by a new method. Bone. 1988;9(4):247-250.
1997	Odgaard A, Kabel J, van Rietbergen B, Dalstra M, Huiskes R. Fabric and elastic principal directions of cancellous bone are closely related. J Biomech. 1997;30(5):487-495.
1998	Van Rietbergen B, Odgaard A, Kabel J, Huiskes R. Relationships between bone morphology and bone elastic properties can be accurately quantified using high‐resolution computer reconstructions. J Orthop Res. January 1998;16(1):23-28.
1993	Odgaard A, Gundersen HJG. Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone. March–April 1993;14(2):173-182.
1990	Odgaard A, Jensen EB, Gundersen HJG. Estimation of structural anisotropy based on volume orientation: a new concept. J Microsc (Oxford). February 1990;157(pt 2):149-162.
1997	Odgaard A. Three-dimensional methods for quantification of cancellous bone architecture. Bone. 1997;20(4):315-328.
1997	McCalden RW, McGeough JA, Court-Brown CM. Age-related changes in the compressive strength of cancellous bone: the relative importance of changes in density and trabecular architecture. J Bone Joint Surg. March 1997;79A(3):421-427.
1991	Vesterby A, Mosekilde L, Gundersen HJG, Melsen F, Mosekilde L, Holme K, Sørensen S. Biologically meaningful determinants of the in vitro strength of lumbar vertebrae. Bone. 1991;12(3):219-224.

Cited By (46)

Year	Entry
2015	Lin C-L. A Study of Human and Bovine Trabecular Bones Using Nanoindentation and Quantitative Backscattered Electron Imaging [PhD thesis]. Brisbane, Australia: University of Queensland; 2015.
2007	McDonnell P, McHugh PE, O’Mahoney D. Vertebral osteoporosis and trabecular bone quality. Ann Biomed Eng. February 2007;35(2):170-189.
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.
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.
2009	Mueller TL, van Lenthe GH, Stauber M, Gratzke C, Eckstein F, Müller R. Regional, age and gender differences in architectural measures of bone quality and their correlation to bone mechanical competence in the human radius of an elderly population. Bone. November 2009;45(5):882-891.
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.
2004	Nägele E, Kuhn V, Vogt H, Link TM, Müller R, Lochmüller E-M, Eckstein F. Technical considerations for microstructural analysis of human trabecular bone from specimens excised from various skeletal sites. Calcif Tiss Int. 2004;75(1):15-22.
2011	Burghardt AJ, Link TM, Majumdar S. High-resolution computed tomography for clinical imaging of bone microarchitecture. Clin Orthop Relat Res. August 2011;469:2179-2193.
2013	Chen H, Zhou X, Fujita H, Onozuka M, Kubo K-Y. Age-related changes in trabecular and cortical bone microstructure. Int J Endocrinol. March 18, 2013;2013:213234.
2020	Januddi F, Harun MN, Syahrom A, Bakri A, Alkbir MFM. Effect of including periodic boundary condition on the fatigue behaviour of cancellous bone. Int J Integr Eng. 2020;12(5):70-80.
2008	Nazarian A, Bauernschmitt M, Eberle C, Meier D, Müller R, Snyder BD. Design and validation of a testing system to assess torsional cancellous bone failure in conjunction with time-lapsed micro-computed tomographic imaging. J Biomech. December 5, 2008;41(16):3496-3501.
2021	Bennison MBL, Pilkey AK, Lievers WB. Misalignment error in cancellous bone apparent elastic modulus depends on bone volume fraction and degree of anisotropy. J Biomech Eng. February 2021;143(2):021005.
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.
2005	Gong H, Zhang M, Yeung HY, Qin L. Regional variations in microstructural properties of vertebral trabeculae with aging. J Bone Min Metab. March 2005;23(2):174-180.
2003	David V, Laroche N, Boudignon B, Lafage‐Proust M, Alexandre C, Ruegsegger P, Vico L. Noninvasive in vivo monitoring of bone architecture alterations in hindlimb‐unloaded female rats using novel three‐dimensional microcomputed tomography. J Bone Miner Res. September 2003;18(9):1622-1631.
2005	Thomsen JS, Laib A, Koller B, Prohaska S, Mosekilde L, Gowin W. Stereological measures of trabecular bone structure: comparison of 3D micro computed tomography with 2D histological sections in human proximal tibial bone biopsies. J Microsc (Oxford). 2005;218(2):171-179.
2006	Stauber M, Müller R. Age-related changes in trabecular bone microstructures: global and local morphometry. Osteoporos Int. April 2006;17(4):616-626.
2008	Chen H, Shoumura S, Emura S, Bunai Y. Regional variations of vertebral trabecular bone microstructure with age and gender. Osteoporos Int. October 2008;19(10):1473-1483.
2008	Cui W-Q, Won Y-Y, Baek M-H, Lee D-H, Chung Y-S, Hur J-H, Ma Y-Z. Age-and region-dependent changes in three-dimensional microstructural properties of proximal femoral trabeculae. Osteoporos Int. 2008;19(11):1579-1587.
2010	Chen H, Zhou X, Shoumura S, Emura S, Bunai Y. Age- and gender-dependent changes in three-dimensional microstructure of cortical and trabecular bone at the human femoral neck. Osteoporos Int. April 2010;21(4):627-636.
2006	Sierpowska J, Hakulinen MA, Töyräs J, Day JS, Weinans H, Kiviranta I, Jurvelin JS, Lappalainen R. Interrelationships between electrical properties and microstructure of human trabecular bone. Phys Med Biol. 2006;51(20):5289-5303.
2019	Mondal A, Nguyen C, Ma X, Elbanna AE, Carlson JM. Network models for characterization of trabecular bone. Phys Rev E. April 18, 2019;99(4):042406.
2006	Gong H, Zhang M, Qin L, Lee KKH, Guo X, Shi S-Q. Regional variations in microstructural properties of vertebral trabeculae with structural groups. Spine. January 2006;31(1):24-32.
2017	Saers JPP. Ontogeny and Functional Adaptation of Trabecular Bone in the Human Foot [PhD thesis]. Cambridge, UK: University of Cambridge; July 2017.
2015	Goff M. The Role of Micro and Ultra-Structure in Microdamage Accumulation in Cancellous Bone [PhD thesis]. Ithaca, NY: Cornell University; August 2015.
2004	İnceoğlu S. Failure of Pedicle Screw-Bone Interface: Biomechanics of Pedicle Screw Insertion and Pullout [PhD thesis]. Cleveland State University; December 2004.
2005	Day JS. Bone Quality: The Mechanical Effects of Microarchitecture and Matrix Properties [PhD thesis]. Erasmus University Rotterdam; 2005.
2005	Stauber M. Volumetric Spatial Decomposition of Porous Microstructures: A Framework for Element Based Analysis of Trabecular Bone [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2005.
2008	Nazarian A. Relative Interaction of Material and Structure in Normal and Pathologic Bone [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2008.
2010	Müller T. Bioimaging and Biomechanics of Bone Competence and Implant Stability [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2010.
2010	Wang JL. Effects of Aging and Remodeling on Bone Microdamage Formation [Master's thesis]. Atlanta, GA: Georgia Institute of Technology; December 2010.
2020	Bennison MBL. The Role of Cancellous Bone Architecture in Misalignment and Side Effect Errors [Master's thesis]. Sudbury, ON: Laurentian University; 2020.
2018	Carlson AK. Characterization of Metabolic Changes in Osteoarthritis Using Global Metabolomic Profiling [PhD thesis]. Bozeman, MT: Montana State University; July 2018.
2020	O’Sullivan LM. Time-Sequence of Biomechanical Adaption in Trabecular Tissue During Estrogen Deficiency [PhD thesis]. National University of Ireland Galway; March 2020.
2022	Khakpour S. Multi-Component Finite Element Analysis of Low- Energy Acetabular Fracture: Computational Study of Pelvic Girdle Fracture Mechanism [PhD thesis]. University of Oulu; 2022.
2012	Tozzi G. In Vitro Studies of Bone-Cement Interface and Related Work on Cemented Acetabular Replacement [PhD thesis]. Portsmouth, England: University of Portsmouth; May 29, 2012.
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.
2020	Dreyer CH. Enhance Bone Regeneration and Implant Fixation by Novel Substitute With Combined Angiogenic and Osteogenic Factors in Animal Models [PhD thesis]. University of Southern Denmark (SDU); 2020.
2011	Su A. The Functional Morphology of Subchondral and Trabecular Bone in the Hominoid Tibiotalar Joint [PhD thesis]. Stony Brook, NY: Stony Brook University; August 2011.
2002	Morgan EF-i. The Dependence on Anatomic Site of Trabecular Bone Structure-Function Relationships [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2002.
2003	Fox JC. Biomechanics of the Proximal Femur: Role of Bone Distribution and Architecture [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2003.
2012	Evdokimenko E. Investigation Into Mechanical Properties of Bone and Its Main Constituents [PhD thesis]. San Diego (UCSD), University of California; 2012.
2007	Rossello RA. Cell-to-Cell Communication as a Strategy to Regenerate Three-Dimensional Tissue [PhD thesis]. University of Michigan; 2007.
2016	Lin C-l. A Study of Human and Bovine Trabecular Bones Using Nanoindentation and Quantitative Backscattered Electron Imaging [PhD thesis]. Brisbane, Australia: University of Queensland; 2016.
2013	Mecke D. Probabilistic Analysis of the Microstructure of Human Trabecular Bone With High and Low Volume Fractions [Master's thesis]. San Antionio, TX: University of Texas at San Antonio; December 2013.
2011	Lala D. Determinants of Fracture Risk Among Individuals With Spinal Cord Injury: A Case Control Study [Master's thesis]. University of Waterloo; 2011.