Dependence of mechanical properties of trabecular bone on plate-rod microstructure determined by individual trabecula segmentation (ITS)

Zhou, Bin; Liu, X. Sherry; Wang, Ji; Lu, X. Lucas; Fields, Aaron J.; Guo, X. Edward

Affiliations

¹Bone Bioengineering Laboratory, Department of Biomedical Engineering, Columbia University, New York, New York, U.S.A.

²McKay Orthopaedic Research Laboratory, University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A.

³Cartilage Bioengineering Laboratory, Department of Mechanical Engineering, University of Delaware, Newark, Delaware, U.S.A.

⁴Depart of Orthopaedic Surgery, University of California, San Francisco, California, U.S.A.

⁵Orthopaedic Biomechanics Laboratory, Department of Mechanical Engineering, University of California, Berkeley, California, U.S.A.

Abstract and keywords

Individual trabecula segmentation (ITS) technique can decompose the trabecular bone network into individual trabecular plates and rods and is capable of quantifying the plate/rod-related microstructural characteristics of trabecular bone. This novel technique has been shown to be able to provide in-depth insights into micromechanics and failure mechanisms of human trabecular bone, as well as to distinguish the fracture status independent of area bone mineral density in clinical applications. However, the plate/rod microstructural parameters from ITS have never been correlated to experimentally determined mechanical properties of human trabecular bone. In this study, on-axis cylindrical trabecular bone samples from human proximal tibia (n=30), vertebral body (n=10), and proximal femur (n=30) were harvested, prepared, scanned using micro computed-tomography (μCT), analyzed with ITS and mechanically tested. Regression analyses showed that the plate bone volume fraction (pBV/TV) and axial bone volume fraction (aBV/TV) calculated by ITS analysis correlated the best with elastic modulus (R²=0.96-0.97) and yield strength (R²=0.95-0.96). Trabecular plate-related microstructural parameters correlated highly with elastic modulus and yield strength, while most rod-related parameters were found inversely and only moderately correlated with the mechanical properties. In addition, ITS analysis also identified that trabecular bone at human femoral neck has the highest trabecular plate-related parameters while the other sites are similar with each other in terms of plate-rod microstructure.

Keywords: Individual trabecula segmentation; Trabecular bone; Mechancial properties; Microstructure

Links

DOI: 10.1016/j.jbiomech.2013.11.039.

PubMed: 24360196

PubMedCentral: PMC3925244

History

Accepted: 2013-11-24

Cited Works (19)

Year	Entry
1997	Saha PK, Chaudhuri BB, Dutta Majumder D. A new shape preserving parallel thinning algorithm for 3D digital images. Pattern Recognit. December 1997;30(2):1939-1955.
1997	Keaveny TM, Pinilla TP, Crawford RP, Kopperdahl DL, Lou A. Systematic and random errors in compression testing of trabecular bone [published correction appears in J Orthop Res. 1995;17(1):151]. J Orthop Res. 1997;15(1):101-110.
1994	Keaveny TM, Guo XE, Wachtel EF, McMahon TA, Hayes WC. Trabecular bone exhibits fully linear elastic behavior and yields at low strains. J Biomech. 1994;27(9):1127-1136.
2001	Keaveny TM, Morgan EF, Niebur GL, Yeh OC. Biomechanics of trabecular bone. Annu Rev Biomed Eng. 2001;3:307-333.
1994	Keaveny TM, Wachtel EF, Ford CM, Hayes WC. Differences between the tensile and compressive strengths of bovine tibial trabecular bone depend on modulus. J Biomech. 1994;27(9):1137-1146.
1996	Amling M, Herden S, Pösl M, Hahn M, Ritzel H, Delling G. Heterogeneity of the skeleton: comparison of the trabecular microarchitecture of the spine, the iliac crest, the femur, and the calcaneus. J Bone Miner Res. January 1996;11(1):36-45.
2013	Thomsen JS, Niklassen AS, Ebbesen EN, Brüel A. Age-related changes of vertical and horizontal lumbar vertebral trabecular 3D bone microstructure is different in women and men. Bone. November 2013;57(1):47-55.
2008	Liu XS, Sajda P, Saha PK, Wehrli FW, Bevill G, Keaveny TM, Guo XE. Complete volumetric decomposition of individual trabecular plates and rods and its morphological correlations with anisotropic elastic moduli in human trabecular bone. J Bone Miner Res. February 2008;23(2):223-235.
2006	Liu XS, Sajda P, Saha PK, Wehrli FW, Guo XE. Quantification of the roles of trabecular microarchitecture and trabecular type in determining the elastic modulus of human trabecular bone. J Bone Miner Res. October 2006;21(10):1608-1617.
1999	Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res. July 1999;14(7):1167-1174.
2010	Shi X, Liu XS, Wang X, Guo XE, Niebur GL. Effects of trabecular type and orientation on microdamage susceptibility in trabecular bone. Bone. May 2010;46(5):1260-1266.
2008	Mittra E, Rubin C, Gruber B, Qin Y-X. Evaluation of trabecular mechanical and microstructural properties in human calcaneal bone of advanced age using mechanical testing, μCT, and DXA. J Biomech. 2008;41(2):368-375.
2004	Morgan E, Bayraktar H, Yeh O, Majumdar S, Burghardt A, Keaveny T. Contribution of inter-site variations in architecture to trabecular bone apparent yield strains. J Biomech. 2004;37(9):1413-1420.
2001	Morgan EF, Keaveny TM. Dependence of yield strain of human trabecular bone on anatomic site. J Biomech. 2001;34(5):569-577.
2007	Akhter MP, Lappe JM, Davies KM, Recker RR. Transmenopausal changes in the trabecular bone structure. Bone. July 2007;41(1):111-116.
2003	Morgan EF, Bayraktar HH, Keaveny TM. Trabecular bone modulus–density relationships depend on anatomic site. J Biomech. July 2003;36(7):897-904.
2010	Liu XS, Cohen A, Shane E, Stein E, Rogers H, Kokolus SL, Yin PT, McMahon DJ, Lappe JM, Recker RR, Guo XE. Individual trabeculae segmentation (ITS)–based morphological analysis of high‐resolution peripheral quantitative computed tomography images detects abnormal trabecular plate and rod microarchitecture in premenopausal women with idiopathic osteoporosis. J Bone Miner Res. July 2010;25(7):1496-1505.
2002	Thomsen JS, Ebbesen EN, Mosekilde L. Age-related differences between thinning of horizontal and vertical trabeculae in human lumbar bone as assessed by a new computerized method. Bone. July 2002;31(1):136-142.
2012	Liu XS, Stein EM, Zhou B, Zhang CA, Nickolas TL, Cohen A, Thomas V, McMahon DJ, Cosman F, Nieves J, Shane E, Guo XE. Individual trabecula segmentation (ITS)‐based morphological analyses and microfinite element analysis of HR‐pQCT images discriminate postmenopausal fragility fractures independent of DXA measurements. J Bone Miner Res. February 2012;27(2):263-272.

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Year	Entry
2015	Wang J, Zhou B, Liu XS, Fields AJ, Sanyal A, Shi X, Adams M, Keaveny TM, Guo XE. Trabecular plates and rods determine elastic modulus and yield strength of human trabecular bone. Bone. March 2015;72:71-80.
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.
2016	Fan R, Gong H, Zhang X, Liu J, Jia Z, Zhu D. Modeling the mechanical consequences of age-related trabecular bone loss by XFEM simulation. Computat Math Methods Med. 2016;2016:3495152.
2015	Prot M, Saletti D, Pattofatto S, Bousson V, Laporte S. Links between mechanical behavior of cancellous bone and its microstructural properties under dynamic loading. J Biomech. February 5, 2015;48(3):498-503.
2016	Prot M, Cloete TJ, Saletti D, Laporte S. The behavior of cancellous bone from quasi-static to dynamic strain rates with emphasis on the intermediate regime. J Biomech. May 3, 2016;49(7):1050-1057.
2021	Feng C, Wang L, Xu P, Chu Z, Yao J, Sun W, Gong H, Zhang X, Li Z, Fan Y. Microstructural and mechanical evaluations of region segmentation methods in classifications of osteonecrosis. J Biomech. April 15, 2021;119:110208.
2015	Maquer G, Musy SN, Wandel J, Gross T, Zysset PK. Bone volume fraction and fabric anisotropy are better determinants of trabecular bone stiffness than other morphological variables. J Bone Miner Res. June 2015;30(6):1000-1008.
2022	Sacher SE, Hunt HB, Lekkala S, Lopez KA, Potts J, Heilbronner AK, Stein EM, Hernandez CJ, Donnelly E. Distributions of microdamage are altered between trabecular rods and plates in cancellous bone from men with type 2 diabetes mellitus. J Bone Miner Res. April 2022;37(4):740-752.
2015	Thomsen JS, Jensen MV, Niklassen AS, Ebbesen EN, Brüel A. Age-related changes in vertebral and iliac crest 3D bone microstructure: differences and similarities. Osteoporos Int. January 2015;26(1):219-228.
2019	Popp KL, Xu C, Yuan A, Hughes JM, Unnikrishnan G, Reifman J, Bouxsein ML. Trabecular microstructure is influenced by race and sex in Black and White young adults. Osteoporos Int. January 2019;30(1):201-209.
2015	Zhou B. Bone Quality Assessment Using High Resolution Peripheral Quantitative Computed Tomography (HR-PQCT) [PhD thesis]. Columbia University; 2015.
2016	Wang J. Plate-Rod Microstructural Modeling for Accurate and Fast Assessment of Bone Strength [PhD thesis]. Columbia University; 2016.
2017	Yu Y. Contributions of Anisotropic and Heterogeneous Tissue Modulus to Apparent Trabecular Bone Mechanical Properties [PhD thesis]. Columbia University; 2017.
2020	Robinson ST. Bone Mechanobiology of Modeling and Remodeling and the Effect of Hematopoietic Lineage Cells [PhD thesis]. Columbia University; 2020.
2021	Golman M. Toughening Mechanisms for the Attachment of Architectured Materials: The Mechanics of the Tendon Enthesis [PhD thesis]. Columbia University; 2021.
2017	Matheny JB. Interactions Between Bone Remodeling and Microdamage in Cancellous Bone [PhD thesis]. Ithaca, NY: Cornell University; August 2017.
2018	Hunt HB. Characterization of Material Properties, Microarchitecture, and Mechanics of Bone from Subjects With Type 2 Diabetes Mellitus [PhD thesis]. Ithaca, NY: Cornell University; December 2018.
2021	Sacher S. Characterization of Trabecular Morphology, Microdamage Accumulation, and Collagen Crosslinking in Bone Tissue from Individuals With Type II Diabetes Mellitus [Master's thesis]. Ithaca, NY: Cornell University; May 2021.
2019	Du J. Mechanical Adaptation of Human Trabecular Bone: Experimental and Computational Study [PhD thesis]. Loughborough University; 2019.
2022	Mielczarek CB. An Investigation of Local Microarchitecture Topology Changes in Long-Duration Spaceflight [Master's thesis]. Calgary, AB: University of Calgary; November 2022.
2020	Amromanoh OA. An Experimental Study of the Effect of Bone Inorganic-Organic Composition on the Mechanical Properties [Master's thesis]. Winnipeg, MB: University of Manitoba; April 2020.
2017	Kirby ML. Digital Modeling of Trabecular Bones: Structural Analysis and Probabilistic Modeling Techniques [Master's thesis]. San Antionio, TX: University of Texas at San Antonio; August 2017.