Three-dimensional microstructural analysis of human trabecular bone in relation to its mechanical properties

wbldb

Uchiyama, T.¹; Tanizawa, T.¹; Muramatsu, H.²; Endo, N.¹; Takahashi, H. E.¹; Hara, T.³

Three-dimensional microstructural analysis of human trabecular bone in relation to its mechanical properties

Bone. 1999;25(4):487-491

Affiliations

¹Department of Orthopedic Surgery, Niigata University School of Medicine, Niigata, Japan

²Graduate School of Science and Technology, Niigata University, Niigata, Japan

³Department of Mechanical Engineering, Niigata University School of Engineering, Niigata, Japan
Abstract

The purpose of this preliminary study is to explore the relationship between elastic modulus, bone mineral density (BMD), and trabecular microstructure in three dimensions. Twenty cubes of trabecular bone were processed from two lumbar vertebrae obtained from one individual. The BMD of each cube was measured by dual-energy X-ray absorptiometry and peripheral quantitative computed tomography. Each cube was serially scanned by microcomputed tomography to produce three-dimensional data sets. By analyzing these data sets, three-dimensional trabecular microstructural indices of connectivity density and fractal dimension were calculated as well as histomorphometric parameters. The cubes were tested mechanically in a nondestructive manner for measurement of their elastic modulus. This preliminary study showed that: (1) bone mass index is correlated with mechanical properties, with coefficients of correlation ranging from 0.552 to 0.601; and (2) when controlling for BMD, no association could be detected between measures of structural complexity (connectivity density and fractal dimension) and elastic modulus in the craniocaudal direction of human vertebral bodies.
Links

DOI: 10.1016/S8756-3282(99)00188-X

PubMed: 10511117

WoS: 000082661000014
History

Received: 1998-07-22

Revised: 1999-06-11

Accepted: 1999-06-14

Online: 1999-09-10

Cited Works (28)

Year	Entry
1986	Garrahan NJ, Mellish RWE, Compston JE. A new method for the two-dimensional analysis of bone structure in human iliac crest biopsies. J Microsc (Oxford). June 1986;142(3):341-349.
1996	Rüegsegger P, Koller B, Müller R. A microtomographic system for the nondestructive evaluation of bone architecture. Calcif Tiss Int. 1996;58(1):24-29.
1990	Odgaard A, Andersen K, Melsen F, Gundersen HJG. A direct method for fast three-dimensional serial reconstruction. J Microsc (Oxford). September 1990;159(pt 3):335-342.
1978	Singh I. The architecture of cancellous bone. J Anat. October 1978;127(2):305-310.
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.
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.
1997	Mori S, Harruff R, Ambrosius W, Burr DB. Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures. Bone. December 1997;21(6):521-526.
1995	Kinney JH, Lane NE, Haupt DL. In vivo, three‐dimensional microscopy of trabecular bone. J Bone Miner Res. February 1995;10(2):264-270.
1993	Faulkner KG, Cummings SR, Black D, Palermo L, Glüer C, Genant HK. Simple measurement of femoral geometry predicts hip fracture: the study of osteoporotic fractures. J Bone Miner Res. September 1993;8(10):1211-1217.
1997	Uchiyama T, Tanizawa T, Muramatsu H, Endo N, Takahashi HE, Hara T. A morphometric comparison of trabecular structure of human ilium between microcomputed tomography and conventional histomorphometry. Calcif Tiss Int. December 1997;61(6):493-498.
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.
1969	Currey JD. The mechanical consequences of variation in the mineral content of bone. J Biomech. March 1969;2(1):1-11.
1987	Linde F, Hvid I. Stiffness behaviour of trabecular bone specimens. J Biomech. 1987;20(1):83-89.
1988	Bergot C, Laval-Jeantet A-M, Prêteux F, Meunier A. Measurement of anisotropic vertebral trabecular bone loss during aging by quantitative image analysis. Calcif Tiss Int. September 1988;43(3):143-149.
1987	Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: standardization of nomenclature, symbols, and units: report of the ASBMR histomorphometry nomenclature committee. J Bone Miner Res. December 1987;2(6):595-610.
1998	Lane NE, Thompson JM, Haupt D, Kimmel DB, Modin G, Kinney JH. Acute changes in trabecular bone connectivity and osteoclast activity in the ovariectomized rat in vivo. J Bone Miner Res. February 1998;13(2):229-236.
1998	Boyde A, Compston JE, Reeve J, Bell KL, Noble BS, Jones SJ, Loveridge N. Effect of estrogen suppression on the mineralization density of iliac crest biopsies in young women as assessed by backscattered electron imaging. Bone. March 1998;22(3):241-250.
1988	Mosekilde L. Age-related changes in vertebral trabecular bone architecture—assessed by a new method. Bone. 1988;9(4):247-250.
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.
1992	Hahn M, Vogel M, Pompesius-Kempa M, Delling G. Trabecular bone pattern factor: a new parameter for simple quantification of bone microarchitecture. Bone. 1992;13(4):327-330.
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.
1969	Rockoff SD, Sweet E, Bleustein J. The relative contribution of trabecular and cortical bone to the strength of human lumbar vertebrae. Calcif Tiss Res. December 1969;3(1):163-175.
1997	Odgaard A. Three-dimensional methods for quantification of cancellous bone architecture. Bone. 1997;20(4):315-328.
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.
1997	Burr DB, Forwood MR, Fyhrie DP, Martin RB, Schaffler MB, Turner CH. Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res. January 1997;12(1):6-15.
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.
1998	Thomsen JS, Ebbesen EN, Mosekilde L. Relationships between static histomorphometry and bone strength measurements in human iliac crest bone biopsies author links open overlay panel. Bone. February 1998;22(2):153-163.

Cited By (15)

Year	Entry
2010	Cichański A, Nowicki K, Mazurkiewicz A, Topoliński T. Investigation of statistical relationships between quantities describing bone architecture, its fractal dimensions and mechanical properties. Acta Bioeng Biomech. 2010;12(4):69-77.
2004	Hellmich C, Ulm F-J, Dormieux L. Can the diverse elastic properties of trabecular and cortical bone be attributed to only a few tissue-independent phase properties and their interactions? arguments from a multiscale approach. Biomech Model Mechanobiol. June 2004;2(4):219-238.
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.
2008	Chappard C, Marchadier A, Benhamou CL. Side-to-side and within-side variability of 3D bone microarchitecture by conventional micro-computed tomography of paired iliac crest biopsies. Bone. July 2008;43(1):203-208.
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.
2008	Chappard C, Marchadier A, Benhamou L. Interindividual and intraspecimen variability of 3-D bone microarchitectural parameters in iliac crest biopsies imaged by conventional micro-computed tomography. J Bone Min Metab. 2008;26(5):506-513.
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.
2016	Boskey AL, Donnelly E, Boskey E, Spevak L, Ma Y, Zhang W, Lappe J, Recker RR. Examining the relationships between bone tissue composition, compositional heterogeneity, and fragility fracture: a matched case-controlled FTIRI study. J Bone Miner Res. May 2016;31(5):1070-1081.
2003	van Ruijven LJ, Giesen EBW, Farella M, van Eijden TMGJ. Prediction of mechanical properties of the cancellous bone of the mandibular condyle. J Dent Res. October 2003;82(10):819-823.
2020	Aggleton J. First-Hand Experience: A Methodology for Exploring Bone Architecture [PhD thesis]. Bristol, UK: University of Bristol; January 2020.
2005	Day JS. Bone Quality: The Mechanical Effects of Microarchitecture and Matrix Properties [PhD thesis]. Erasmus University Rotterdam; 2005.
2010	Rami E. Automated Design of Trabecular Structures [PhD thesis]. Loughborough, UK: Loughborough University; February 2010.
2005	Espinoza Orias AA. The Relationship Between the Mechanical Anisotropy of Human Cortical Bone Tissue and Its Microstructure [PhD thesis]. University of Notre Dame; April 2005.
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.
2020	Belda González R. Mechanical and Morphometric Characterization of Cancellous Bone [PhD thesis]. Universität Politècnica de València; March 2020.