Structural parameters and mechanical strength of cancellous bone in the femoral head in osteoarthritis do not depend on age

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Perilli, E.¹; Baleani, M.¹; Öhman, C.¹; Baruffaldi, F.¹; Viceconti, M.¹

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

©2007 Elsevier Inc. All rights reserved.

Affiliations

¹Laboratorio di Tecnologia Medica, Istituti Ortopedici Rizzoli, Via di Barbiano 1/10, 40136 Bologna, Italy
Abstract and keywords

For normal bone, aging has been associated with a decrease of both density and failure strength, and with the development of pathologies such as osteoporosis. Conversely, it has been reported that another common disease, osteoarthritis, may alter these age-related changes in cancellous bone, suggesting that it may have a protective role against osteoporosis and the correspondent fracture risk. It was reported that in the principal compressive region of the femoral head in osteoarthritis the bone density does not depend on age. However, it is not clear if this independence on age of the cancellous bone density corresponds also to a reduced dependence on age of the strength to failure.

The present work examined cancellous bone from the principal compressive region of the femoral head of 37 patients having severe osteoarthritis. The aim was (1) to investigate the dependence on age of both the structural parameters and the ultimate stress and (2) to investigate the relationships between the ultimate stress and the structural parameters. Using X-ray microcomputed tomography, three-dimensional structural parameters, such as bone volume fraction, direct trabecular thickness and structure model index were calculated. Then the specimens were compressed to failure to determine the ultimate stress.

It was found that none of the investigated structural parameters did depend on age, and also the ultimate stress did not depend on age (p > 0.05 for all regressions on age). In addition, the ultimate stress was significantly correlated with the structural parameters, primary with the minimum bone volume fraction and the average bone volume fraction (R2 = 0.95 and R2 = 0.84, respectively).

These findings show that severe osteoarthritis or a related factor may change the age dependences of both the structural parameters and the mechanical properties usually reported for normal cancellous bone. These results suggest for this pathology to have a protective role against the age-related decrease in density, the age-related deterioration of the microarchitecture and the age-related decrease of the failure strength for the cancellous bone in the principal compressive region of the human femoral head.

Keywords: Cancellous bone microarchitecture; Osteoarthritis; Strength; Age variation; MicroCT scanning
Links

DOI: 10.1016/j.bone.2007.07.014

PubMed: 17707709

WoS: 000250528900003
History

Received: 2007-05-17

Revised: 2007-07-04

Accepted: 2007-07-24

Online: 2007-08-01

Cited Works (54)

Year	Entry
1985	Gibson LJ. The mechanical behaviour of cancellous bone. J Biomech. 1985;18(5):317-328.
2000	McCreadie BR, Goldstein SA. Biomechanics of fracture: is bone mineral density sufficient to assess risk? J Bone Miner Res. December 2000;15(12):2305-2308.
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.
1997	Li B, Aspden RM. Composition and mechanical properties of cancellous bone from the femoral head of patients with osteoporosis or osteoarthritis. J Bone Miner Res. 1997;12(4):641-651.
1997	Li B, Aspden R. Material properties of bone from the femoral neck and calcar femorale of patients with osteoporosis or osteoarthritis. Osteoporos Int. September 1997;7(5):450-456.
2000	Ciarelli TE, Fyhrie DP, Schaffler MB, Goldstein SA. Variations in three‐dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res. 2000;15(1):32-40.
1997	Odgaard A. Three-dimensional methods for quantification of cancellous bone architecture. Bone. 1997;20(4):315-328.
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.
2007	Perilli E, Baruffaldi F, Visentin M, Bordini B, Traina F, Cappello A, Viceconti M. MicroCT examination of human bone specimens: effects of polymethylmethacrylate embedding on structural parameters. J Microsc (Oxford). 2007;225(pt 2):192-200.
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.
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.
2003	Morgan EF, Bayraktar HH, Keaveny TM. Trabecular bone modulus–density relationships depend on anatomic site. J Biomech. July 2003;36(7):897-904.
1988	Turner CH, Cowin SC. Errors induced by off-axis measurement of the elastic properties of bone. J Biomech Eng. August 1988;110(3):213-215.
2006	Nazarian A, Stauber M, Zurakowski D, Snyder BD, Müller R. The interaction of microstructure and volume fraction in predicting failure in cancellous bone. Bone. December 2006;39(6):1196-1202.
1997	Hildebrand T, Rüegsegger P. Quantification of bone microarchitecture with the structure model index. Comput Methods Prog Biomed. 1997;1(1):15-23.
1998	Kopperdahl DL, Keaveny TM. Yield strain behavior of trabecular bone. J Biomech. July 1998;31(7):601-608.
1991	Slemenda CW, Christian JC, Williams CJ, Norton JA, Johnston CC Jr. Genetic determinants of bone mass in adult women: a reevaluation of the twin model and the potential importance of gene interaction on heritability estimates. J Bone Miner Res. June 1991;6(6):561-567.
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.
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.
1994	Keller TS. Predicting the compressive mechanical behavior of bone. J Biomech. September 1994;27(9):1159-1168.
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.
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.
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.
2001	Guo XE. Mechanical properties of cortical and cancellous bone tissue. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:10-1–10-23.
2000	Dempster DW. The contribution of trabecular architecture to cancellous bone quality. J Bone Miner Res. January 2000;15(1):20-23.
1996	Müller R, Hahn M, Vogel M, Delling G, Rüegsegger P. Morphometric analysis of noninvasively assessed bone biopsies: comparison of high-resolution computed tomography and histologic sections. Bone. March 1996;18(3):215-220.
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.
2006	Teo JCM, Si-Hoe KM, Keh JEL, Teoh SH. Relationship between CT intensity, micro-architecture and mechanical properties of porcine vertebral cancellous bone. Clin Biomech (Bristol, Avon). March 2006;21(3):235-244.
1970	Singh M, Nagrath AR, Maini PS. Changes in trabecular pattern of the upper end of the femur as an index of osteoporosis. J Bone Joint Surg. April 1970;52A(3):457-467.
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.
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.
1983	Martens M, Van Audekercke R, Delport P, De Meester P, Mulier JC. The mechanical characteristics of cancellous bone at the upper femoral region. J Biomech. 1983;16(12):971-983.
1991	Røhl L, Larsen E, Linde F, Odgaard A, Jørgensen J. Tensile and compressive properties of cancellous bone. J Biomech. 1991;24(12):1143-1149.
1998	Majumdar S. A review of magnetic resonance (MR) imaging of trabecular bone micro-architecture: contribution to the prediction of biomechanical properties and fracture prevalence. Technol Health Care. 1998;6(5-6):321-327.
2007	Öhman C, Baleani M, Perilli E, Dall’Ara E, Tassani S, Baruffaldi F, Viceconti M. Mechanical testing of cancellous bone from the femoral head: experimental errors due to off-axis measurements. J Biomech. 2007;40(11):2426-2433.
1997	Hildebrand T, Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc (Oxford). 1997;185(1):67-75.
1970	Galante J, Rostoker W, Ray RD. Physical properties of trabecular bone. Calcif Tiss Res. 1970;5(1):236-246.
1984	Feldkamp LA, Davis LC, Kress JW. Practical cone-beam algorithm. J Opt Soc Am. 1984;A1(6):612-619.
2004	Kaneko TS, Bell JS, Pejcic MR, Tehranzadeh J, Keyak JH. Mechanical properties, density and quantitative CT scan data of trabecular bone with and without metastases. J Biomech. April 2004;37(4):523-530.
1989	Linde F, Hvid I. The effect of constraint on the mechanical behaviour of trabecular bone specimens. J Biomech. 1989;22(5):485-490.
1998	Fazzalari NL, Forwood MR, Smith K, Manthey BA, Herreen P. Assessment of cancellous bone quality in severe osteoarthrosis: bone mineral density, mechanics, and microdamage. Bone. 1998;22(4):381-388.
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.
1994	Keyak JH, Lee IY, Skinner HB. Correlations between orthogonal mechanical properties and density of trabecular bone: use of different densitometric measures. J Biomed Mater Res. November 1994;A28(11):1329-1336.
1991	Odgaard A, Linde F. The underestimation of Young's modulus in compressive testing of cancellous bone specimens. J Biomech. 1991;24(8):691-698.
2005	Mittra E, Rubin C, Qin Y-X. Interrelationship of trabecular mechanical and microstructural properties in sheep trabecular bone. J Biomech. June 2005;38(6):1229-1237.
2001	Morgan EF, Keaveny TM. Dependence of yield strain of human trabecular bone on anatomic site. J Biomech. 2001;34(5):569-577.
1998	Majumdar S, Kothari M, Augat P, Newitt DC, Link TM, Lin JC, Lang T, Lu Y, Genant HK. High-resolution magnetic resonance imaging: three-dimensional trabecular bone architecture and biomechanical properties. Bone. May 1998;22(5):445-454.
2002	Fazzalari NL, Kuliwaba JS, Forwood MR. Cancellous bone microdamage in the proximal femur: influence of age and osteoarthritis on damage morphology and regional distribution. Bone. December 2002;31(6):697-702.
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.
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.
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.
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.
1993	Keaveny TM, Borchers RE, Gibson L, Hayes WC. Trabecular bone modulus and strength can depend on specimen geometry. J Biomech. August 1993;26(8):991-995.

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2011	Tassani S, Particelli F, Perilli E, Traina F, Baruffaldi F, Viceconti M. Dependence of trabecular structure on bone quantity: a comparison between osteoarthritic and non-pathological bone. Clin Biomech (Bristol, Avon). July 2011;26:632-639.
2015	Salmon PL, Ohlsson C, Shefelbine SJ, Doube M. Structure model index does not measure rods and plates in trabecular bone. Front Endocrinol (Lausanne). 2015;6:162.
2010	Tassani S, Öhman C, Baleani M, Baruffaldi F, Viceconti M. Anisotropy and inhomogeneity of the trabecular structure can describe the mechanical strength of osteoarthritic cancellous bone. J Biomech. April 19, 2010;43(6):1160-1166.
2011	Dall'Ara E, Öhman C, Baleani M, Viceconti M. Reduced tissue hardness of trabecular bone is associated with severe osteoarthritis. J Biomech. May 17, 2011;44(8):1593-1598.
2012	Tassani S, Matsopoulos GK, Baruffaldi F. 3D identification of trabecular bone fracture zone using an automatic image registration scheme: a validation study. J Biomech. July 26, 2012;45(11):2035-2040.
2014	Roberts BC, Perilli E, Reynolds KJ. Application of the digital volume correlation technique for the measurement of displacement and strain fields in bone: a literature review. J Biomech. March 21, 2014;47(5):923-934.
2014	Yamada S, Tadano S, Fukuda S. Nanostructure and elastic modulus of single trabecula in bovine cancellous bone. J Biomech. November 7, 2014;47(14):3482-3487.
2014	Chen Y, Pani M, Taddei F, Mazzà C, Li X, Viceconti M. Large-scale finite element analysis of human cancellous bone tissue micro computer tomography data: a convergence study. J Biomech Eng. October 2014;136(10):101013.
2020	Chu L, Liu X, He Z, Han X, Yan M, Qu X, Li X, Yu Z. Articular cartilage degradation and aberrant subchondral bone remodeling in patients with osteoarthritis and osteoporosis. J Bone Miner Res. March 2020;35(3):505-515.
2020	Fleps I, Bahaloo H, Zysset PK, Ferguson SJ, Pálsson H, Helgason B. Empirical relationships between bone density and ultimate strength: a literature review. J Mech Behav Biomed Mater. October 2020;110:103866.
2020	Knowles NK, Kusins J, Columbus MP, Athwal GS, Ferreira LM. Morphological and apparent‐level stiffness variations between normal and osteoarthritic bone in the humeral head. J Orthop Res. March 2020;38(3):503-509.
2022	Kusins J, Knowles N, Martensson N, Columbus MP, Athwal GS, Ferreira LM. Full-field experimental analysis of the influence of microstructural parameters on the mechanical properties of humeral head trabecular bone. J Orthop Res. September 2022;40(9):2048-2056.
2020	Ryan MK, Oliviero S, Costa MC, Wilkinson JM, Dall’Ara E. Heterogeneous strain distribution in the subchondral bone of human osteoarthritic femoral heads, measured with digital volume correlation. Materials. 2020;13(20):4619.
2011	Yan Y-B, Qi W, Wang J, Liu L-F, Teo E-C, Tianxia Q, Ba J-j, Lei W. Relationship between architectural parameters and sample volume of human cancellous bone in micro-CT scanning. Med Eng Phys. July 2011;33(6):764-769.
2016	Guang Y. Characterization of Bone and Bone Marrow Lesions in the Osteoarthritic Hip [Master's thesis]. Boston University; 2016.
2011	Ahmed F. Multiscale Quantitative Imaging of Human Femoral Heads Using X-Ray Microtomography [PhD thesis]. Queen Mary University of London; 2011.
2023	Branni MG. Constitutive Models of Bone: The Human Femur [PhD thesis]. Queensland University of Technology; 2023.
2012	Dall'Ara E. QCT Based Finite Element Models of the Human Vertebra and Femur: Validation With Experiments and Comparison With Bone Densitometry [PhD thesis]. Vienna University of Technology; October 2012.
2019	Knowles NK. Improving Material Mapping in Glenohumeral Finite Element Models: A Multi-Level Evaluation [PhD thesis]. University of Western Ontario; 2019.
2021	Kusins J. A Multi-Level Mechanical Assessment of the Shoulder Coupled With Evaluation of Upper Extremity Predictive Finite Element Models [PhD thesis]. University of Western Ontario; 2021.