Fatigue-caused damage in trabecular bone from clinical, morphological and mechanical perspectives

Mirzaali, M. J.; Libonati, F.; Böhm, C.; Rinaudo, L.; Cesana, B. M.; Ulivieri, F. M.; Vergani, L.

Affiliations

¹Department of Mechanical Engineering, Politecnico di Milano, Via La Masa 1, 20156 Milano, Italy

²Department of Biomechanical Engineering, Faculty of Mechanical, Maritime, and Materials Engineering, Delft University of Technology (TU Delft), Mekelweg 2, 2628 CD, Delft, The Netherlands

³Technologic s.r.l., Torino, Italy

⁴University of Milan, Milan, Italy

⁵Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico, UO Nuclear Medicine-Bone Metabolic Unit, Milano, Italy

Abstract and keywords

Bone quantity and quality are considered the main predictors of bone mechanical properties (i.e., strength and fracture resistance). These factors deal with the morphology and chemical composition of bone and can be assessed by non-invasive techniques such as dual-energy x-ray absorptiometry (DXA), providing the bone mineral density (BMD) and the trabecular bone score (TBS). These parameters, and in particular BMD, are currently used as clinical predictors of fracture risk but do not provide information regarding the fatigue life. Bone is continuously subjected to fatigue loading and fatigue-induced damage can be crucial in fragility fractures. To probe the effect of fatigue-induced damage on bone microarchitecture and elucidate the effect of such damage on the bone clinical parameters, we combined fatigue testing on ex-vivo porcine trabecular bone samples with DXA measurements and μCT imaging. In addition, we performed interrupted cyclic tests at different load levels and measured fatigue-induced damage accumulation in the form of stiffness degradation. We also highlighted the change of clinical and microstructural parameters during the accumulation of fatigue-induced damage in interrupted fatigue tests. Our results suggest that the parameters obtained from the current non-invasive diagnostic protocols (i.e. μCT and DXA) are not able to assess the amount of fatigue-induced damage. This can be due to the fact that such techniques provide global parameters, whereas fatigue-induced damage is a local phenomenon, closely connected to the microarchitecture.

Keywords: Fatigue loading; Bone damage; Trabecular bone score; Bone mineral density; μCT-imaging

Links

DOI: 10.1016/j.ijfatig17ue.2019.105451

WoS: 000510947500021

History

Received: 2019-09-24

Revised: 2019-12-19

Accepted: 2019-12-20

Online: 2019-12-23

Cited Works (47)

Year	Entry
2015	Goff MG, Lambers FM, Nguyen TM, Sung J, Rimnac CM, Hernandez CJ. Fatigue-induced microdamage in cancellous bone occurs distant from resorption cavities and trabecular surfaces. Bone. October 2015;79:8-14.
2010	Fang G, Ji B, Liu XS, Guo XE. Quantification of trabecular bone microdamage using the virtual internal bond model and the individual trabeculae segmentation technique. Comput Methods Biomech Biomed Eng. October 2010;13(5):605-15.
2010	Diez‐Perez A, Güerri R, Nogues X, Cáceres E, Peña MJ, Mellibovsky L, Randall C, Bridges D, Weaver JC, Proctor A, Brimer D, Koester KJ, Ritchie RO, Hansma PK. Microindentation for in vivo measurement of bone tissue mechanical properties in humans. J Bone Miner Res. 2010;25(8):1877-1885.
2009	Ritchie R, Buehler M, Hansma P. Plasticity and toughness in bone. Phys Today. June 2009;62(6):41-47.
2008	Dendorfer S, Maier HJ, Taylor D, Hammer J. Anisotropy of the fatigue behaviour of cancellous bone. J Biomech. 2008;41(3):636-641.
1987	Lorensen WE, Cline HE. Marching cubes: a high resolution 3D surface construction algorithm. Comput Graph. 1987;21(4):163-169.
1996	Zysset PK, Curnier A. A 3D damage model for trabecular bone based on fabric tensors. J Biomech. December 1996;29(12):1549-1558.
2004	Schuit SCE, van der Klift M, Weel AEAM, de Laet CEDH, Burger H, Seeman E, Hofman A, Uitterlinden AG, van Leeuwen JPTM, Pols HAP. Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam Study. Bone. January 2004;34(1):195-202.
1999	Keaveny TM, Wachtel EF, Kopperdahl DL. Mechanical behavior of human trabecular bone after overloading. J Orthop Res. May 1999;17(3):346-353.
2011	Wolfram U, Wilke H-J, Zysset PK. Damage accumulation in vertebral trabecular bone depends on loading mode and direction. J Biomech. April 7, 2011;44(7):1164-1169.
1999	Keaveny TM, Wachtel EF, Zadesky SP, Arramon YP. Application of the Tsai–Wu quadratic multiaxial failure criterion to bovine trabecular bone. J Biomech Eng. February 1999;121(1):99-107.
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.
2011	Landrigan MD, Li J, Turnbull TL, Burr DB, Niebur GL, Roeder RK. Contrast-enhanced micro-computed tomography of fatigue microdamage accumulation in human cortical bone. Bone. March 2011;48(3):443-450.
1998	Bowman SM, Guo XE, Cheng DW, Keaveny TM, Gibson LJ, Hayes WC, McMahon TA. Creep contributes to the fatigue behavior of bovine trabecular bone. J Biomech Eng. October 1998;120(5):647-654.
2010	Doube M, Kłosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, Schmid B, Hutchinson JR, Shefelbine SJ. BoneJ: free and extensible bone image analysis in ImageJ. Bone. December 2010;47(6):1076-1079.
1974	Whitehouse WJ. The quantitative morphology of anisotropic trabecular bone. J Microsc (Oxford). July 1974;101:153-168.
2016	Torres AM, Matheny JB, Keaveny TM, Taylor D, Rimnac CM, Hernandez CJ. Material heterogeneity in cancellous bone promotes deformation recovery after mechanical failure. Proc Natl Acad Sci USA. March 15, 2016;113(11):2892-2897.
2015	Silva BC, Broy SB, Boutroy S, Schousboe JT, Shepherd JA, Leslie WD. Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD official positions part 2: trabecular bone score. J Clin Densitom. July–September 2015;18(3):309-330.
2014	Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP. Trabecular bone score: a noninvasive analytical method based upon the dxa image. J Bone Miner Res. March 2014;29(3):518-530.
2013	Lambers FM, Bouman AR, Rimnac CM, Hernandez CJ. Microdamage caused by fatigue loading in human cancellous bone: relationship to reductions in bone biomechanical performance. PLoS One. December 2013;8(12):e83662.
1979	Lafferty JF, Raju PVV. The influence of stress frequency on the fatigue strength of cortical bone. J Biomech Eng. April 1979;101(2):112-113.
2005	Nagaraja S, Couse TL, Guldberg RE. Trabecular bone microdamage and microstructural stresses under uniaxial compression. J Biomech. 2005;38(4):707-716.
2007	Bolotin HH. DXA in vivo BMD methodology: an erroneous and misleading research and clinical gauge of bone mineral status, bone fragility, and bone remodelling. Bone. July 2007;41(1):138-154.
2013	Nishiyama KK, Shane E. Clinical imaging of bone microarchitecture with HR-pQCT. Curr Osteoporos Rep. June 2013;11(2):147-155.
1993	Michel MC, Guo X-DE, Gibson LJ, McMahon TA, Hayes WC. Compressive fatigue behavior of bovine trabecular bone. J Biomech. April–May 1993;26(4-5):453-463.
2006	Wang X, Niebur GL. Microdamage propagation in trabecular bone due to changes in loading mode. J Biomech. 2006;39(5):781-790.
1996	Pattin CA, Caler WE, Carter DR. Cyclic mechanical property degradation during fatigue loading of cortical bone. J Biomech. January 1996;29(1):69-79.
1994	Keaveny TM, Wachtel EF, Guo XE, Hayes WC. Mechanical behavior of damaged trabecular bone. J Biomech. November 1994;27(11):1309-1318.
1988	Hui SL, Slemenda CW, Johnston CC Jr. Age and bone mass as predictors of fracture in a prospective study. J Clin Invest. June 1988;81(6):1804-1809.
1990	Schaffler MB, Radin EL, Burr DB. Long-term fatigue behavior of compact bone at low strain magnitude and rate. Bone. 1990;11(5):321-326.
1989	Caler WE, Carter DR. Bone creep-fatigue damage accumulation. J Biomech. 1989;22(6-7):625-635.
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.
1979	Otsu N. A threshold selection method from gray-level histograms. IEEE Trans Sys Man Cyb. 1979;9(1):62-66.
1981	Carter DR, Caler WE, Spengler DM, Frankel VH. Fatigue behavior of adult cortical bone: the influence of mean strain and strain range. Acta Orthop Scand. 1981;52(5):481-490.
2007	Taylor D, Hazenberg JG, Lee TC. Living with cracks: damage and repair in human bone. Nat Mater. April 2007;6(4):263-268.
2007	Blake GM, Fogelman I. The role of DXA bone density scans in the diagnosis and treatment of osteoporosis. Postgrad Med J. August 2007;83(982):509-517.
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.
2016	Hunt HB, Donnelly E. Bone quality assessment techniques: geometric, compositional, and mechanical characterization from macroscale to nanoscale. Clin Rev Bone Miner Metab. September 2016;14(3):133-149.
2004	Haddock SM, Yeh OC, Mummaneni PV, Rosenberg WS, Keaveny TM. Similarity in the fatigue behavior of trabecular bone across site and species. J Biomech. February 2004;37(2):181-187.
1994	Fyhrie DP, Schaffler MB. Failure mechanisms in human vertebral cancellous bone. Bone. 1994;15(1):105-109.
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.
2009	Garcia D, Zysset PK, Charlebois M, Curnier A. A three-dimensional elastic plastic damage constitutive law for bone tissue. Biomech Model Mechanobiol. April 2009;8(2):149-165.
1990	Burr DB, Stafford T. Validity of the bulk-staining technique to separate artifactual from in vivo bone microdamage. Clin Orthop Relat Res. November 1990;260:305-308.
1997	Griffin LV, Gibeling JC, Martin RB, Gibson VA, Stover SM. Model of flexural fatigue damage accumulation for cortical bone. J Orthop Res. July 1997;15(4):607-614.
2003	Moore TLA, Gibson LJ. Fatigue microdamage in bovine trabecular bone. J Biomech Eng. December 2003;125(6):769-776.
1988	Brinckmann P, Biggemann M, Hilweg D. Fatigue fracture of human lumbar vertebrae. Clin Biomech (Bristol, Avon). 1988;3(suppl 1):S1-S23.
1998	Burr DB, Turner CH, Naick P, Forwood MR, Ambrosius W, Hasan MS, Pidaparti R. Does microdamage accumulation affect the mechanical properties of bone? J Biomech. April 1998;31(4):337-345.

Cited By (2)

Year	Entry
2020	Lin X, Zhao J, Gao L, Zhang C, Gao H. Ratcheting-fatigue behavior of trabecular bone under cyclic tensile-compressive loading. J Mech Behav Biomed Mater. December 2020;112:104003.
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.