Full-field strain measurement during mechanical testing of the human femur at physiologically relevant strain rates

Grassi, Lorenzo<sup>1,2</sup>; Väänänen, Sami P.<sup>3</sup>; Yavari, Saber Amin<sup>4</sup>; Jurvelin, Jukka S.<sup>2</sup>; Weinans, Harrie<sup>3,5</sup>; Ristinmaa, Matti<sup>1</sup>; Zadpoor, Amir A.<sup>3</sup>; Isaksson, Hanna<sup>1,2,6</sup>

Affiliations

¹Division of Solid Mechanics, Lund University, Lund 22363, Sweden

²Department of Biomedical Engineering, Lund University, BMC D13, Sölvegatan 19, Lund 22184, Sweden

³Department of Applied Physics, University of Eastern Finland, Kuopio 70211, Finland

⁴Faculty of Mechanical, Maritime, and Materials Engineering, Delft University of Technology, Delft 2628 CD, The Netherlands

⁵Department of Orthopaedics, UMC Utrecht 3508 GA, The Netherlands

⁶Department of Orthopaedics, Lund University, Lund 22184, Sweden

Abstract

Understanding the mechanical properties of human femora is of great importance for the development of a reliable fracture criterion aimed at assessing fracture risk. Earlier ex vivo studies have been conducted by measuring strains on a limited set of locations using strain gauges (SGs). Digital image correlation (DIC) could instead be used to reconstruct the full-field strain pattern over the surface of the femur. The objective of this study was to measure the full-field strain response of cadaver femora tested at a physiological strain rate up to fracture in a configuration resembling single stance. The three cadaver femora were cleaned from soft tissues, and a white background paint was applied with a random black speckle pattern over the anterior surface. The mechanical tests were conducted up to fracture at a constant displacement rate of 15 mm/s, and two cameras recorded the event at 3000 frames per second. DIC was performed to retrieve the full-field displacement map, from which strains were derived. A low-pass filter was applied over the measured displacements before the crack opened in order to reduce the noise level. The noise levels were assessed using a dedicated control plate. Conversely, no filtering was applied at the frames close to fracture to get the maximum resolution. The specimens showed a linear behavior of the principal strains with respect to the applied force up to fracture. The strain rate was comparable to the values available in literature from in vivo measurements during daily activities. The cracks opened and fully propagated in less than 1 ms, and small regions with high values of the major principal strains could be spotted just a few frames before the crack opened. This corroborates the hypothesis of a strain-driven fracture mechanism in human bone. The data represent a comprehensive collection of full-field strains, both at physiological load levels and up to fracture. About 10,000 points were tracked on each bone, providing superior spatial resolution compared to ∼15 measurements typically collected using SGs. These experimental data collection can be further used for validation of numerical models, and for experimental verification of bone constitutive laws and fracture criteria.

Links

DOI: 10.1115/1.4028415

PubMed: 25162941

WoS: 000342750600011

History

Received: 2014-05-08

Revised: 2014-08-13

Accepted: 2014-08-27

Online: 2014-09-17

Cited Works (15)

Year	Entry
2012	Al Nazer R, Lanovaz J, Kawalilak C, Johnston JD, Kontulainen S. Direct in vivo strain measurements in human bone: a systematic literature review. J Biomech. January 3, 2012;45(1):27-40.
2008	Schileo E, Taddei F, Cristofolini L, Viceconti M. Subject-specific finite element models implementing a maximum principal strain criterion are able to estimate failure risk and fracture location on human femurs tested in vitro. J Biomech. 2008;41(2):356-367.
1996	Burr DB, Milgrom C, Fyhrie D, Forwood M, Nyska M, Finestone A, Hoshaw S, Saiag E, Simkin A. In vivo measurement of human tibial strains during vigorous activity. Bone. May 1996;18(5):405-410.
2009	Brauer CA, Coca-Perraillon M, Cutler DM, Rosen AB. Incidence and mortality of hip fractures in the United States. JAMA. October 14, 2009;302(10):1573-1579.
2011	Dickinson AS, Taylor AC, Ozturk H, Browne M. Experimental validation of a finite element model of the proximal femur using digital image correlation and a composite bone model. J Biomech Eng. January 2011;133(1):014504.
2010	Cristofolini L, Conti G, Juszczyk M, Cremonini S, Sint Jan SV, Viceconti M. Structural behaviour and strain distribution of the long bones of the human lower limbs. J Biomech. March 22, 2010;43(5):826-835.
2009	Currey J. Measurement of the mechanical properties of bone: a recent history. Clin Orthop Relat Res. August 2009;467(8):1948-1954.
2011	Juszczyk MM, Cristofolini L, Viceconti M. The human proximal femur behaves linearly elastic up to failure under physiological loading conditions. J Biomech. August 11, 2011;44(12):2259-2266.
2010	Cristofolini L, Schileo E, Juszczyk M, Taddei F, Martelli S, Viceconti M. Mechanical testing of bones: the positive synergy of finite–element models and in vitro experiments. Philos Trans R Soc A-Math Phys Eng Sci. June 13, 2010;368(1920):2725-2763.
1986	Wolff J. The Law of Bone Remodelling. Maquet P, Furlong R, trans. New York, NY: Springer; 1986.
2009	Cristofolini L, Juszczyk M, Taddei F, Viceconti M. Strain distribution in the proximal human femoral metaphysis. Proc Inst Mech Eng Part H-J Eng Med. April 2009;2223(3):273-288.
2011	Amin S, Kopperdhal DL, Melton LJ, Achenbach SJ, Therneau TM, Riggs BL, Keaveny TM, Khosla S. Association of hip strength estimates by finite‐element analysis with fractures in women and men. J Bone Miner Res. July 2011;26(7):1593-1600.
2005	Kanis JA, Borgstrom F, De Laet C, Johansson H, Johnell O, Jonsson B, Oden A, Zethraeus N, Pfleger B, Khaltaev N. Assessment of fracture risk. Osteoporos Int. June 2005;16(6):581-589.
2013	Gilchrist S, Guy P, Cripton PA. Development of an inertia-driven model of sideways fall for detailed study of femur fracture mechanics. J Biomech Eng. December 2013;135(12):121001.
2013	Kersh ME, Zysset PK, Pahr DH, Wolfram U, Larsson D, Pandy MG. Measurement of structural anisotropy in femoral trabecular bone using clinical-resolution CT images. J Biomech. October 18, 2013;46(15):2659-2666.

Cited By (18)

Year	Entry
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	Palanca M, Tozzi G, Cristofolini L. The use of digital image correlation in the biomechanical area: a review. Int Biomech. 2016;3(1):1-21.
2015	Zani L, Erani P, Grassi L, Taddei F, Cristofolini L. Strain distribution in the proximal human femur during in vitro simulated sideways fall. J Biomech. July 16, 2015;48(10):2130-2143.
2016	Grassi L, Väänänen SP, Ristinmaa M, Jurvelin JS, Isaksson H. How accurately can subject-specific finite element models predict strains and strength of human femora? investigation using full-field measurements. J Biomech. March 21, 2016;49(5):802-806.
2020	Katz Y, Yosibash Z. New insights on the proximal femur biomechanics using digital image correlation. J Biomech. March 5, 2020;101:109599.
2020	Grassi L, Kok J, Gustafsson A, Zheng Y, Väänänen SP, Jurvelin JS, Isaksson H. Elucidating failure mechanisms in human femurs during a fall to the side using bilateral digital image correlation. J Biomech. June 9, 2020;106:109826.
2015	Grassi L, Isaksson H. Extracting accurate strain measurements in bone mechanics: a critical review of current methods. J Mech Behav Biomed Mater. October 2015;50:43-54.
2019	Gustafsson A, Khayyeri H, Wallin M, Isaksson H. An interface damage model that captures crack propagation at the microscale in cortical bone using XFEM. J Mech Behav Biomed Mater. February 2019;90:556-565.
2021	Gustafsson A, Tognini M, Bengtsson F, Gasser TC, Isaksson H, Grassi L. Subject-specific FE models of the human femur predict fracture path and bone strength under single-leg-stance loading. J Mech Behav Biomed Mater. January 2021;113:104118.
2019	Väänänen SP, Grassi L, Venäläinen MS, Matikka H, Zheng Y, Jurvelin JS, Isaksson H. Automated segmentation of cortical and trabecular bone to generate finite element models for femoral bone mechanics. Med Eng Phys. September 2019;70:19-28.
2020	Iori G, Peralta L, Reisinger A, Heyer F, Wyers C, van den Bergh J, Pahr D, Raum K. Femur strength predictions by nonlinear homogenized voxel finite element models reflect the microarchitecture of the femoral neck. Med Eng Phys. May 2020;79:60-66.
2020	Turunen MJ, Le Cann S, Tudisco E, Lovric G, Patera A, Hall SA, Isaksson H. Sub-trabecular strain evolution in human trabecular bone. Sci Rep. 2020;10:13788.
2020	Aggleton J. First-Hand Experience: A Methodology for Exploring Bone Architecture [PhD thesis]. Bristol, UK: University of Bristol; January 2020.
2018	Muckatira SK. Error Estimation in Whole Bone Microstrain Measurement When Using Digital Volume Correlation [Master's thesis]. University of Illinois at Urbana-Champaign; 2018.
2020	Karali A. Multi-Scale Evaluation of Bone Combining Indentation, in Situ XCT Mechanics and Digital Volume Correlation [PhD thesis]. Portsmouth, England: University of Portsmouth; 2020.
2023	Branni MG. Constitutive Models of Bone: The Human Femur [PhD thesis]. Queensland University of Technology; 2023.
2016	Gustafson HM. Quantifying the Response of Vertebral Bodies to Compressive Loading Using Digital Image Correlation [PhD thesis]. Vancouver, BC: University of British Columbia; October 2016.
2017	Palanca M. In Vitro Full-Field Methods for the Biomechanical Characterization of Spine Segments [PhD thesis]. University of Bologna; March 2017.