Osteoporosis-related variations of trabecular bone properties of proximal human humeral heads at different scale lengths

Molino, Giulia<sup>1</sup>; Dalpozzi, Alessio<sup>1</sup>; Ciapetti, Gabriela<sup>2</sup>; Lorusso, Massimo<sup>3</sup>; Novara, Chiara<sup>1</sup>; Cavallo, Marco<sup>4</sup>; Baldini, Nicola<sup>5</sup>; Giorgis, Fabrizio<sup>1</sup>; Fiorilli, Sonia<sup>1</sup>; Vitale-Brovarone, Chiara<sup>1</sup>

Affiliations

¹Politecnico di Torino, Department of Applied Science and Technology, Corso Duca degli Abruzzi 24, 10129, Torino, Italy

²Laboratory for Orthopaedic Pathophysiology and Regenerative Medicine, IRCCS Istituto Ortopedico Rizzoli, Bologna, Italy

³Center for Sustainable Future Technologies@Polito, Istituto Italiano di Tecnologia, Via Livorno 60, 10145, Torino, Italy

⁴Shoulder and Elbow Surgery Unit, IRCCS Istituto Ortopedico Rizzoli, Bologna, Italy

⁵Laboratory for Orthopaedic Pathophysiology and Regenerative Medicine, IRCCS Istituto Ortopedico Rizzoli, & Department of Biomedical and Neuromotor Sciences, University of Bologna, Italy

Abstract and keywords

Osteoporosis (OP) is a skeletal disorder responsible for the weakening of the bone structure and, consequently, for an increased fracture risk in the elderly population. In the past, bone mineral density (BMD) variation was considered the best OP indicator, but recently the focus has shifted toward the variation of microstructural bone parameters. This work is based on the characterisation of 8-mm cylindrical biopsies harvested from proximal humeral heads belonging to healthy and osteoporotic patients, in order to assess the OP-related variations of bone properties at different scale lengths. In particular, bone biopsies underwent micro-computed tomography analysis to study the most relevant features of bone architecture and extrapolate the tissue mineral density (TMD) value of bone trabeculae. Compression tests and nanoindentations were performed to investigate the macro- and micromechanical properties of bone biopsies, respectively. In addition, XRD analyses were performed to obtain the mean hydroxyapatite (HA) crystallite size, while Raman spectroscopy investigated the collagen secondary structure. Thermogravimetric analysis was performed to evaluate the ratio between organic and inorganic phases.

From the obtained results, OP samples showed a more anisotropic and less interconnected structure responsible for reduced compression strength. From this, it can be supposed that OP caused an alteration of bone structure that led to inferior macroscopic mechanical properties. Furthermore, OP samples possessed higher TMD and bigger HA crystals that are correlated to an increase of the hardness value obtained by means of nanoindentation. This less controlled HA crystal growth is probably due to an alteration of the organic matrix structure, as revealed by the increase of the random coil contribution in the Raman spectra of the OP bone. This higher crystal content led to an increase in trabecular density and hardness. In conclusion, the obtained data showed that OP affects bone properties at different scale lengths causing an alteration of its morphological, structural and mechanical features.

Keywords: Osteoporosis; Humeral head; Micro-CT; Compression test; Nanoindentation; Raman spectroscopy

Links

DOI: 10.1016/j.jmbbm.2019.103373

PubMed: 31369957

WoS: 000496832200003

History

Received: 2019-01-29

Revised: 2019-04-01

Accepted: 2019-07-25

Online: 2019-07-26

Cited Works (18)

Year	Entry
2006	Stauber M, Müller R. Age-related changes in trabecular bone microstructures: global and local morphometry. Osteoporos Int. April 2006;17(4):616-626.
2008	Nazarian A, von Stechow D, Zurakowski D, Müller R, Snyder BD. Bone volume fraction explains the variation in strength and stiffness of cancellous bone affected by metastatic cancer and osteoporosis. Calcif Tiss Int. December 2008;83(6):368-379.
2004	Fratzl P, Gupta HS, Paschalis EP, Roschger P. Structure and mechanical quality of the collagen–mineral nano-composite in bone. J Mater Chem. 2004;14(14):2115-2123.
2011	Morris MD, Mandair GS. Raman assessment of bone quality. Clin Orthop Relat Res. August 2011;469:2160-2169.
1992	Oliver WC, Pharr GM. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res. 1992;7(6):1564-1583.
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.
2016	Mirzaali MJ, Schwiedrzik JJ, Thaiwichai S, Best JP, Michler J, Zysset PK, Wolfram U. Mechanical properties of cortical bone and their relationships with age, gender, composition and microindentation properties in the elderly. Bone. December 2016;93:196-211.
2009	Gourion‐Arsiquaud S, Faibish D, Myers E, Spevak L, Compston J, Hodsman A, Shane E, Recker RR, Boskey ER, Boskey AL. Use of FTIR spectroscopic imaging to identify parameters associated with fragility fracture. J Bone Miner Res. September 2009;24(9):1565-1571.
2004	Kim D-G, Christopherson GT, Dong XN, Fyhrie DP, Yeni YN. The effect of microcomputed tomography scanning and reconstruction voxel size on the accuracy of stereological measurements in human cancellous bone. Bone. December 2004;35(6):1375-1382.
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.
2006	Oyen ML. Nanoindentation hardness of mineralized tissues. J Biomech. 2006;39(14):2699-2702.
1995	Rho JY, Hobatho MC, Ashman RB. Relations of mechanical properties to density and CT numbers in human bone. Med Eng Phys. July 1995;17(5):347-355.
2011	Tjhia CK, Odvina CV, Rao DS, Stover SM, Wang X, Fyhrie DP. Mechanical property and tissue mineral density differences among severely suppressed bone turnover (SSBT) patients, osteoporotic patients, and normal subjects. Bone. December 2011;49(6):1279-1289.
2012	Nikodem A. Correlations between structural and mechanical properties of human trabecular femur bone. Acta Bioeng Biomech. 2012;14(2):37-46.
2016	Osterhoff G, Morgan EF, Shefelbine SJ, Karim L, McNamara LM, Augat P. Bone mechanical properties and changes with osteoporosis. Injury. June 2016;47(suppl 2):S11-S20.
1999	Zysset PK, Guo XE, Hoffler CE, Moore KE, Goldstein SA. Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J Biomech. October 1999;32(10):1005-1012.
2002	Hengsberger S, Kulik A, Zysset P. Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone. 2002;30(1):178-184.
1998	Rho J-Y, Kuhn-Spearing L, Zioupos P. Mechanical properties and the hierarchical structure of bone. Med Eng Phys. 1998;20(2):92-102.

Cited By (3)

Year	Entry
2021	Ramírez A CE, Hurtado-Macías A, Talamantes R, Flores E, Ladrón de Guevara HP, Delgado JI, Estrella RA, Riestra JM, Montes JM, Esmonde-White K, Vardaki M, González-Hernández J, Viveros JM. Assessing mechanical behavior of ostrich and equine trabecular and cortical bone based on depth sensing indentation measurements. J Mech Behav Biomed Mater. May 2021;117:104404.
2020	O’Sullivan LM. Time-Sequence of Biomechanical Adaption in Trabecular Tissue During Estrogen Deficiency [PhD thesis]. National University of Ireland Galway; March 2020.
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.