Differences in the degree of bone tissue mineralization account for little of the differences in tissue elastic properties

Zebaze, Roger M. D.; Jones, Anthony C.; Pandy, Marcus G.; Knackstedt, Mark A.; Seeman, Ego

Affiliations

¹Departments of Endocrinology & Medicine, Austin Health, University of Melbourne, Melbourne, Australia

²Department of Applied Mathematics, Research School of Physical Sciences and Engineering, Australian National University, Canberra ACT 0200, Australia

³Department of Mechanical Engineering, University of Melbourne, Australia

Abstract and keywords

Mini-abstrac: Study of postmortem samples of cortical bone from the trochanters of 12 Caucasian females revealed that tissue mineral density (TMD) and tissue elastic modulus correlate weakly within and between individuals. Other material properties need to be taken into account to more fully predict variation in tissue elastic modulus.

Introduction: Bone is a composite material that varies in its material composition and structural organization at the macro-, micro-, and nano-scales. This hierarchical organization is essential for bone's resistance to crack initiation and propagation. We quantified the relationship between regional heterogeneity in TMD and tissue elastic modulus in cortical bone of the trochanter to determine whether TMD can be used as a predictor of tissue elastic modulus.

Methods: Measurements of tissue elastic modulus and hardness were made using nanoindentation at 5 × 20 indent points spaced 100 μm apart. TMD at the same location was computed from quantitative backscattered scanning electron microscopy imaging of cortical samples from trochanters obtained at postmortem from 12 Caucasian females (mean age: 69 years; range: 29 to 85 years).

Results: Within an individual, the variance in tissue elastic modulus (CV = 18.7%; range: 9 to 41.5%) was five times greater than the variance in TMD (3.6%, range: 1.8 to 5.7%). On average, only 45% of the variance in tissue elastic modulus was explained by TMD. From individual to individual, the proportion of the variance in tissue elastic modulus explained by TMD ranged from 0 to 64%. In 6 of 12 samples, TMD explained less than 30% of the variance in tissue elastic modulus. Results were similar for tissue hardness.

Conclusion: Tissue mineral density is an incomplete surrogate for tissue elastic modulus. Other material properties need to be accounted for to more fully predict regional variation in tissue elastic modulus.

Keywords: Bone quality; Tissue mineral density; Tissue elastic modulus

Links

DOI: 10.1016/j.bone.2011.02.023

PubMed: 21385633

WoS: 000290974200004

History

Received: 2010-08-5

Revised: 2011-02-24

Accepted: 2011-02-26

Online: 2011-03-6

Cited Works (18)

Year	Entry
2000	Boivin GY, Chavassieux PM, Santora AC, Yates J, Meunier PJ. Alendronate increases bone strength by increasing the mean degree of mineralization of bone tissue in osteoporotic women. Bone. November 2000;27(5):687-694.
2002	Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.
2006	Gupta HS, Stachewicz U, Wagermaier W, Roschger P, Wagner HD, Fratzl P. Mechanical modulation at the lamellar level in osteonal bone. J Mater Res. August 2006;21(8):1913-1921.
2008	Keaveny TM, Hoffmann PF, Singh M, Palermo L, Bilezikian JP, Greenspan SL, Black DM. Femoral bone strength and its relation to cortical and trabecular changes after treatment with PTH, alendronate, and their combination as assessed by finite element analysis of quantitative CT scans. J Bone Miner Res. December 2008;23(12):1974-1982.
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.
2010	Farlay D, Panczer G, Rey C, Delmas PD, Boivin G. Mineral maturity and crystallinity index are distinct characteristics of bone mineral. J Bone Min Metab. July 2010;28(4):433-445.
1990	Boyce TM, Bloebaum RD, Bachus KN, Skedros JG. Reproducible methods for calibrating the backscattered electron signal for quantitative assessment of mineral content in bone. Scanning Microsc. September 1990;4(3):591-600.
2006	Saito M, Fujii K, Mori Y, Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int. October 2006;17(10):1514-1523.
2004	Follet H, Boivin G, Rumelhart C, Meunier PJ. The degree of mineralization is a determinant of bone strength: a study on human calcanei. Bone. May 2004;34(5):783-789.
1989	Martin RB, Ishida J. The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. J Biomech. 1989;22(5):419-426.
1984	Currey JD. Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc Lond B Biol Sci. February 13, 1984;304(1121):509-518.
2008	Oyen ML, Ferguson VL, Bembey AK, Bushby AJ, Boyde A. Composite bounds on the elastic modulus of bone. J Biomech. August 7, 2008;41(11):2585-2588.
2007	Mulder L, Koolstra JH, den Toonder JMJ, van Eijden TMGJ. Intratrabecular distribution of tissue stiffness and mineralization in developing trabecular bone. Bone. August 2007;41(2):256-265.
2006	Gupta HS, Seto J, Wagermaier W, Zaslansky P, Boesecke P, Fratzl P. Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc Natl Acad Sci USA. November 21, 2006;103(47):17741-17746.
2006	Seeman E, Delmas PD. Bone quality: the material and structural basis of bone strength and fragility. NEJM. May 25, 2006;354(21):2250-2261.
2005	Gupta HS, Schratter S, Tesch W, Roschger P, Berzlanovich A, Schoeberl T, Klaushofer K, Fratzl P. Two different correlations between nanoindentation modulus and mineral content in the bone–cartilage interface. J Struct Biol. February 2005;149(2):138-148.
2007	van Ruijven LJ, Mulder L, van Eijden TMGJ. Variations in mineralization affect the stress and strain distributions in cortical and trabecular bone. J Biomech. 2007;40(6):1211-1218.
2004	Oliver WC, Pharr GM. Measurement of hardness and elastic modulus by instrumented indentation: advances in understanding and refinements to methodology. J Mater Res. January 2004;19(1):3-20.

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Year	Entry
2020	Chen X, Hughes R, Mullin N, Hawkins RJ, Holen I, Brown NJ, Hobbs JK. Mechanical heterogeneity in the bone microenvironment as characterized by atomic force microscopy. Biophys J. August 4, 2020;119(3):502-513.
2011	Paschalis EP, Tatakis DN, Robins S, Fratzl P, Manjubala I, Zoehrer R, Gamsjaeger S, Buchinger B, Roschger A, Phipps R, Boskey AL, Dall'Ara E, Varga P, Zysset P, Klaushofer K, Roschger P. Lathyrism-induced alterations in collagen cross-links influence the mechanical properties of bone material without affecting the mineral. Bone. December 2011;49(6):1232-1241.
2013	Zebaze R, Ghasem-Zadeh A, Mbala A, Seeman E. A new method of segmentation of compact-appearing, transitional and trabecular compartments and quantification of cortical porosity from high resolution peripheral quantitative computed tomographic images. Bone. May 2013;54(1):8-20.
2012	Feng L, Chittenden M, Schirer J, Dickinson M, Jasiuk I. Mechanical properties of porcine femoral cortical bone measured by nanoindentation. J Biomech. June 26, 2012;45(10):1775-1782.
2012	Pathak S, Vachhani SJ, Jepsen KJ, Goldman HM, Kalidindi SR. Assessment of lamellar level properties in mouse bone utilizing a novel spherical nanoindentation data analysis method. J Mech Behav Biomed Mater. September 2012;13:102-117.
2015	Chittenden M, Najafi AR, Li J, Jasiuk I. Nanoindentation and ash content study of age dependent changes in porcine cortical bone. J Mech Med Biol. October 2015;15(5):1550074.
2011	Wu Z. Measures of Bone Quality and Their Relationship to Bone Mechanical Properties [PhD thesis]. University of Notre Dame; December 2011.
2013	Toal VR. The Mechanics of Microdamage and Microfracture in Trabecular Bone [PhD thesis]. Brisbane, Australia: Queensland University of Technology; September 2013.
2011	Reisinger AG. Modeling and Validation of Multiscale Lamellar Bone Elasticity [PhD thesis]. Vienna University of Technology; November 2011.
2011	Spiesz EM. Experimental and Computational Micromechanics of Mineralized Tendon and Bone [PhD thesis]. Vienna University of Technology; October 2011.
2012	Tjhia CKH. Bone Quality of Patients With Atypical Fractures and Severely Suppressed Bone Turnover [PhD thesis]. Davis, University of California; 2012.
2014	Sinder BP. Sclerostin Antibody as a Treatment for Osteogenesis Imperfecta [PhD thesis]. University of Michigan; 2014.
2019	Küsters NV. Auswirkungen des Alters und der Knochenmikroarchitektur auf die trabekuläre Knochenmineralisationsdichteverteilung: Eine rasterelektronenmikroskopische Studie an 152 humanen Beckenkammbiopsien [PhD thesis]. Hamburg, Germany: Universität Hamburg; 2019.
2015	Lin C-L. A Study of Human and Bovine Trabecular Bones Using Nanoindentation and Quantitative Backscattered Electron Imaging [PhD thesis]. Brisbane, Australia: University of Queensland; 2015.
2016	Lin C-l. A Study of Human and Bovine Trabecular Bones Using Nanoindentation and Quantitative Backscattered Electron Imaging [PhD thesis]. Brisbane, Australia: University of Queensland; 2016.
2018	Burnett WD. Relationships Between Image-Based and Mechanical Bone Properties With Pain in Knee Osteoarthritis [PhD thesis]. University of Saskatchewan; July 2018.
2013	Faingold A. Bone Elementary Units: Mechanical Properties and Structure [PhD thesis]. Weizmann Institute of Science; February 2013.