Elsevier

Bone

Volume 26, Issue 6, June 2000, Pages 603-609
Bone

ORIGINAL ARTICLES
Heterogeneity of bone lamellar-level elastic moduli

https://doi.org/10.1016/S8756-3282(00)00268-4Get rights and content

Abstract

Advances in our ability to assess fracture risk, predict implant success, and evaluate new therapies for bone metabolic and remodeling disorders depend on our understanding of anatomically specific measures of local tissue mechanical properties near and surrounding bone cells. Using nanoindentation, we have quantified elastic modulus and hardness of human lamellar bone tissue as a function of tissue microstructures and anatomic location. Cortical and trabecular bone specimens were obtained from the femoral neck and diaphysis, distal radius, and fifth lumbar vertebra of ten male subjects (aged 40–85 years). Tissue was tested under moist conditions at room temperature to a maximum depth of 500 nm with a loading rate of 10 nm/sec. Diaphyseal tissue was found to have greater elastic modulus and hardness than metaphyseal tissues for all microstructures, whereas interstitial elastic modulus and hardness did not differ significantly between metaphyses. Trabecular bone varied across locations, with the femoral neck having greater lamellar-level elastic modulus and hardness than the distal radius, which had greater properties than the fifth lumbar vertebra. Osteonal, interstitial, and primary lamellar tissues of compact bone had greater elastic moduli and hardnesses than trabecular bone when comparing within an anatomic location. Only femoral neck interstitial tissue had a greater elastic modulus than its osteonal counterpart, which suggests that microstructural distinctions can vary with anatomical location and may reflect differences in the average tissue age of cortical bone or mineral and collagen organization.

Introduction

Advances in our ability to assess fracture risk, predict implant success, and evaluate new therapies for bone metabolic and remodeling disorders demand anatomically specific measures of the local mechanical environment of the cell. Moreover, quantifying anatomic heterogeneity in extracellular matrix properties may provide input for computational models of physiological strategies for balancing mechanical function with mineral homeostasis requirements.

In support of this structure–function paradigm, several investigators have explored regional and anatomical variation in the macroscopic mechanical properties of human cortical and trabecular bone.2, 9, 12, 16, 19, 23, 24, 28, 45, 49, 50, 60 Many of these studies have also been summarized in reviews by Reilly and Burstein,46 Goldstein,27 and Keaveny and Hayes.36 Paralleling studies of bone mechanical heterogeneity, investigators have also quantified the biochemical constituency of bone, suggesting that tissue-level variations in intrinsic material properties may exist between lamellae,34 between cortical and trabecular tissue,41 and across anatomical locations.1, 29, 43 However, the ability of microscopic material properties, when coupled with architecture, microstructure, biochemical composition, and organization, to influence whole bone mechanical integrity is unknown.13, 20, 27, 31, 36

Although anatomical variations in cortical and trabecular bone material properties have been extensively quantified at the continuum level, parallel studies at the microscopic level are far less numerous. This disparity exists despite the existence of methods to measure microscopic bone tissue properties including microhardness, microtesting, and acoustic techniques.3, 10, 15, 17, 18, 32, 35, 39, 42, 48, 54, 55, 56, 58, 60 Indeed, the study by Weaver60 stands as the only investigation using a microscopic technique to explicitly characterize bone tissue lamellae from several different organs. Traditionally, hardness is described as the resistance to plastic deformation and is defined as the applied load divided by the residual indentation area.11 Microscopic hardness correlates with tissue-level elastic modulus in bone,21, 25, 32 but it is not a fundamental material property. Hardness integrates all constitutive behaviors of a material exhibited during deformation, making interpretation of its physical meaning challenging.

Recently, investigators have begun to use nanoindentation to measure lamellar-level bone elastic properties.33, 38, 51, 53, 59, 63 With 0.3 μN load, 0.16 nm displacement, and 400 nm spatial resolution, nanoindentation has recently been validated as an accurate and reproducible technique for evaluating the elastic moduli of bone tissue lamellae.33 Unfortunately, a comprehensive evaluation of the lamellar-level elastic properties of bone tissue from different anatomic sites remains unavailable. Hence, the objective of this study was to quantify the elastic properties of human bone tissue lamellae from four different anatomical locations representing different inherent microstructural organization.

Section snippets

Materials and methods

Subjects were obtained through the University of Michigan Anatomical Donations Program. All cadavers were fresh-frozen and screened for arthroplasty, osteosarcoma, paralysis, and metabolic bone disorders, using medical records. Cadavers of uncertain medical history were not included. Osteoporotic specimens were excluded on the basis of femoral neck fractures identified during dissection or radiographically apparent compression fractures in the fourth or fifth lumbar vertebrae. Cortical and

Results

Before statistical analysis, data with zero values were eliminated because they represented errors caused by excess fluid, which impairs sample surface detection. A total of 4037 nonzero observations were made for ten subjects in four anatomic locations. Next, 133 data points were excluded because data were recorded at depths more than 10% away from the 500 nm target depth. Histograms and univariate descriptions were generated for this reduced data set, and 22 statistical outliers were removed.

Discussion

Early studies by Weaver determined that the microhardness of interstitial lamellar-level bone is lower in the iliac crest cortex than in diaphyseal cortices.60 However, interstitial tissue from long bone diaphyses was uniform. Similarly, the present study found diaphyseal tissue to have greater elastic modulus and hardness than metaphyseal tissues for all microstructures. Analogous to the study by Weaver, interstitial tissue properties did not differ significantly between metaphyses. Osteonal

Acknowledgements

The authors recognize the contributions of W. Pan for statistical consultation and Dr. M. B. Schaffler, K. D. Burrell, and B. Riemer-McCreadie for technical assistance. This work was supported by National Institutes of Health Grant AR-34399.

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