Elsevier

Bone

Volume 42, Issue 3, March 2008, Pages 591-596
Bone

Trabecular shear stress amplification and variability in human vertebral cancellous bone: Relationship with age, gender, spine level and trabecular architecture

https://doi.org/10.1016/j.bone.2007.11.011Get rights and content

Abstract

Trabecular shear stress magnitude and variability have been implicated in damage formation and reduced bone strength associated with bone loss for human vertebral bone. This study addresses the issue of whether these parameters change with age, gender or anatomical location, and if so whether this is independent of bone mass. Additionally, 3D-stereology-based architectural parameters were examined in order to establish the relationship between stress distribution parameters and trabecular architecture. Eighty cancellous bone specimens were cored from the anterior region of thoracic 12 and donor-matched lumbar 1 vertebrae from a randomly selected population of 40 cadavers. The specimens were scanned at 21-μm voxel size using microcomputed tomography (μCT) and reconstructed at 50μm. Bone volume fraction (BV/TV), trabecular number (Tb.N), trabecular thickness (Tb.Th), trabecular separation (Tb.Sp), bone surface-to-volume ratio (BS/BV), degree of anisotropy (MIL1/MIL3), and connectivity density (-#Euler/Vol) were calculated directly from micro-CT images. Large-scale finite element models were constructed and superoinferior compressive loading was simulated. Apparent cancellous modulus (EFEM) was calculated. The average trabecular von Mises stress generated per uniaxial apparent stress (σ¯VM/σapp) and coefficient of variation of trabecular von Mises stresses (COV) were calculated as measures of the magnitude and variability of shear stresses in the trabeculae. Mixed-models and regression were used for analysis. σ¯VM/σapp and COV were not different between genders and vertebrae. Both σ¯VM/σapp and COV increased with age accompanied by a decrease in BV/TV. Strong relationship of σ¯VM/σapp with BV/TV was found whereas COV was strongly related to EFEM/(BV/TV). The results from T12 and L1 were not different and highly correlated with each other. The relationship of σ¯VM/σapp with COV was observed to be different between males and females. This difference could not be explained by architectural parameters considered in this study. Our results support the relevance of trabecular shear stress amplification and variability in age-related vertebral bone fragility. The relationships found are expected to help understand the micro-mechanisms by which cancellous bone mass and mechanical properties are modulated through a collection of local stress parameters.

Introduction

Increase of trabecular stress variability with loss of bone mass has been implicated as a mechanism for increased cancellous bone fragility with age and disease [11], [35]. The underlying notion was that increased variability in trabecular stresses would give rise to stress concentrations resulting in a reduction of bone strength. Consistent with this notion, coefficient of variation of trabecular von Mises stress distributions (COV) as estimated from microcomputed tomography (μCT)-based finite element (FE) calculations has been shown to increase with decreasing bone volume (BV/TV) accompanied by a decrease in strength in human vertebral cancellous bone. It has also been shown that there is a significant positive correlation between COV and the density of in vivo microdamage from the same region in human vertebrae [34].

Average trabecular von Mises stress per apparent uniaxial stress (σ¯VM/σapp) as estimated from finite element (FE) calculations was proposed as a structural index that represents the tendency of the cancellous structure to amplify shear stresses in the tissue [35]. This parameter, too, has been shown to correlate with the density of in vivo microdamage in human vertebral bone [34]. It should be noted that, though only moderately explanatory, COV and σ¯VM/σapp had the strongest correlations ever demonstrated with in vivo microdamage in cancellous bone among mechanical parameters considered thus far. In addition, it was observed that the tissue from the thoracic 12-lumbar 1 junction had the largest σ¯VM/σapp[35] accompanied by the lowest strength [36] suggesting that this parameter may be relevant to the high incidence of vertebral fractures at these spine levels [2], [3], [10], [12], [16], [20], [23], [26].

Together, trabecular shear stress distribution parameters, namely COV and σ¯VM/σapp, appear important in understanding the mechanistic consequence of bone loss and trabecular adaptation. However, it is not known whether these parameters change with age and if so, whether these changes are independent of changes in bone volume or gender and type of vertebral bone. Secondly, which microstructural parameters of cancellous bone can explain stress distribution parameters is unknown. Also not known is whether shear stress parameters in tissue from one vertebra can be predicted by those in tissue from another vertebra of the same individual. Our objective was to answer these questions for thoracic 12 (T12) and lumbar 1 (L1) vertebrae from the same individuals.

Section snippets

Methods

Thoracic 12 and L1 vertebrae were collected fresh from 15 male (66 ± 15yrs) and 25 female (54± 16yrs) cadavers. Because complete medical history was not available for all donors, all cadavers were included without screening for bone diseases. Eight-mm-diameter and 10-mm-long cylindrical cancellous bone specimens were prepared from the anterior region of vertebral bodies in the superoinferior direction as described previously [15], [30]. Only one specimen from each vertebra was prepared and all

Results

COV and σ¯VM/σapp were not different between T12 and L1 (p > 0.76 and p > 0.07, respectively) or between males and females (p > 0.54 and p > 0.18, respectively) after accounting for age. Age was significantly associated with both COV (p < 0.0044) and σ¯VM/σapp (p < 0.0004) (Fig. 1), however, there was no longer any association between age and the outcomes (p > 0.33) with adjustment for BV/TV.

COV, σ¯VM/σapp and microstructural parameters from T12 were significantly correlated to those from L1 in

Discussion

We demonstrated that the magnitude of trabecular shear stresses relative to the compressive stress applied on the tissue (σ¯VM/σapp) and their nonuniformity (COV) increase with age. These increases were explainable by the negative relationship between bone mass and age. However, this does not mean that the stress parameters are not important once bone mass is taken into account but rather points to a mechanistic consequence of bone loss with aging. These findings are consistent with the idea

Acknowledgments

This publication was made possible by Grant Number AR049343 from the National Institutes of Health. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH.

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