Local and global microarchitecture is associated with different features of bone biomechanics

Jean-Paul Roux,Stéphanie Boutroy,Mary L Bouxsein,Roland Chapurlat,Julien Wegrzyn

doi:10.1016/j.bonr.2020.100716

Abstract

PurposeBeside areal bone mineral density (aBMD), evaluation of fragility fracture risk mostly relies on global microarchitecture. However, microarchitecture is not a uniform network. Therefore, this study aimed to compare local structural weakness to global microarchitecture on whole vertebral bodies and to evaluate how local and global microarchitecture was associated with bone biomechanics. MethodsFrom 21 human L3 vertebrae, aBMD was measured using absorptiometry. Parameters of global microarchitecture were measured using HR-pQCT: trabecular bone volume fraction (Tb.BV/TVglobal), trabecular number, structure model index and connectivity density (Conn.D). Local minimal values of aBMD and Tb.BV/TV were identified in the total (Tt) or trabecular (Tb) area of each vertebral body. “Two dimensional (2D) local structural weakness” was defined as Tt.BMDmin, Tt.BV/TVmin and Tb.BV/TVmin. Mechanical testing was performed in 3 phases: 1/ initial compression until mild vertebral fracture, 2/ unloaded relaxation, and 3/ second compression until failure. ResultsInitial and post-fracture mechanics were significantly correlated with bone mass, global and local microarchitecture. Tt.BMDmin, Tt.BV/TVmin, Tb.BV/TVmin, and initial and post-fracture mechanics remained significantly correlated after adjustment for aBMD or Tb.BV/TVglobal (p < 0.001 to 0.038). The combination of the most relevant parameter of bone mass, global and local microarchitecture associated with failure load and stiffness demonstrated that global microarchitecture explained initial and post-fracture stiffness, while local structural weakness explained initial and post-fracture failure load (p < 0.001). ConclusionLocal and global microarchitecture was associated with different features of vertebral bone biomechanics, with global microarchitecture controlling stiffness and 2D local structural weakness controlling strength. Therefore, determining both localized low density and impaired global microarchitecture could have major impact on vertebral fracture risk prediction.

Highlights

Osteoporosis is characterized by an increased fracture risk and operationally defined using dual-energy X-ray absorptiometry (DXA) measurement of areal bone mineral density
These studies emphasized that whole bone failure was controlled by local mechanical effects potentially attributable to local structural weakness (Nazarian et al, 2006; Perilli et al, 2008; Costa et al, 2017; Jackman et al, 2016; Crawford et al, 2003; Goff et al, 2015). Most of these previous studies were performed on trabecular bone samples or biopsies with average measurements across the whole bone specimen even though trabecular microarchitecture is not uniformly distributed throughout a vertebra and have not investigated local structural weakness (Roux et al, 2010; Wegrzyn et al, 2010; Wegrzyn et al, 2011; Boutroy et al, 2005; Sornay-Rendu et al, 2007; Burghardt et al, 2011; Banse et al, 2001; Hulme et al, 2007). These results provide a strong rationale for exploring the contribution of local variations in trabecular microarchitecture on the whole bone mechanical behavior
Even though the vertebral trabecular bone is not a uniform microarchitectural network, most of the previous studies evaluating the relationship between vertebral mechanical behavior and bone microarchitecture was based on averaged microarchitectural parameter measurements or microrachitectural heterogeneity assessment across whole bone specimens (Roux et al, 2010; Wegrzyn et al, 2010; Wegrzyn et al, 2011; Boutroy et al, 2005; Sornay-Rendu et al, 2007; Burghardt et al, 2011; Banse et al, 2001; Hulme et al, 2007; Hussein and Morgan, 2013; Hussein et al, 2013)

Summary

Introduction

Osteoporosis is characterized by an increased fracture risk and operationally defined using dual-energy X-ray absorptiometry (DXA) measurement of areal bone mineral density (aBMD) It has been demonstrated, that the biomechanical evaluation of osteoporotic fracture risk was improved by a global approach of exploring “bone strength”, that includes various averaged parameters of the whole volume of interest such as bone geometry, microarchitecture and matrix properties, rather than aBMD measurement alone (SornayRendu et al, 2005; Siris et al, 2004; Bouxsein, 2005; Lester, 2005). The anterior part of the lumbar vertebral body appeared to be more strongly related to the vertebral failure load and, probably, the best region to explore when predicting the vertebral fracture risk (Hulme et al, 2007)

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