Mechanical failure begins preferentially near resorption cavities in human vertebral cancellous bone under compression

Abstract

Summary The amount of bone turnover in the body has been implicated as a factor that can influence fracture risk and bone strength. Here we test the idea that remodeling cavities promote local tissue failure by determining if microscopic tissue damage (microdamage) caused by controlled loading in vitro is more likely to form near resorption cavities. Specimens of human vertebral cancellous bone (L4, 7 male and 2 female, age 70 ± 10, mean ± SD) were loaded in compression to the yield point, stained for microscopic tissue damage and submitted to three-dimensional fluorescent imaging using serial milling (image voxel size 0.7 × 0.7 × 5.0 µm). We found the resulting damage volume per bone volume (DV/BV) was correlated with percent eroded surface (p < 0.01, r2 = 0.65), demonstrating that whole specimen measures of resorption cavities and microdamage are related. Locations of microdamage were more than two times as likely to have a neighboring resorption cavity than randomly selected sites without microdamage (relative risk 2.39, 95% confidence interval of relative risk: 2.09 – 2.73), indicating a spatial association between resorption cavities and microdamage at the local level. Individual microdamage sites were 48,700 (40,100; 62,700) µm3 in size (median, 25th and 75th percentiles). That microdamage was associated with resorption cavities when measured at the whole specimen level as well as at the local level provides strong evidence that resorption cavities play a role in mechanical failure processes of cancellous bone and therefore have the potential to influence resistance to clinical fracture.

Continuum damage interactions between tension and compression in osteonal bone

“…Microcracks are associated and guided by micro-structural and ultra-structural features of bone (Rho et al, 1998;Jepsen et al, 1999;O'Brien et al, 2005O'Brien et al, , 2007. They appear at highly mineralised zones in bone tissue, between interstitial lamellae, along osteonal cement lines, at the boundaries of trabecular packages, at resorption cavities in trabecular bone, and, in case of sub-lamellar microcracking, along the canaliculi in cortical bone (Zioupos and Currey, 1994;Jepsen et al, 1999;O'Brien et al, 2005O'Brien et al, , 2007Vashishth, 2007;Peterlik et al, 2006;Slyfield et al, 2012;Ebacher et al, 2012).…”

The effects of tensile-compressive loading mode and microarchitecture on microdamage in human vertebral cancellous bone

“…Two-dimensional assessment of microdamage is useful for characterizing whole specimen amounts of damage, but cannot provide accurate measures of the number or size of damage sites. Three-dimensional assessment of microdamage in cancellous bone has recently been demonstrated (Bigley et al, 2008; Slyfield et al, 2012; Tang and Vashishth, 2007, 2010) and could measure the number, size and shape of individual microdamage sites, but has so far only been applied to study microdamage generated by apparent compression.…”

“…In addition to apparent loading mode, trabecular microarchitecture, and local geometry such as the presence of resorption cavities or thickness of individual trabeculae, have also been implicated as factors that may influence the generation of microdamage (Green et al, 2011; Slyfield et al, 2012). To our knowledge, differences in microdamage generation between tensile and compressive loading have not been assessed using three-dimensional analysis and it is not known how the number and size of microdamage sites varies among the apparent loading modes.…”

Multiscale Contribution of Bone Tissue Material Property Heterogeneity to Trabecular Bone Mechanical Behavior

“…At the scale of a single trabecula, computational studies have not yet addressed the effect of heterogeneity. Current computational studies at this length scale address the effect of osteoclast remodeling lacunae on trabecular strut mechanics [69][70][71][72] and the effects of loading orientation on trabecular mechanical behavior [73].…”