A New Quantitative Index of Trabecular Bone Microstructural Organization and Its Association With Tissue Failure in Human Vertebrae

Abstract

Trabecular bone is a lightweight porous tissue with critical load-bearing function that is optimized through load-driven structural remodeling. One critical feature of trabecular bone microstructure at the level of whole trabeculae is the predominance of plate-like and rod-like forms with distinct orientations, material properties, and mechanical roles. Trabecular plates primarily align in the direction of typical loads and dominate structural stiffness under such loads. Thinner, less dense trabecular rods primarily align transverse to typical loads, contribute little to structural stiffness, but preferentially serve as sites for early tissue failure. These distinct roles impart resistance to both overload (plates) and fatigue failure (rods), and topological decomposition algorithms like individual trabecular segmentation (ITS) enable identification of plates and rods and their orientations in three-dimensional (3D) images of trabecular bone. However, no existing metric describes the degree of organization between plates and rods, which is critical to their complementary functions. To quantify this feature of trabecular microstructure, we present a novel structural organization index (SOI), which accounts for variability in the orientations of trabecular plates and rods, and their degree of orthogonality relative to each other. In human vertebral trabecular bone, SOI was positively associated with experimentally measured apparent-level yield strain, as well as the proportion of failed tissue in trabecular rods assessed through finite element analysis. We conclude that SOI produces valuable insights related to trabecular bone damage and yielding and may be particularly useful in cases where homeostatic remodeling is perturbed, such as during pregnancy or spaceflight.