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Altered topological blueprint of trabecular bone associates with skeletal pathology in humans

Natalie Reznikov (1), Ammar Alsheghri (2), Nicolas Piche (3), Mathieu Gendron (3), Catherine Desrosiers (3), Ievgeniia Morozova (4), Juan Manuel Sanchez Siles (5), David Gonzalez- Quevedo (5), Iskandar Tamimi (5), Jun Song (2), Faleh Tamimi (1)

Bone Reports, 12, June 2020. DOI: 10.1016/j.bonr.2020.100264

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Keywords

Human trabecular bone; Topology; Knee articular cartilage; Computational simulation; Osteoporosis; Osteoarthritis

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Abstract

Bone is a hierarchically organized biological material, and its strength is usually attributed to overt factors such as mass, density, and composition. Here we investigate a covert factor – the topological blueprint, or the network organization pattern of trabecular bone. This generally conserved metric of an edge-and-node simplified presentation of trabecular bone relates to the average coordination/valence of nodes and the equiangular 3D offset of trabeculae emanating from these nodes. We compare the topological blueprint of trabecular bone in presumably normal, fractured osteoporotic, and osteoarthritic samples (all from human femoral head, cross-sectional study). We show that bone topology is altered similarly in both fragility fracture and in joint degeneration. Decoupled from the morphological descriptors, the topological blueprint subjected to simulated loading associates with an abnormal distribution of strain, local stress concentrations and lower resistance to the standardized load in pathological samples, in comparison with normal samples. These topological effects show no correlation with classic morphological descriptors of trabecular bone. The negative effect of the altered topological blueprint may, or may not, be partly compensated for by the morphological parameters. Thus, naturally occurring optimization of trabecular topology, or a lack thereof in skeletal disease, might be an additional, previously unaccounted for, contributor to the biomechanical performance of bone, and might be considered as a factor in the life-long pathophysiological trajectory of common bone ailments.

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How Our Software Was Used

Dragonfly's Bone Analysis module was used to analyze bone samples morphometrically to obtain bone volume fraction, trabecular thickness, trabecular separation, connectivity density per unit of volume and mean intercept length (MIL) anisotropy. It was also used to perform a topological analysis, to reduce binary 3D images to 3D edge-and-node networks (or graphs) and for image reconstruction.

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Author Affiliation

(1) Faculty of Dentistry, McGill University, 2001 Avenue McGill College, Montréal, QC H3A 1G1, Canada
(2) Department of Mining and Materials Engineering, McGill University, 3610 University St. Montréal, QC H3A 0C5, Canada
(3) Object Research Systems Inc., 760 Saint-Paul St W, Montréal, QC H3C 1M4, Canada
(4) Trikon Technologies Inc., 208 Rue Joseph-Carrier, Vaudreuil-Dorion, QC J7V 5V5, Canada
(5) Regional University Hospital of Málaga, 84 Av. de Carlos Haya, 29010 Málaga, Spain

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