Chewing Affects Structural and Material Coupling, and Age-Related Dentoalveolar Joint Biomechanics and Strain

Understanding how primary structural features and secondary material properties adapt to functional loads is essential to determining their effect on changes in joint biomechanics over time. The objective of this study was to map and correlate spatiotemporal changes in primary structural features, secondary material properties, and dentoalveolar joint (DAJ) stiffness with age in rats subjected to prolonged chewing of soft foods versus hard foods. To probe how loading history shapes the balance between the primary and secondary features, four-week-old rats were fed either a hard-food (HF, N = 25) or soft-food (SF, N = 25) diet for 4, 12, 16, and 20 weeks, and functional imaging of intact mandibular DAJs was performed at 8, 12, 16, 20, and 24 weeks. Across this time course, the primary structural determinants of joint function (periodontal ligament (PDL) space, contact area, and alveolar bone socket morphology) and secondary material and microstructural determinants (tissue-level stiffness encoded by bone and cementum volume fractions, pore architecture, and bone microarchitecture) were quantified. As the joints matured, bone and cementum volume fractions increased in both the HF and SF groups but along significantly different trajectories, and these changes correlated with a pronounced decrease in PDL-space from 12 to 16 weeks in both diets. With further aging, older HF rats maintained significantly wider PDL-spaces than SF rats. These evolving physical features were accompanied by an age-dependent significant increase in the contact ratio in the SF group. The DAJ stiffness was significantly greater in SF than HF animals at younger ages, indicating that food hardness-dependent remodeling alters the relative contribution of structural versus material factors to joint function across the life course. At the tissue level, volumetric strains, representing overall volume changes, and von Mises bone strains, representing shape changes, increased with age in HF and SF joints, with volumetric strain rising rapidly from 16 to 20 weeks and von Mises strain increasing sharply from 12 to 16 weeks. Bone in SF animals exhibited higher and more variable strain values than age-matched HF bone, and changes in joint space, degrees of freedom, contact area, and bone strain correlated with joint biomechanics, demonstrating that multiscale functional biomechanics, including bone strain in intact DAJs, are colocalized with anatomy-specific physical effectors. Together, these spatiotemporal shifts in primary (structure/form), and secondary features (material properties and microarchitecture) define divergent mechanobiological pathways for the DAJ and suggest that altered loading histories can bias joints toward early maladaptation and potential degeneration.