Tibiotarsal mechanical behaviour is mainly a function of bone structure and not mineral density in female adolescent chickens

Introduction Bone fragility and disuse osteoporosis in commercial egg-laying chickens is a major welfare concern. Efforts to address this have focused on eliciting increases in bone mass during growth by raising chickens in more spacious and complex housing systems that motivate increased physical activity. However, it remains unclear how these bone adaptations influence in vivo bone mechanical behaviour in chickens, namely, whole-bone stiffness and strength. Methods To investigate this, we sampled female chickens of two genetic strains (Lohmann Brown: brown-feathered, Lohmann LSL Lite: white-feathered) with different loading histories (sedentary: housed in cages with no opportunity for dynamic load bearing activity; active: raised in one of two styles of aviary housing systems requiring locomotion including jumping and other aerial transitions) just prior to the onset of sexual maturity at 16 weeks of age. We imaged their whole right tibiotarsi ( ex vivo ) using microCT and for the first time developed finite element models of the chicken tibiotarsi under controlled in vivo axial compressive loading on a limited sample size (n = 1, N = 6), which we validated with in vivo strain gauge measurements. Each bone was modelled with both homogeneous and heterogeneous material properties to assess the effects of tissue mineral density and bone structure on the mechanical behaviour. We also quantified a variety of structural measures along the bone length and determined their correlation to simulated mechanical behaviour. Results We found that consideration of volumetric tissue mineralization heterogeneity in our FE models had negligible influence on the modelled mechanical behaviour, and thus further analyses used only homogeneous FEMs. We identified bone area, total area, bone area ratio, bone thickness, eccentricity, normalized outer perimeter, and inner-to-outer perimeter ratio to be significantly correlated to decreased modelled stress. Increased activity levels was associated with lower modelled stresses in brown-, but not white-feathered chickens, and this pattern could be explained by differences in bone area, total area, and inner-to-outer perimeter ratio. Conclusion These results suggest that, similar to what has been shown in humans, bone structure and not just mineral density is a critical determinant of mechanical behaviour and therefore fracture risk. We identify structural outcomes that can be candidates for genetic selection, targeting improved bone strength, a subset of which may adapt to loading in brown-feathered chickens. We also present a novel (in the poultry science field) approach to assess the relationship between bone structure and mechanical behaviour, which can be further used to inform genetic selection and breeding for improved bone strength and fracture resistance.