A 50-year perspective on the use and potential of artiodactyl calcanei in bone adaptation studies

Sheep and deer calcanei are important models for studying cortical (compact) and trabecular (cancellous) bone adaptation because they are amenable to direct strain measurement (due to lack of surrounding muscles), experience relatively simple/unidirectional bending, exhibit osteon remodelling, and have the most pronounced regional variations in mineralization and other histological characteristics reported in any bone. This simple loading environment is characterized by bending that produces prevalent/predominant tension on the plantar side and predominant compression on the dorsal side of the cantilevered, beam-like shaft of these bones. Histocompositional differences are clear between these opposing cortices, optimizing their mechanical properties for these regional differences in loading environment. This keeps the fracture risk low by enhancing the safety factor of the entire bone. Understanding how mechanosensitive cells within bone accomplish this is fundamentally important for advancing core concepts in bone biology and functional adaptation, and for clinical applications. However, an uncontested 1995 study used qualitative histological observations from a small sample (two sub-adults; three adults) of domesticated sheep calcanei and in vivo strain data from Lanyon's seminal study of sheep calcanei to reject the idea that this bone is simply loaded. That study argued that reversals of bending during the swing phase of gait negate the 'tension/compression (plantar/dorsal)' concept, thus invalidating much of the basic and translational value of the model. Their opinion is important because many investigators consider it valid despite contrary conclusions of subsequent biomechanical/histomorphological studies. This review critically evaluates the foundations of the main conclusion of that 1995 study, because their refutation of the simplicity of the artiodactyl calcaneus model has been favourably cited nearly 60 times in the peer-reviewed literature. After exposing and correcting errors and reconciling contradictory observations in that study, this review explores the strengths, limitations, and potential applications of the artiodactyl calcaneus model for advancing understanding of mechanisms and consequences of bone adaptation. Studies reviewed herein support viewing artiodactyl calcanei as simply loaded 'tension/compression bones', validating their continued use in this context in a broad spectrum of studies of cortical and trabecular bone adaptation. A particularly promising application of this model is that it can serve as a 'control bone' for studies of other presumably simply loaded bone regions, such as the human femoral neck, especially regarding the relationship of its load history, structural and material organization, and propensity to fracture.