Strain‐mode‐specific mechanical testing and the interpretation of bone adaptation in the deer calcaneus

Abstract

AbstractThe artiodactyl (deer and sheep) calcaneus is a model that helps in understanding how many bones achieve anatomical optimization and functional adaptation. We consider how the dorsal and plantar cortices of these bones are optimized in quasi‐isolation (the conventional view) versus in the context of load sharing along the calcaneal shaft by “tension members” (the plantar ligament and superficial digital flexor tendon). This load‐sharing concept replaces the conventional view, as we have argued in a recent publication that employs an advanced analytical model of habitual loading and fracture risk factors of the deer calcaneus. Like deer and sheep calcanei, many mammalian limb bones also experience prevalent bending, which seems problematic because the bone is weaker and less fatigue‐resistant in tension than compression. To understand how bones adapt to bending loads and counteract deleterious consequences of tension, it is important to examine both strain‐mode‐specific (S‐M‐S) testing (compression testing of bone habitually loaded in compression; tension testing of bone habitually loaded in tension) and non‐S‐M‐S testing. Mechanical testing was performed on individually machined specimens from the dorsal “compression cortex” and plantar “tension cortex” of adult deer calcanei and were independently tested to failure in one of these two strain modes. We hypothesized that the mechanical properties of each cortex region would be optimized for its habitual strain mode when these regions are considered independently. Consistent with this hypothesis, energy absorption parameters were approximately three times greater in S‐M‐S compression testing in the dorsal/compression cortex when compared to non‐S‐M‐S tension testing of the dorsal cortex. However, inconsistent with this hypothesis, S‐M‐S tension testing of the plantar/tension cortex did not show greater energy absorption compared to non‐S‐M‐S compression testing of the plantar cortex. When compared to the dorsal cortex, the plantar cortex only had a higher elastic modulus (in S‐M‐S testing of both regions). Therefore, the greater strength and capacity for energy absorption of the dorsal cortex might “protect” the weaker plantar cortex during functional loading. However, this conventional interpretation (i.e., considering adaptation of each cortex in isolation) is rejected when critically considering the load‐sharing influences of the ligament and tendon that course along the plantar cortex. This important finding/interpretation has general implications for a better understanding of how other similarly loaded bones achieve anatomical optimization and functional adaptation.