Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs

Abstract

In most mammals, especially those adapted for cursoriality, distal limb bones are thinner than more proximal bones, giving the limb skeleton a tapered shape (Smith and Savage, 1956;Alexander, 1980Alexander, , 1996Hildebrand, 1985;Lieberman and Pearson, 2001;Currey, 2002). In sheep, for example, midshaft cortical areas decrease about 16% between the femur and tibia, and 24% between the tibia and metatarsal. Limb tapering is generally thought to save energy by reducing a limb's moment of inertia (Hildebrand, 1985). How much energy is saved by distal tapering has been the subject of debate, but is probably considerable in most species. While Taylor et al. (1974) found that three species (cheetah, gazelle and goats) with different limb configurations had similar energy costs (VO∑·g -1 ·h -1 ) over a range of speeds, the conclusions of the study may be flawed because the animals were not run at comparable speeds. The results of Taylor et al. (1974) contradict not only theoretical predictions (for example, see Hildebrand, 1985), but also more controlled studies such as by Myers and Steudel (1985), who found that redistributing 3.6·kg from the thigh to the ankles in trained humans increases the metabolic cost of running at 2.68·m·s -1 by 15%.Limb tapering may save energy during swing, but may also affect bone strength during stance. Limbs during stance are usually modeled as cylinders subject to a combination of bending and axial compression from body mass and ground reaction forces. At midstance, when ground reaction forces (GRFs) are typically highest and approximately vertical, bending stress/strain at midshaft (the likely location of maximum bending) is a function of many factors, including the magnitude and orientation of GRF relative to the element and the cross-sectional and the material properties of the bone (Biewener et al., 1983). Distal tapering, therefore, leads not How bones respond dynamically to mechanical loading through changes in shape and structure is poorly understood, particularly with respect to variations between bones. Structurally, cortical bones adapt in vivo to their mechanical environments primarily by modulating two processes, modeling and Haversian remodeling. Modeling, defined here as the addition of new bone, may occur in response to mechanical stimuli by altering bone shape or size through growth. Haversian remodeling is thought to be an adaptation to repair microcracks or prevent microcrack propagation. Here, we examine whether cortical bone in sheep limbs modulates periosteal modeling and Haversian remodeling to optimize strength relative to mass in hind-limb midshafts in response to moderate levels of exercise at different growth stages. Histomorphometry was used to compare rates of periosteal growth and Haversian remodeling in exercised and sedentary treatment groups of juvenile, subadult and young adult sheep. In vivo strain data were also collected for the tibia and metatarsal midshafts of juvenile sheep. The results suggest that limb bones initially optimize responses to loading...

The myokine irisin increases cortical bone mass

“…Specifically, by distributing bone mass away from the center, enlarged bone perimeter and cross-sectional area both contribute to increased pMOI and resistance to bending. The effect of r-irisin, essentially mimicking the effect of mechanotransduction (25)(26)(27), thus allows bone to become structurally more efficient for bending and torsion. Indeed, both mouse (28)(29)(30) and rat (31-34) models have collectively shown positive associations between exercise and increased bone size and bone mass.…”

Bone strain gradients and optimization in vertebrate skulls

“…In Alligator during fast locomotion, the mean peak c-max strains in the femur are 1.6 times higher than those recorded from the tibia (Blob and Biewener 1999) and, in Ovis, normal strains in the metatarsal are 1.5-1.7 times higher than those recorded from the tibia (Lieberman et al 2003). Moreover, there is evidence that strain gradients might actually be preferred over equivalent strains and equivalent strength.…”

“…Moreover, there is evidence that strain gradients might actually be preferred over equivalent strains and equivalent strength. Lieberman et al (2003) found that in growing sheep subjected to exercise, midshafts of proximal limb elements (tibiae) experienced lower strains and higher rates of periosteal remodeling relative to distal limb elements (metatarsals), which experienced higher strains and higher rates of Haversian remodeling. They hypothesized that Haversian remodeling predominates in distal limb elements to avoid adding bone mass distally where it is energetically costly to move during locomotion.…”

Blood flow to long bones indicates activity metabolism in mammals, reptiles and dinosaurs

“…The bone cells respond to local strain by either net deposition or resorption of bone as appropriate, creating strength along the lines of stress [11,12]. Many studies indicate that loading and exercise increase micro-damage in the short term and bone remodelling over a longer period [11,13]. Bone cells have high aerobic metabolic rates, comparable with nervous tissue [14], and they are accompanied by blood capillary loops [10].…”