Analysis of a tension/compression skeletal system: possible strain-specific differences in the hierarchical organization of bone.

BACKGROUND: Examination of a simple skeletal cantilevered beam-like bone (artiodactyl calcaneus) suggests that regional differences in strain magnitude and mode (tension vs. compression) reflect regional adaptation in the structural/material organization of bone. The artiodactyl (e.g., sheep and deer) calcaneus has a predominant loading condition typified by the unambiguous presence of prevailing compressive and tensile strains on opposite cortices. Bone habitually loaded in bending may accommodate regional disparities in loading conditions through modifications of various aspects of its organization. These include overall bone build (gross size and shape), cross-sectional shape, cortical thickness, and mineral content. METHODS & RESULTS: Cross-sections taken along the calcaneal body exhibited cranial-caudal elongation with the compression (cranial) cortex thicker than the tension cortex (P < 0.01). Mineral content (ash fraction) was significantly greater in the compression cortex (P < 0.01), averaging 6.6% greater than in the tension cortex. Strong positive correlations were found between mineral content and section location in both the tension (r2 = 0.955) and compression (r2 = 0.812) cortices. These correlations may reflect functional adaptations to the linear increases in stress that are known to occur in the distal-to-proximal direction in simple, unidirectionally loaded cantilevered beams. According to engineering principles, the roughly triangular transverse cross-sectional geometries and thicker compression cortex are features consistent with a short cantilevered structure designed to resist unidirectional bending. CONCLUSIONS: Known differences in mechanical properties of bone in tension vs. compression suggest that these regional differences in cortical thickness and mineralization may be related to differences in strain mode. These structural/material dissimilarities, however, may be related to regional variations in strain magnitude, since bending and axially directed stresses in a simple cantilevered structure produce greater strain magnitudes in the compression domain. It is possible that the superimposed habitual strain magnitudes enhance strain-mode-specific adaptive responses. We hypothesize that these structural/material differences reflect the capacity of bone to process local information and produce a regionally heterogeneous organization that is appropriate for prevailing loading conditions.

Mammalian locomotor-respiratory integration: implications for diaphragmatic and pulmonary design.

Diaphragmatic function and intrapulmonary respiratory flow in running mammals were found to differ substantially from the corresponding conditions known in resting mammals. In trotting dogs, orbital oscillations of the diaphragm were driven by inertial displacements of the viscera induced by locomotion. In turn, oscillations of the visceral mass drove pulmonary ventilation independent of diaphragmatic contractions, which primarily served to modulate visceral kinetics. Visceral displacements and loading of the anterior chest wall by the forelimbs are among the factors that contribute to an asynchronous ventilation of the lungs and interlobar gas recycling. Basic features of mammalian respiratory design, including the structure of the diaphragm and lobation of the lungs, appear to reflect the mechanical requirements of locomotor-respiratory integration.

Running and breathing in mammals.

Mechanical constraints appear to require that locomotion and breathing be synchronized in running mammals. Phase locking of limb and respiratory frequency has now been recorded during treadmill running in jackrabbits and during locomotion on solid ground in dogs, horses, and humans. Quadrupedal species normally synchronize the locomotor and respiratory cycles at a constant ratio of 1:1 (strides per breath) in both the trot and gallop. Human runners differ from quadrupeds in that while running they employ several phase-locked patterns (4:1, 3:1, 2:1, 1:1, 5:2, and 3:2), although a 2:1 coupling ratio appears to be favored. Even though the evolution of bipedal gait has reduced the mechanical constraints on respiration in man, thereby permitting greater flexibility in breathing pattern, it has seemingly not eliminated the need for the synchronization of respiration and body motion during sustained running. Flying birds have independently achieved phase-locked locomotor and respiratory cycles. This hints that strict locomotor-respiratory coupling may be a vital factor in the sustained aerobic exercise of endothermic vertebrates, especially those in which the stresses of locomotion tend to deform the thoracic complex.