Breed and loading history influence in vivo skeletal strain patterns in pre-pubertal female chickens.

The influence of loading history on in vivo strains within a given specie remains poorly understood, and although in vivo strains have been measured at the hindlimb bones of various species, strains engendered during modes of activity other than locomotion are lacking, particularly in non-human species. For commercial egg-laying chickens specifically, there is an interest in understanding their bones' mechanical behaviour, particularly during youth, to develop early interventions to prevent the high incidence of osteoporosis in this population. We measured in vivo mechanical strains at the tibiotarsus midshaft during steady activities (ground, uphill, downhill locomotion) and non-steady activities (perching, jumping, aerial transition landing) in 48 pre-pubescent female (egg-laying) chickens from two breeds that were reared in three different housing systems, allowing varying amounts and types of physical activity. Mechanical strain patterns differed between breeds, and were dependent on the activity performed. Mechanical strains were also affected by rearing environment: chickens that were restricted from performing dynamic load bearing activity due to caged-housing generally exhibited higher mechanical strain levels during steady, but not non-steady activities, compared to chickens with prior dynamic load-bearing activity experience. Among chickens with prior experience of dynamic load bearing activity, those reared in housing systems that allowed more frequent physical activity did not exhibit lower mechanical strains. In all groups, the tibiotarsus was subjected to a loading environment consisting of a combination of axial compression, bending, and torsion, with torsion being the predominant source of strain. Aerial transition landing produced the highest strain levels with unusual strain patterns compared to other activities, suggesting it may produce the strongest anabolic response. These results exemplify how different breeds within a given specie adapt to maintain different patterns of mechanical strains, and how benefits of physical activity in terms of resistance to strain are activity-type dependent and do not necessarily increase with increased physical activity. These findings directly inform controlled loading experiments aimed at studying the bone mechanoresponse in young female chickens and can also be associated to measures of bone morphology and material properties to understand how these features influence bone mechanical properties in vivo.

The mechanoresponse of bone is closely related to the osteocyte lacunocanalicular network architecture.

Organisms rely on mechanosensing mechanisms to adapt to changes in their mechanical environment. Fluid-filled network structures not only ensure efficient transport but can also be employed for mechanosensation. The lacunocanalicular network (LCN) is a fluid-filled network structure, which pervades our bones and accommodates a cell network of osteocytes. For the mechanism of mechanosensation, it was hypothesized that load-induced fluid flow results in forces that can be sensed by the cells. We use a controlled in vivo loading experiment on murine tibiae to test this hypothesis, whereby the mechanoresponse was quantified experimentally by in vivo micro-computed tomography (µCT) in terms of formed and resorbed bone volume. By imaging the LCN using confocal microscopy in bone volumes covering the entire cross-section of mouse tibiae and by calculating the fluid flow in the three-dimensional (3D) network, we could perform a direct comparison between predictions based on fluid flow velocity and the experimentally measured mechanoresponse. While local strain distributions estimated by finite-element analysis incorrectly predicts preferred bone formation on the periosteal surface, we demonstrate that additional consideration of the LCN architecture not only corrects this erroneous bias in the prediction but also explains observed differences in the mechanosensitivity between the three investigated mice. We also identified the presence of vascular channels as an important mechanism to locally reduce fluid flow. Flow velocities increased for a convergent network structure where all of the flow is channeled into fewer canaliculi. We conclude that, besides mechanical loading, LCN architecture should be considered as a key determinant of bone adaptation.

Bone adaptation: Safety factors and load predictability in shaping skeletal form.

Much is known about skeletal adaptation in relation to the mechanical functions that bones serve. This includes how bone adapts to mechanical loading during an individual's lifetime as well as over evolutionary time. Although controlled loading in animal models allows us to observe short-term bone adaptation (epigenetic mechanobiology), examining an assemblage of extant vertebrate bones or a group of fossils' bony structures can reveal the combined effects of long-term trends in loading history and the effects of natural selection. In this survey we examine adaptations that take place over both time scales and highlight a few of the extraordinary insights first published by John Currey. First, we provide a historical perspective on bone adaptation control mechanisms, followed by a discussion of safety factors in bone. We then summarize examples of structural- and material-level adaptations and mechanotransduction, and analyze the relationship between these structural- and material-level adaptations observed in situations where loading modes are either predictable or unpredictable. We argue that load predictability is a major consideration for bone adaptation broadly across an evolutionary timescale, but that its importance can also be seen during ontogenetic growth trajectories, which are subject to natural selection as well. Furthermore, we suggest that bones with highly predictable load patterns demonstrate more precise design with lower safety factors, while bones that experience less predictable loads or those that are less capable of repair and adaptation are designed with a higher safety factor. Finally, exposure to rare loading events with high potential costs of failure leads to design of structures with very high safety factor compared to everyday loading experience. Understanding bone adaptations at the structural and material levels, which take place over an individual's lifetime or over evolutionary time has numerous applications in translational and clinical research to understand and treat musculoskeletal diseases, as well as to permit the furthering of human extraterrestrial exploration in environments with altered gravity.