are reduced. For instance, when the forelimbs of dogs are immobilized by a cast, the medullary cavities of bones in that limb increase in diameter due to net endosteal surface resorption [52]. This loss of bone mass is reversed with re‐introduction of normal activity, demonstrating the dynamic nature of mechanically related bone modelling.
Functional adaptation to mechanical conditions may be localized to a single bone or even to a specific site within a bone. Experimentally, external fixators used to reduce the strain environment of the tarsus of sheep induced reduced bone mineral content of the os calcis [53]. Similarly, application of a rigid external fixator to the intact ovine tibial diaphysis resulted in 50% reduction in normal functional strain magnitudes, which was associated with a progressive time‐related reduction in bone mineral content [54].
Removal of all loads on the diaphysis of the ulna in chickens resulted in predictable loss of bone mass, but this was reduced or prevented by application of only very short periods of cyclical load via pins that transfixed the bone. As few as four cycles of osteogenic strain applied once per day were sufficient to maintain the pre‐isolation bone mass [44]. Rubin et al. [55] subsequently observed a distinct strain energy component in bone in the 20–30 Hz frequency range, which they hypothesized, arose directly from muscular action. In the same avian model, others demonstrated that loss of bone mass in isolated ulnas could be prevented through sub‐physiological levels of deformation applied at a specific frequency of 30 Hz [56]. Frequency analysis of in vivo strain data from a range of different species and anatomical sites (weight‐bearing and non‐weight‐bearing) revealed that the highest strains (>1000 microstrain) occur relatively few times a day, while lower magnitude strains (<10 microstrain) occur many thousands of times per day [57]. This suggests that the predominant contribution to the strain history of a bone arises from activities not necessarily associated with vigorous locomotion. Furthermore, the application of induced electrical fields at 15, 75, and 150 Hz was found to inhibit the loss of bone mass seen in isolated avian ulnas [58].
Loss of bone at specific sites within one skeletal element is also seen following application of orthopaedic implants, both in fracture fixation and joint replacement. After a fracture, the limb is functionally impaired, which reduces loading and consequent bone strain. When a fixation device is used to stabilize the fragments, the loading close to the fracture site is further diminished because the implant provides a shared load path. Strain gauge studies, in conjunction with both internal and external fixation techniques, have confirmed the reduction in functional bone strain. Application of a dynamic compression plate (DCP) to the dorsal cortex of the sheep radius resulted in a 30% reduction in strain beneath the plate [59].
The reduction in the functional strain initiates a bone resorption response, and the use of rigid internal fixation plates is associated with both modelling and remodelling changes. This has been documented as localized increase in porosity in the cortex underlying a compression plate together with resorption of bone at the endosteal surface [60]. The effect on intracortical porosity was shown to be temporary [61] and was reduced following redesign of the plates to redistribute pressure on the periosteal surface. Conventional fixation plates applied tightly to the bone surface compress the periosteal blood vessels. It appears that the intracortical effects are due to vascular compromise, as the use of redesigned plates with lower contact (LC‐DCP) reduced intracortical porosity [62].
Endosteal resorption results from reduced mechanical loading attributed to the loss of functional activity and the load sharing between the bone and the plate. In preliminary studies, it was shown that a plate incorporating a spring section applied under tension to an intact bone did not induce strain protection under the spring section when compared with a standard DCP plate [63].
Conclusions
Bone is a remarkable tissue that has evolved to optimize its composition and structure to meet functional needs. The overall mass, geometric properties and structural components, at varying levels of scale, are constantly refined through cellular processes of modelling and remodelling to maintain optimal mechanical support with minimal tissue mass in the face of varying demands throughout an animal’s life. Healthy bone is densely populated with cells that are maintained by a rich blood supply. Just like any other tissues, bone cells are liable to disruption and death following insult. However, bone is able to repair through removal and replacement of damaged matrix or, when necessary, through regeneration to fill voids.
References
1 1 Firth, E.C., Delahunt, J., Wichtel, J.W. et al. (1999). Galloping exercise induces regional changes in bone density within the third and radial carpal bones of Thoroughbred horses. Equine Vet. J. 31: 111–115.
2 2 Murray, R.C., Vedi, S., Birch, H.L. et al. (2001). Subchondral bone thickness, hardness and remodelling are influenced by short‐term exercise in a site‐specific manner. J. Orthop. Res. 19: 1035–1042.
3 3 Murray, R.C., Branch, M.V., Dyson, S.J. et al. (2007). How does exercise intensity and type affect equine distal tarsal subchondral bone thickness? J. Appl. Physiol. 102: 2194–2200.
4 4 Simkin, P.A. (2018). Marrow fat may distribute the energy of impact loading throughout subchondral bone. Rheumatology 57: 414–418.
5 5 Clarke, B. (2008). Normal bone anatomy and physiology. Clin. J. Am. Soc. Nephrol. 3: S131–S139.
6 6 McLaughlin, B.G. and Doige, C.E. (1982). A study of carpal and tarsal bones in normal and hypothyroid foals. Can. Vet. J.: 164–168.
7 7 Marenzana, M. and Arnett, T.R. (2013). The key role of the blood supply to bone. Bone Res. 3: 203–215.
8 8 Nencini, S. and Ivanusic, J.J. (2016). The physiology of bone pain. How much do we really know? Front. Physiol. 7: 157. https://doi.org/10.3389/phys.2016.00157.
9 9 Chenu, C. (2004). Role of innervation in the control of bone remodelling. J. Musculoskelet. Neuronal Interact. 4: 132–134.
10 10 Riggs, C.M. and Evans, G.P. (1990). The microstructural basis for the mechanical properties of equine bone. Equine Vet. Educ. 2: 197–205.
11 11 Mori, R., Kodaka, T., Sano, T. et al. (2003). Comparative histology of the laminar bone between young calves and foals. Cells Tissues Organs 175: 43–50.
12 12 Burr, D.B. (2002). Targeted and nontargeted remodeling. Bone 30: 2–4.
13 13 Martin, R.B. (2002). Is all cortical bone remodeling initiated by microdamage? Bone 30: 8–13.
14 14 Lee, T.C., Mohsin, S., Taylor, D. et al. (2003). Detecting microdamage in bone. J. Anat. 203: 161–172.
15 15 Zioupos, P. (2001). Accumulation of in‐vivo fatigue microdamage and its relation to biomechanical properties in ageing human bone. J. Microsc. 201: 270–278.
16 16 Cardoso, L., Herman, B.C., Verborgt, O. et al. (2009). Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue. J. Bone Miner. Res. 24: 597–605.
17 17 Boyde, A. (2003). The real response of bone to exercise. J. Anat. 203: 173–189.
18 18 Riggs, C.M., Vaughan, L.C., Evans, G.P. et al. (1993). Mechanical implications of collagen fibre orientation in cortical bone of the equine radius. Anat. Embryol. 187: 239–248.
19 19 Aszódi, A., Bateman, J.F., Gustafsson, E. et al. (2000). Mamalian skeletogenesis and extracellular matrix: what can we learn from knockout mice? Cell Struct. Funct. 25: 73–84.
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