Differences in osteonal micromorphology between tensile and compressive cortices of a bending skeletal system: Indications of potential strain-specific differences in bone microstructure

Background: It has been hypothesized that bone has the capacity to accommodate regional differences in tension and compression strain mode and/or magnitude by altering its osteonal microstructure. We examined a simple cantilevered bone to determine whether regional differences in particular strain-related features are reflected in the microstructural organization of compact bone. Methods & Results: The artiodactyl (e.g., sheep and deer) calcaneus has a predominant loading condition which is typified by prevailing compressive and tensile strains on opposite cortices, and variations in strain magnitudes across each of these cortices. Microscopic examination showed osteon density and cortical porosity differences between tension (caudal) and compression (cranial) cortices, averaging 11.4% more osteons in the compression cortex (P < 0.01) and 80.2% greater porosity in the tension cortex (P < 0.01). There is 43.5% more interstitial bone in the compression cortex (P < 0.01). Osteons in the compression cortex also have smaller areas in contrast to the larger area per osteon in the tension cortex. Although no definite transcortical gradient in osteonal density or cortical porosity is found, fractional area of interstitial bone is largest and osteon population density is lowest in the endocortical regions of both tension and compression cortices. The endocortical regions also have greater porosity than their corresponding middle and pericortical regions (P < 0.01). Conclusions: These osteonal microstructure and cortical porosity differences may be adaptations related to regional differences in strain mode and/or strain magnitude. This may be related to the disparity in mechanical properties of compact bone in tension vs. compression. These differences may reflect a capacity of bone to process local and regional strain-related information. © 1994 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, is in the public dotmain in the United states of America

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Advancing the deer calcaneus model for bone adaptation studies: ex vivo strains obtained after transecting the tension members suggest an unrecognized important role for shear strains

Sheep and deer calcanei are finding increased use as models for studies of bone adaptation, including advancing understanding of how the strain (deformation) environment influences the ontogenetic emergence of biomechanically relevant structural and material variations in cortical and trabecular bone. These artiodactyl calcanei seem ideal for these analyses because they function like simply loaded short‐cantilevered beams with net compression and tension strains on the dorsal and plantar cortices, respectively. However, this habitual strain distribution requires more rigorous validation because it has been shown by limited in vivo and ex vivo strain measurements obtained during controlled ambulation (typically walking and trotting). The conception that these calcanei are relatively simply and habitually loaded ‘tension/compression bones’ could be invalid if infrequent, though biologically relevant, loads substantially change the location of the neutral axis (NA) that separates ‘compression’ and ‘tension’ regions. The effect on calcaneus strains of the tension members (plantar ligament and flexor tendon) is also not well understood and measuring strains after transecting them could reveal that they significantly modulate the strain distribution. We tested the hypothesis that the NA location previously described during simulated on‐axis loads of deer calcanei would exhibit limited variations even when load perturbations are unusual (e.g. off‐axis loads) or extreme (e.g. after transection of the tension members). We also examined regional differences in the predominance of the three strain modes (tension, compression, and shear) in these various load conditions in dorsal, plantar, medial, and lateral cortices. In addition to considering principal strains (tension and compression) and maximum shear strains, we also considered material‐axis (M‐A) shear strains. M‐A shear strains are those that are aligned along the long axis of the bone and are considered to have greater biomechanical relevance than maximum shear strains because failure theories of composite materials and bone are often based on stresses or strains in the principal material directions. We used the same load apparatus from our prior study of mule deer calcanei. Results showed that although the NA rotated up to 8° medially and 15° laterally during these off‐axis loads, it did not shift dramatically until after transection of all tension members. When comparing results based on maximum shear strain data vs. M‐A shear strain data, the dominant strain mode changed only in the plantar cortex – as expected (in accordance with our a priori view) it was tension when M‐A shear strains were considered (shear : tension = 0.2) but changed to dominant shear when maximum shear strain data were considered (shear : tension = 1.3). This difference leads to different conclusions and speculations regarding which specific strain modes and magnitudes most strongly influence the emergence of the marked mineralization and histomorphological differences in the dorsal vs. plantar cortices. Consequently, our prior simplification of the deer calcaneus model as a simply loaded ‘tension/compression bone’ (i.e. plantar/dorsal) might be incorrect. In vivo and in finite element analyses are needed to determine whether describing it as a ‘shear‐tension/compression’ bone is more accurate. Addressing this question will help to advance the artiodactyl calcaneus as an experimental model for bone adaptation studies.     

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

The 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.     

Modeling and remodeling in a developing artiodactyl calcaneus: a model for evaluating Frost's Mechanostat hypothesis and its corollaries

The artiodactyl (mule deer) calcaneus was examined for structural and material features that represent regional differences in cortical bone modeling and remodeling activities. Cortical thickness, resorption and formation surfaces, mineral content (percent ash), and microstructure were quantified between and within skeletally immature and mature bones. These features were examined to see if they are consistent with predictions of Frost's Mechanostat paradigm of mechanically induced bone adaptation in a maturing "tension/compression" bone (Frost, 1990a,b, Anat Rec 226:403-413, 414-422). Consistent with Frost's hypothesis that surface modeling activities differ between the "compression" (cranial) and "tension" (caudal) cortices, the elliptical cross-section of the calcaneal diaphysis becomes more elongated in the direction of bending as a result of preferential (> 95%) increase in thickness of the compression cortex. Regional differences in mineral content and population densities of new remodeling events (NREs = resorption spaces plus newly forming secondary osteons) support Frost's hypothesis that intracortical remodeling activities differ between the opposing cortices: 1.) in immature and mature bones, the compression cortex had attained a level of mineralization averaging 8.9 and 6.8% greater (P < 0.001), respectively, than that of the tension cortex, and 2.) there are on average 350 to 400% greater population densities of NREs in the tension cortices of both age groups (P < 0.0003). No significant differences in cortical thickness, mineral content, porosity, or NREs were found between medial and lateral cortices of the skeletally mature bones, suggesting that no modeling or remodeling differences exist along a theoretical neutral axis. However, in mature bones these cortices differed considerably in secondary osteon cross-sectional area and population density. Consistent with Frost's hypothesis, remodeling in the compression cortex produced bone with microstructural organization that differs from the tension cortex. However, the increased remodeling activity of the tension cortex does not appear to be related to a postulated low-strain environment. Although most findings are consistent with predictions of Frost's Mechanostat paradigm, there are several notable inconsistencies. Additional studies are needed to elucidate the nature of the mechanisms that govern the modeling and remodeling activities that produce and maintain normal bone. It is proposed that the artiodactyl calcaneus will provide a useful experimental model for these studies.     

Mechanical implications of collagen fibre orientation in cortical bone of the equine radius

Mechanical test specimens were prepared from the cranial and caudal cortices of radii from eight horses. These were subjected to destructive tests in either tension or compression. The ultimate stress, elastic modulus and energy absorbed to failure were calculated in either mode of loading. Analysis was performed on the specimens following mechanical testing to determine their density, mineral content, mineral density distribution and histological type. A novel technique was applied to sections from each specimen to quantify the predominant collagen fibre orientation of the bone near the plane of fracture. The collagen map for each bone studied was in agreement with the previously observed pattern of longitudinal orientation in the cranial cortex and more oblique to transverse collagen in the caudal cortex. Bone from the cranial cortex had a significantly higher ultimate tensile stress (UTS) than that from the caudal cortex (160 MPa vs 104 MPa; P<0.001) though this trend was reversed in compression, the caudal cortex becoming relatively stronger (185 MPa vs 217 MPa; P<0.01). Bone from the cranial cortex was significantly suffer than that from the caudal cortex both in tension (22 GPa vs 15 GPa; P<0.001) and compression (19 GPa vs 15 GPa; P<0.01). Of all the histo-compositional variables studied, collagen fibre orientation was most closely correlated with mechanical properties, accounting for 71% of variation in ultimate tensile stress and 58% of variation in the elastic modulus. Mineral density and porosity were the only other variables to show any significant correlation with either UTS or elastic modulus. The variations in mechanical properties around the equine radius, which occur in close association with the different collagen fibre orientations, provide maximal safety factors in terms of ultimate stress, yet contribute to greater bending of the bone as it is loaded during locomotion, and thus lower safety factors through the higher strains this engenders.     

Pattern of collagen fiber orientation in the ovine calcaneal shaft and its relation to locomotor-induced strain

Background: Gebhardt (1905. Arch. Entwickl. Org., 20:187–322) originated the hypothesis that the direction of collagen fibers in bone is a structural response to the type of mechanical load to which the bone is subjected. He proposed that collagen fibers aligned parallel to the loading axis are best suited to withstand tensile strain, whereas fibers oriented perpendicular to the loading axis are best able to resist compressive strain. Research comparing load patterns with fiber alignment in bone have tended to support Gebhardt's hypothesis. The aim of the present study is to further test this hypothesis by assessing the correspondence between the distribution of strain and the distribution of collagen fiber orientation in a bone that is subjected to compound loading (i.e., both tension and compression at different phases during the loading cycle). The ovine calcaneum was selected to meet this criterion. Methods: Calcaneum surface strain distributions were obtained from experimental results reported by Lanyon (1973. J. Biomech. 6:41–49). Histological sections of the calcaneal shaft were prepared and observed using circularly polorized light (CPL) microscopy to determine the distribution of collagen fiber alignment. The observed alignment pattern was then compared with the predicted pattern based on Gebhardt's hypothesis. Results: Contrary to previous studies, our findings show no clear correspondence between the strain type of greatest magnitude and the direction of collagen fibers. Areas of bone characterized by high compression and low tension showed predominantly longitudinal collagen alignment (contra to Gebhardt). Conclusions: It is argued that even small magnitudes of tension operating on local areas of bone may be sufficient to induced collagen alignment favorable to this type of strain, even when greater magnitudes of compressive strain are acting on the same bone volume. © 1995 Wiley-Liss, Inc.     

Relationships between in vivo microdamage and the remarkable regional material and strain heterogeneity of cortical bone of adult deer, elk, sheep and horse calcanei

Natural loading of the calcanei of deer, elk, sheep and horses produces marked regional differences in prevalent/predominant strain modes: compression in the dorsal cortex, shear in medial-lateral cortices, and tension/shear in the plantar cortex. This consistent non-uniform strain distribution is useful for investigating mechanisms that mediate the development of the remarkable regional material variations of these bones (e.g. collagen orientation, mineralization, remodeling rates and secondary osteon morphotypes, size and population density). Regional differences in strain-mode-specific microdamage prevalence and/or morphology might evoke and sustain the remodeling that produces this material heterogeneity in accordance with local strain characteristics. Adult calcanei from 11 animals of each species (deer, elk, sheep and horses) were transversely sectioned and examined using light and confocal microscopy. With light microscopy, 20 linear microcracks were identified (deer: 10; elk: six; horse: four; sheep: none), and with confocal microscopy substantially more microdamage with typically non-linear morphology was identified (deer: 45; elk: 24; horse: 15; sheep: none). No clear regional patterns of strain-mode-specific microdamage were found in the three species with microdamage. In these species, the highest overall concentrations occurred in the plantar cortex. This might reflect increased susceptibility of microdamage in habitual tension/shear. Absence of detectable microdamage in sheep calcanei may represent the (presumably) relatively greater physical activity of deer, elk and horses. Absence of differences in microdamage prevalence/morphology between dorsal, medial and lateral cortices of these bones, and the general absence of spatial patterns of strain-mode-specific microdamage, might reflect the prior emergence of non-uniform osteon-mediated adaptations that reduce deleterious concentrations of microdamage by the adult stage of bone development.     

Collagen fiber orientation pattern,osteon morphology and distribution,and presence of laminar histology do not distinguish torsion from bending in bat and pigeon wing bones

Bone can adapt to its habitual load history at various levels of its hierarchical structural and material organization. However, it is unclear how strongly a bone's structural characteristics (e.g. cross‐sectional shape) are linked to microstructural characteristics (e.g. distributions of osteons and their vascular canals) or ultrastructural characteristics [e.g. patterns of predominant collagen fiber orientation (CFO)]. We compared the cross‐sectional geometry, microstructure and ultrastructure of pigeon (Columba livia domestica) humeri, and third metacarpals (B3M) and humeri of a large bat (Pteropus poliocephalus). The pigeon humerus is habitually torsionally loaded, and has unremodeled (‘primary’) bone with vessels (secondary osteons are absent) and high ‘laminarity’ because a large majority of these vessels course circularly with respect to the bone's external surface. In vivo data show that the bat humerus is also habitually torsionally loaded; this contrasts with habitual single‐plane bending of the B3M, where in vivo data show that it oscillates back and forth in the same direction. In contrast to pigeon humeri where laminar bone is present, the primary tissue of these bat bones is largely avascular, but secondary osteons are present and are usually in the deeper cortex. Nevertheless, the load history of humeri of both species is prevalent/predominant torsion, producing diffusely distributed shear stresses throughout the cross‐section. We tested the hypothesis that despite microstructural/osteonal differences in these pigeon and bat bones, they will have similar characteristics at the ultrastructural level that adapt each bone for its load history. We postulate that predominant CFO is this characteristic. However, even though data reported in prior studies of bones of non‐flying mammals suggest that CFO would show regional variations in accordance with the habitual ‘tension regions’ and ‘compression regions’ in the direction of unidirectional habitual bending, we hypothesized that alternating directions of bending within the same plane would obviate these regional/site‐specific adaptations in the B3M. Similarly, but for other reasons, we did not expect regional variations in CFO in the habitually torsionally loaded bat and pigeon humeri because uniformly oblique‐to‐transverse CFO is the adaptation expected for the diffusely distributed shear stresses produced by torsion/multidirectional loads. We analyzed transverse sections from mid‐diaphyses of adult bones for CFO, secondary osteon characteristics (size, shape and population density), cortical thickness in quadrants of the cortex, and additional measures of cross‐sectional geometry, including the degree of circular shape that can help distinguish habitual torsion from bending. Results showed the expected lack of regional CFO differences in quasi‐circular shaped, and torsionally loaded, pigeon and bat humeri. As expected, the B3M also lacked CFO variations between the opposing cortices along the plane of bending, and the quasi‐elliptical cross‐sectional shape and regional microstructural/osteonal variations expected for bending were not found. These findings in the B3M show that uniformity in CFO does not always reflect habitual torsional loads. Osteon morphology and distribution, and presence of laminar histology also do not distinguish torsion from bending in these bat and pigeon wing bones.     

Differences in the mechanical behavior of cortical bone between compression and tension when subjected to progressive loading

The hierarchical arrangement of collagen and mineral into bone tissue presumably maximizes fracture resistance with respect to the predominant strain mode in bone. Thus, the ability of cortical bone to dissipate energy may differ between compression and tension for the same anatomical site. To test this notion, we subjected bone specimens from the anterior quadrant of human cadaveric tibiae to a progressive loading scheme in either uniaxial tension or uniaxial compression. One tension (dog-bone shape) and one compression specimen (cylindrical shape) were collected each from tibiae of nine middle aged male donors. At each cycle of loading-dwell-unloading-dwell-reloading, we calculated maximum stress, permanent strain, modulus, stress relaxation, time constant, and three pathways of energy dissipation for both loading modes. In doing so, we found that bone dissipated greater energy through the mechanisms of permanent and viscoelastic deformation in compression than in tension. On the other hand, however, bone dissipated greater energy through the release of surface energy in tension than in compression. Moreover, differences in the plastic and viscoelastic properties after yielding were not reflected in the evolution of modulus loss (an indicator of damage accumulation), which was similar for both loading modes. A possible explanation is that differences in damage morphology between the two loading modes may favor the plastic and viscoelastic energy dissipation in compression, but facilitate the surface energy release in tension. Such detailed information about failure mechanisms of bone at the tissue-level would help explain the underlying causes of bone fractures.     

A Device for Long Term, <Emphasis Type="Italic">In Vitro</Emphasis> Loading of Three-Dimensional Natural and Engineered Tissues

In vitro studies of mechanical loads applied to three-dimensional tissue constructs are important to the design and production of functional, engineered bone tissue. This study reports the development and characterization of a mechanical device capable of subjecting a three-dimensional section of natural or engineered tissue to precise, reproducible four-point bending deformations over a range of programmable magnitudes and frequencies. To test the biological and mechanical capabilities of the system, a low-cycle (360 cycles/day), medium-range strain (2500 microstrain), long-term (16 day) loading regime was applied to rat bone marrow stromal cells cultured in porous DL-polylactic acid scaffolds. Cells proliferated in culture throughout the experiment, and with time showed an increase in alkaline phosphatase expression per cell. Calcium and phosphorus mineral deposition by the unloaded group was significantly greater (p < 0.05) than that deposited by the loaded group. The molar ratio of calcium to phosphorus in the unloaded group (0.94:1) was significantly greater (p < 0.05) than that of the loaded group (0.41:1). The loading device presented here is a tool which can be used to help elucidate contributions of mechanical loading/fatigue on biodegradable materials, as well as study the effects of mechanical loading on natural or engineered tissues in vitro. © 2003 Biomedical Engineering Society. PAC2003: 8768+z, 8780Rb     

Strain response of an instrumented intramedullary nail to three-point bending

Objectives:?An experimental biomechanical evaluation of an instrumented intramedullary nail (TriGen® META Nail, Smith&Nephew®) was undertaken. The objectives were two-fold. The first was to identify the most sensitive strain gauge positions and orientations on the nail, and the second was to demonstrate that the nail was capable of detecting changes in stiffness of the nail–bone composite. The function of the instrumented nail is to quantify fracture healing objectively and directly, and so to predict delayed repair or non-union 2 months before current methods.

Methods:?Eight flat pockets were machined onto the surface of the nail and three strain gauges attached in each pocket. The instrumented nail was inserted into fourth generation biomechanical grade Sawbones® tibiae with three different fracture configurations as well as into a non-fractured bone. The nail–bone composite was loaded in three-point bending at five positions to determine the strain changes in each of the eight strain gauge pockets located along the length of the nail. To simulate callus in the simplest way and to increase the stiffness of the nail–bone composite, loops of duct tape in multiples of four were applied over the fracture locus. A three-point loading jig was used to obtain the change in strain with increasing stiffness. Relative displacement of the bone ends was quantified using radiostereometric analysis.

Results:?There was no single position of greatest strain sensitivity for all fracture types. The greatest change in strain occurred when the strain gauge pocket and fracture line were closest. Applying the loading moment directly over the strain gauge pocket also maximised its sensitivity. The duct tape callus simulation showed that the instrumented nail was able to detect a change in stiffness of less than 4.1 Nm/°.

Conclusions:?It has been shown that the instrumented nail can detect physiologically relevant changes in stiffness, and so to provide a useful function as an objective monitor of fracture repair.     

Mandibular corpus bone strain in goats and alpacas: Implications for understanding the biomechanics of mandibular form in selenodont artiodactyls

The goal of this study is to clarify the functional and biomechanical relationship between jaw morphology and in vivo masticatory loading in selenodont artiodactyls. We compare in vivo strains from the mandibular corpus of goats and alpacas to predicted strain patterns derived from biomechanical models for mandibular corpus loading during mastication. Peak shear strains in both species average 600–700 µɛ on the working side and approximately 450 µɛ on the balancing side. Maximum principal tension in goats and alpacas is directed at approximately 30° dorsocaudally relative to the long axis of the corpus on the working side and approximately perpendicular to the long axis on the balancing side. Strain patterns in both species indicate primarily torsion of the working-side corpus about the long axis and parasagittal bending and/or lateral transverse bending of the balancing-side corpus. Interpretation of the strain patterns is consistent with comparative biomechanical analyses of jaw morphology suggesting that in goats, the balancing-side mandibular corpus is parasagittally bent whereas in alpacas it experiences lateral transverse bending. However, in light of higher working-side corpus strains, biomechanical explanations of mandibular form also need to consider that torsion influences relative corpus size and shape. Furthermore, the complex combination of loads that occur along the selenodont artiodactyl mandibular corpus during the power stroke has two implications. First, added clarification of these loading patterns requires in vivo approaches for elucidating biomechanical links between mandibular corpus morphology and masticatory loading. Second, morphometric approaches may be limited in their ability to accurately infer masticatory loading regimes of selenodont artiodactyl jaws.     

Functional associations between collagen fibre orientation and locomotor strain direction in cortical bone of the equine radius

A novel technique for determining the collagen fibre orientation pattern of cross-sections of cortical bone was used to study mid-diaphyseal sections from the equine radius. Several in vivo strain gauge studies have demonstrated that this bone is loaded in bending during locomotion in such a way that the cranial cortex is consistently subjected to longitudinal tensile strains and the caudal cortex to longitudinal compressive strains. Twenty-three radii from 17 horses were studied. All the bones obtained from adult horses exhibited a consistent pattern of collagen fibre orientation across the cortex. The cranial cortex, subjected to intermittent tension, and the lateral and medial cortices, through which the neutral axis passes, contained predominantly longitudinally oriented collagen fibres. The caudal cortex, subjected to longitudinal compression during life, contained predominantly oblique/transverse collagen. This pattern was less evident in bones from foals. Microscopic analysis of the bones studied showed that primary lamellar bone was composed of predominantly longitudinal collagen fibres, irrespective of cortex. However, there was a strong relationship between cortical location and fibre orientation within remodelled bone. Secondary osteons which formed in the caudal (compressive) cortex contained predominantly oblique/transverse collagen, while those which formed elsewhere contained longitudinal collagen. This observation explained the developmental appearance of the characteristic macroscopic pattern of collagen fibre orientation across the whole cortex in the adult. These findings provide evidence for the existence of a relationship between the mechanical function of a bone with its architecture, and now demonstrate that it extends to the molecular level.     

Histological organization and its relationship to function in the femur of Alligator mississippiensis

Histological analysis of a growth series of alligator femora tests the correlation between strain milieu and microstructure. From mid‐diaphyseal cross‐sections of these femora (n = 7), vascular canal orientation and density as well as collagen fibre organization were recorded. Throughout ontogeny, the proportion of transverse–spiral (TS) collagen in the dorsal cortex is significantly greater than it is in the ventral cortex (P = 0.008). This regional difference in the proportion of TS collagen is correlated with a regional difference in the state of peak principal strain (compressive or tensile). Nevertheless, the predominant orientation of collagen fibres is longitudinal, which is inconsistent with biomechanical hypotheses that involve peak principal or shear strains. Although the density and orientation of vascular canals do not show significant regional differences (P = 0.26 and P = 0.26, respectively), as with collagen orientation, the vascular canal orientation is predominantly longitudinal. The longitudinal organization of both the vascular canals and the collagen fibres is probably a consequence of longitudinal shifting of subperiosteal osteoid during femoral lengthening. When taken together, these data suggest that growth dynamics is the dominant influence on the histological organization of primary bony tissues in alligator femora.     

Net change in periosteal strain during stance shift loading after surgery correlates to rapid de novo bone generation in critically sized defects

In an ovine femur model, proliferative woven bone fills critically sized defects enveloped by periosteum within 2 weeks of treatment with the one-stage bone-transport surgery. We hypothesize that mechanical loading modulates this process. Using high-definition optical strain measurements we determined prevailing periosteal strains for normal and surgically treated ovine femora subjected ex vivo to compressive loads simulating in vivo stance shifting (n = 3 per group, normal vs. treated). We determined spatial distribution of calcein green, a label for bone apposition in first the 2 weeks after surgery, in 15°, 30°, and 45° sectors of histological cross sections through the middle of the defect zone (n = 6 bones, three to four sections per bone). Finally, we correlated early bone formation to either the maximal periosteal strain or the net change in maximal periosteal strain. We found that treatment with the one-stage bone-transport surgery profoundly changes the mechanical environment of cells within the periosteum during stance shift loading. The pattern of early bone formation is repeatable within and between animals and relates significantly to the actual strain magnitude prevailing in the periosteum during stance shift loading. Interestingly, early bone apposition after the surgery correlates well to the maximal net change in strain (above circa 2000–3000 με, in tension or compression) rather than strain magnitude per se, providing further evidence that changes in cell shape may drive mechanoadaptation by progenitor cells. These important insights regarding mechanobiological factors that enhance rapid bone generation in critically sized defects can be translated to the tissue and organ scale, providing a basis for the development of best practices for clinical implementation and the definition of movement protocols to enhance the regenerative effect.     

Assessment of the initial viscoelastic properties of a critical segmental long bone defect reconstructed with impaction bone grafting and intramedullary nailing

IntroductionThis study compared the initial viscoelastic properties of a segmental tibial defect stabilized with intramedullary nailing and impaction bone grafting to that of a transverse fracture stabilized with intramedullary nailing.Materials and methodsSeven sheep tibiae were tested in compression (1000 N), bending and torsion (6 Nm) in a six degree-of-freedom hexapod robot. Tests were repeated across three groups: intact tibia (Intact), transverse fracture stabilized by intramedullary nailing (Fracture), and segmental defect stabilized with a nail and impaction bone grafting (Defect). Repeated measures ANOVA on the effect of group on stiffness/phase angle were conducted for each loading direction.ResultsThe Intact group was significantly stiffer than the Fracture and Defect groups in bending and torsion (p < 0.022 for both loading directions), and was marginal for the Defect group in compression (p = 0.052). No significant differences were found between the Fracture and Defect groups (p > 0.246 for all loading directions) for stiffness/phase angle. In compression and bending, phase angles were significantly greater for the Fracture and Defect groups compared to Intact (p < 0.025), with no significant differences between groups in torsion (p = 0.13). Sensitivity analyses conducted between the Fracture and Defect group differences found that they were not of clinical significance.ConclusionThe initial properties of a segmental defect stabilized with intramedullary nailing and impaction bone grafting was not clinically significantly different to that of a transverse fracture stabilized with intramedullary nailing.     

Mechanisms governing the inelastic deformation of cortical bone and application to trabecular bone

To understand the inelastic response of bone, a three-part investigation has been conducted. In the first, unload/reload tests have been used to characterize the hysteresis and provide insight into the mechanisms causing the strain. The second part devises a model for the stress/strain response, based on understanding developed from the measurements. The model rationalizes the inelastic deformation in tension, as well as the permanent strain and hysteresis. In the third part, a constitutive law representative of the deformation is selected and used to illustrate the coupled buckling and bending of ligaments that arise when trabecular bone is loaded in compression.     

Mechanotransduction of bone cells<Emphasis Type="Italic">in vitro</Emphasis>: Mechanobiology of bone tissue

Mechanical force plays an important role in the regulation of bone remodelling in intact bone and bone repair. In vitro, bone cells demonstrate a high responsiveness to mechanical stimuli. Much debate exists regarding the critical components in the load profile and whether different components, such as fluid shear, tension or compression, can influence cells in differing ways. During dynamic loading of intact bone, fluid is pressed through the osteocyte canaliculi, and it has been demonstrated that fluid shear stress stimulates osteocytes to produce signalling molecules. It is less clear how mechanical loads act on mature osteoblasts present on the surface of cancellous or trabecular bone. Although tissue strain and fluid shear stress both cause cell deformation, these stimuli could excite different signalling pathways. This is confirmed by our experimental findings, in human bone cells, that strain applied through the substrate and fluid flow stimulate the release of signalling molecules to varying extents. Nitric oxide and prostaglandin E₂ values increased by between two- and nine-fold after treatment with pulsating fluid flow (0.6±0.3 Pa). Cyclic strain (1000 μstrain) stimulated the release of nitric oxide two-fold, but had no effect on prostaglandin E₂. Furthermore, substrate strains enhanced the bone matrix protein collagen I two-fold, whereas fluid shear caused a 50% reduction in collagen I. The relevance of these variations is discussed in relation to bone growth and remodelling. In applications such as tissue engineering, both stimuli offer possibilities for enhancing bone cell growth in vitro.     

The effect of loading and ethnicity on annual changes in cortical bone of the radius and tibia in pre-pubertal children

Abstract

Background: It is unclear what effect habitual physical activity or ethnicity has on annual changes in bone size and strength in pre-pubertal children.

Aim: To determine whether the annual relative change in bone size and strength differed between high and low bone loaders and also between black and white pre-pubertal children.

Subjects and methods: Peripheral quantitative computed tomography (pQCT) scans of the 65% radius and tibia were completed on 41 black and white children (15 boys, 26 girls) between the ages of 8–11 years, at baseline and 1 year later. Children were categorised into either a high or low bone loading group from a peak bone strain score obtained from a bone-specific physical activity questionnaire. Total area (ToA), cortical area (CoA), cortical density (CoD), strength-strain index (SSI), periosteal circumference (PC), endosteal circumference (EC) and cortical thickness (CT) were assessed.

Results: There was no difference in annual relative change in radial or tibia bone size and strength between the low and high bone loaders. Black children had a greater annual relative change in CoD (p?=?0.03) and SSI (p?=?0.05) compared to the white children.

Conclusion: Children who performed high bone loading activities over a 1-year period had similar bone growth to children who did low bone loading activities over the same period. Rapid maturational growth over this period may have resulted in bone adapting to the strains of habitual physical activity placed on it. Black children may have greater tibial bone strength compared to white children due to a greater annual increase in cortical density.     

Structural Properties of a Novel Design of Composite Analogue Humeri Models

Background Mechanical analogue composite bone models have been used as cadaveric bone substitutes in a wide variety of biomechanical tests. The objective of this study was to compare the structural properties of two types (Third- and Fourth-Generation) of commercially available composite analogue humeri. Methods Eighteen of each generation composite analogue humeri were evaluated for flexural rigidity, torsional rigidity, and failure strength. Three tests were performed: medial–lateral four-point bending, anterior–posterior four-point bending, and external rotational torque. Results The Fourth-Generation analogue humeri performed more closely to the biological average with respect to failure strength, flexural rigidity, and torsional stiffness when compared to the Third-Generation humeri. Both the Third- and Fourth-Generation analogues were within the range of published human bone values. There was a statistically significant difference in strength in all modes of testing between the Fourth-Generation humeri and the Third-Generation humeri. Conclusion These composite analogue humeri are ideal for standardization in biomechanical analyses. The advantage of these humeri is that their variability is significantly lower than that of cadaveric specimens for all loading regimens. The widely varying results observed when comparing composite analogue humeri to cadaveric humeri might be derived from the use of different ranges of applied load, varied test methodologies, and diverse methods of computing the stiffness. Mechanical validation of whole Fourth-Generation humeri bone models would be an appropriate follow-up to this study with a direct comparison to cadaveric humeri. Clinical relevance This study validated and advanced our overall understanding of the capacity of composite analogue humeri to model the structural properties of human bone. Investigation was performed at the Orthopaedic Research Institute, at Wichita, KS, USA