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.     

Spatial distribution of osteocyte lacunae in equine radii and third metacarpals: considerations for cellular communication, microdamage detection and metabolism

Osteocytes, which are embedded in bone matrix, are the most abundant cells in bone. Despite the ideal location of osteocytes to sense the local environment and influence bone remodeling, their functions, and the relative importance of these functions, remain controversial. In this study, we tested several hypotheses that address the possibilities that population densities of osteocyte lacunae (Ot.Lc.N/B.Ar) correlate with strain-, remodeling- or metabolism-related aspects of the local biomechanical environments of mid-third diaphyseal equine radii and third metacarpals from skeletally mature animals. Ot.Lc.N/B.Ar data, quantified in multiple cortical locations, were analyzed for possible correlations with (1) structural and material characteristics (e.g., cortical thickness, percent ash, secondary osteon population density, mean osteon cross-sectional area, and predominant collagen fiber orientation), (2) strain characteristics, including prevalent/predominant strain magnitude and mode (tension, compression, shear), (3) hypothesized strain-mode-related microdamage characteristics, which might be perceived by osteocyte 'operational' networks, and (4) variations in remodeling dynamics and/or metabolism (i.e. presumably higher in endocortical regions than in other transcortical locations). Results showed relatively uniform Ot.Lc.N/B.Ar between regions with highly non-uniform strain and strain-related environments and markedly heterogeneous structural and material organization. These results suggest that population densities of these cells are poorly correlated with mechanobiological characteristics, including local variations in metabolic rate and strain magnitude/mode. Although osteocytes hypothetically evolved both as strain sensors and fatigue damage sensors able to direct the removal of damage as needed, the mechanisms that govern the distribution of these cells remain unclear. The results of this study provide little or no evidence that the number of osteocyte lacunae has a functional role in mechanotransduction pathways that are typically considered in bone adaptation.     

Analysis of the Effect of Osteon Diameter on the Potential Relationship of Osteocyte Lacuna Density and Osteon Wall Thickness

An important hypothesis is that the degree of infilling of secondary osteons (Haversian systems) is controlled by the inhibitory effect of osteocytes on osteoblasts, which might be mediated by sclerostin (a glycoprotein produced by osteocytes). Consequently, this inhibition could be proportional to cell number: relatively greater repression is exerted by progressively greater osteocyte density (increased osteocytes correlate with thinner osteon walls). This hypothesis has been examined, but only weakly supported, in sheep ulnae. We looked for this inverse relationship between osteon wall thickness (On.W.Th) and osteocyte lacuna density (Ot.Lc.N/B.Ar) in small and large osteons in human ribs, calcanei of sheep, deer, elk, and horses, and radii and third metacarpals of horses. Analyses involved: (1) all osteons, (2) smaller osteons, either ≤150 μm diameter or less than or equal to the mean diameter, and (3) larger osteons (>mean diameter). Significant, but weak, correlations between Ot.Lc.N/B.Ar and On.W.Th/On.Dm (On.Dm = osteon diameter) were found when considering all osteons in limb bones (r values ?0.16 to ?0.40, P < 0.01; resembling previous results in sheep ulnae: r = ?0.39, P < 0.0001). In larger osteons, these relationships were either not significant (five/seven bone types) or very weak (two/seven bone types). In ribs, a negative relationship was only found in smaller osteons (r = ?0.228, P < 0.01); this inverse relationship in smaller osteons did not occur in elk calcanei. These results do not provide clear or consistent support for the hypothesized inverse relationship. However, correlation analyses may fail to detect osteocyte‐based repression of infilling if the signal is spatially nonuniform (e.g., increased near the central canal). Anat Rec,, 2011. © 2011 Wiley‐Liss, Inc.     

Histomorphometric assessment of Haversian canal and osteocyte lacunae in different-sized osteons in human rib

There is no detailed information available concerning the variations in bone, the Haversian canal, and osteocyte populations in different-sized osteons. In this study a total of 398 secondary osteons were measured in archived rib sections from nine white men (20-25 years old). The sections were stained with basic fuchsin. The parameters included the osteon area (On.Ar), Haversian canal area (HC.Ar) and perimeter (HC.Pm), bone area (B.Ar), and osteocyte lacunar number (Lc.N). From these primary measurements the following indices were deduced: 1) lacunar number per bone area (Lc.N/B.Ar) and per osteon (Lc.N/On); 2) the ratio between Haversian canal perimeter and bone area (HC.Pm/B.Ar); and 3) the fraction of Haversian canal area (HC.Ar/On.Ar) and its complement, the fraction of bone area (B.Ar/On.Ar). The results showed that the osteons varied greatly in size, but very little in the fraction of bone area. Regression analyses showed that HC.Ar, HC.Pm, and Lc.N/On were positively associated with On.Ar (P < 0.001 for all). A significant negative correlation was found between On.Ar and Lc.N/B.Ar (P < 0.05) and HC.Pm/B.Ar (P < 0.0001). HC.Ar and HC.Pm increased significantly with increasing Lc.N/On (both P < 0.0001) rather than Lc.N/B.Ar. Lc.N/B.Ar had a significant positive correlation with HC.Ar/On.Ar (P < 0.05) and HC.Pm/B.Ar (P < 0.01). We conclude that: 1) the size of the osteon is determined by the quantum of bone removed by osteoclasts, 2) the osteon is well designed for molecular exchange, and 3) a well designed osteon may be produced via the regulation of bone apposition by osteocytes during the process of osteon refilling.     

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.     

Ontogenetic and regional morphologic variations in the turkey ulna diaphysis: implications for functional adaptation of cortical bone

This study examines relationships between bone morphology and mechanically mediated strain/fluid-flow patterns in an avian species. Using mid-diaphyseal transverse sections of domestic turkey ulnae (from 11 subadults and 11 adults), we quantified developmental changes in predominant collagen fiber orientation (CFO), mineral content (%ash), and microstructure in cortical octants or quadrants (i.e., %ash). Geometric parameters were examined using whole mid-diaphyseal cross-sections. The ulna undergoes habitual bending and torsion, and demonstrates nonuniform matrix fluid-flow patterns, and high circumferential strain gradients along the neutral axis (cranial-caudal) region at mid-diaphysis. The current results showed significant porosity differences: 1) greater osteocyte lacuna densities (N.Lac/Ar) (i.e., "non-vascular porosity") in the caudal and cranial cortices in both groups, 2) greater N.Lac/Ar in the pericortex vs. endocortex in mature bones, and 3) greater nonlacunar porosity (i.e., "vascular porosity") in the endocortex vs. pericortex in mature bones. Vascular and nonvascular porosities were not correlated. There were no secondary osteons in subadults. In adults, the highest secondary osteon population densities and lowest %ash occurred in the ventral-caudal, caudal, and cranial cortices, where shear strains, circumferential strain gradients, and fluid displacements are highest. Changes in thickness of the caudal cortex explained the largest proportion of the age-related increase in cranial-caudal breadth; the thickness of other cortices (dorsal, ventral, and cranial) exhibited smaller changes. Only subadult bones exhibited CFO patterns corresponding to habitual tension (ventral) and compression (dorsal). These CFO variations may be adaptations for differential mechanical requirements in "strain-mode-specific" loading. The more uniform oblique-to-transverse CFO patterns in adult bones may represent adaptations for shear strains produced by torsional loading, which is presumably more prevalent in adults. The micro- and ultrastructural heterogeneities may influence strain and fluid-flow dynamics, which are considered proximate signals in bone adaptation.     

Ontogenetic structural and material variations in ovine calcanei: A model for interpreting bone adaptation

Experimental models are needed for resolving relative influences of genetic, epigenetic, and nonheritable functionally induced (extragenetic) factors in the emergence of developmental adaptations in limb bones of larger mammals. We examined regional/ontogenetic morphologic variations in sheep calcanei, which exhibit marked heterogeneity in structural and material organization by skeletal maturity. Cross‐sections and lateral radiographs of an ontogenetic series of domesticated sheep calcanei (fetal to adult) were examined for variations in biomechanically important structural (cortical thickness and trabecular architecture) and material (percent ash and predominant collagen fiber orientation) characteristics. Results showed delayed development of variations in cortical thickness and collagen fiber orientation, which correlate with extragenetic factors, including compression/tension strains of habitual bending in respective dorsal/plantar cortices and load‐related thresholds for modeling/remodeling activities. In contrast, the appearance of trabecular arches in utero suggests strong genetic/epigenetic influences. These stark spatial/temporal variations in sheep calcanei provide a compelling model for investigating causal mechanisms that mediate this construction. In view of these findings, it is also suggested that the conventional distinction between genetic and epigenetic factors in limb bone development be expanded into three categories: genetic, epigenetic, and extragenetic factors. Anat Rec, 2007. © 2007 Wiley‐Liss, Inc.     

Do regional modifications in tissue mineral content and microscopic mineralization heterogeneity adapt trabecular bone tracts for habitual bending? Analysis in the context of trabecular architecture of deer calcanei

Calcanei of mature mule deer have the largest mineral content (percent ash) difference between their dorsal 'compression' and plantar 'tension' cortices of any bone that has been studied. The opposing trabecular tracts, which are contiguous with the cortices, might also show important mineral content differences and microscopic mineralization heterogeneity (reflecting increased hemi-osteonal renewal) that optimize mechanical behaviors in tension vs. compression. Support for these hypotheses could reveal a largely unrecognized capacity for phenotypic plasticity - the adaptability of trabecular bone material as a means for differentially enhancing mechanical properties for local strain environments produced by habitual bending. Fifteen skeletally mature and 15 immature deer calcanei were cut transversely into two segments (40% and 50% shaft length), and cores were removed to determine mineral (ash) content from 'tension' and 'compression' trabecular tracts and their adjacent cortices. Seven bones/group were analyzed for differences between tracts in: first, microscopic trabecular bone packets and mineralization heterogeneity (backscattered electron imaging, BSE); and second, trabecular architecture (micro-computed tomography). Among the eight architectural characteristics evaluated [including bone volume fraction (BVF) and structural model index (SMI)]: first, only the 'tension' tract of immature bones showed significantly greater BVF and more negative SMI (i.e. increased honeycomb morphology) than the 'compression' tract of immature bones; and second, the 'compression' tracts of both groups showed significantly greater structural order/alignment than the corresponding 'tension' tracts. Although mineralization heterogeneity differed between the tracts in only the immature group, in both groups the mineral content derived from BSE images was significantly greater (P < 0.01), and bulk mineral (ash) content tended to be greater in the 'compression' tracts (immature 3.6%, P = 0.03; mature 3.1%, P = 0.09). These differences are much less than the approximately 8% greater mineral content of their 'compression' cortices (P < 0.001). Published data, suggesting that these small mineralization differences are not mechanically important in the context of conventional tests, support the probability that architectural modifications primarily adapt the tracts for local demands. However, greater hemi-osteonal packets in the tension trabecular tract of only the mature bones (P = 0.006) might have an important role, and possible synergism with mineralization and/or microarchitecture, in differential toughening at the trabeculum level for tension vs. compression strains.     

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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Does the degree of laminarity correlate with site‐specific differences in collagen fibre orientation in primary bone? An evaluation in the turkey ulna diaphysis

de Margerie hypothesized that preferred orientations of primary vascular canals in avian primary cortical bone mediate important mechanical adaptations. Specifically, bones that receive habitual compression, tension or bending stresses typically have cortices with a low laminarity index (LI) (i.e. relatively lower cross-sectional areas of circularly (C) orientated primary vascular canals, and relatively higher areas of canals with radial (R), oblique (O) or longitudinal (L) orientations. By contrast, bones subject to habitual torsion have a high LI (i.e. relatively higher C-orientated canal area) [LI, based on percentage vascular canal area, = C/(C + R + O + L)]. Regional variations in predominant collagen fibre orientation (CFO) may be the adaptive characteristic mediated by LI. Using turkey ulnae, we tested the hypothesis that site-specific variations in predominant CFO and LI are strongly correlated. Mid-diaphyseal cross-sections (100 +/- 5 micro m) from subadult and adult bones were evaluated for CFO and LI using circularly polarized light images of cortical octants. Results showing significant differences between mean LI of subadult (40.0% +/- 10.7%) and adult (50.9% +/- 10.4%) (P < 0.01) bones suggest that adult bones experience more prevalent/predominant torsion. Alternatively, this relationship may reflect differences in growth rates. High positive correlations between LI and predominant CFO (subadults: r = 0.735; adults: r = 0.866; P < 0.001) suggest that primary bone can exhibit potentially adaptive material variations that are independent of secondary osteon formation.     

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.     

Microdamage in bone: implications for fracture, repair, remodeling, and adaptation

Fatigue microdamage accumulates in bone as a result of physiological loading. The damage is often manifested as microcracks, which are typically 50-100 mum long. These types of cracks develop in the interstitial bone and frequently abut osteon cement lines. In vitro experimentation has shown that an accumulation of fatigue damage reduces the material properties of bone (e.g., elastic modulus). An accumulation of fatigue damage has been implicated in the etiology of stress fractures and fragility fractures. However, bone has a remarkable ability to detect and repair fatigue microdamage. This article reviews the experimental techniques for identifying and quantifying different types of microdamage in bone, the density of in vivo microcracks at different skeletal locations, the effect of microdamage on bone material properties, the role of microdamage in bone fracture, and the biological mechanisms for the detection and repair of fatigue microdamage.     

Morphologic changes associated with functional adaptation of the navicular bone of horses

Failure of functional adaptation to protect the skeleton from damage is common and is often associated with targeted remodeling of bone microdamage. Horses provide a suitable model for studying loading-related skeletal disease because horses are physically active, their exercise is usually regulated, and adaptive failure of various skeletal sites is common. We performed a histologic study of the navicular bone of three groups of horses: (1) young racing Thoroughbreds (n = 10); (2) young unshod ponies (n = 10); and (3) older horses with navicular syndrome (n = 6). Navicular syndrome is a painful condition that is a common cause of lameness and is associated with extensive remodeling of the navicular bone; a sesamoid bone located within the hoof which articulates with the second and third phalanges dorsally. The following variables were quantified: volumetric bone mineral density; cortical thickness (Ct.Th); bone volume fraction, microcrack surface density; density of osteocytes and empty lacunae; and resorption space density. Birefringence of bone collagen was also determined using circularly polarized light microscopy and disruption of the lacunocanalicular network was examined using confocal microscopy. Remodeling of the navicular bone resulted in formation of transverse secondary osteons orientated in a lateral to medial direction; bone collagen was similarly orientated. In horses with navicular syndrome, remodeling often led to the formation of intracortical cysts and development of multiple tidemarks at the articular surface. These changes were associated with high microcrack surface density, low bone volume fraction, low density of osteocytes, and poor osteocyte connectivity. Empty lacunae were increased in Thoroughbreds. Resorption space density was not increased in horses with navicular syndrome. Taken together, these data suggest that the navicular bone may experience habitual bending across the sagittal plane. Consequences of cumulative cyclic loading in horses with navicular syndrome include arthritic degeneration of adjacent joints and adaptive failure of the navicular bone, with accumulation of microdamage and associated low bone mass, poor osteocyte connectivity, and low osteocyte density, but not formation of greater numbers of resorption spaces.     

Exercise‐induced metacarpophalangeal joint adaptation in the Thoroughbred racehorse

Repetitive bone injury and development of stress fracture is a common problem in humans and animals. The Thoroughbred racehorse is a model in which adaptive failure and associated development of stress fracture is common. We performed a histologic study of the distal end of the third metacarpal bone in two groups of horses: young Thoroughbreds that were actively racing (n = 10) and a group of non‐athletic horses (n = 8). The purpose of this study was to determine whether development of articular microcracks was associated with specific alterations to subchondral plate osteocytes. Morphometric measurements were made in five regions of the joint surface: lateral condyle, lateral condylar groove, sagittal ridge, medial condylar groove, and medial condyle. The following variables were quantified: hyaline cartilage width; calcified cartilage width; the number of tidemarks; microcrack density at the articular surface; blood vessel density entering articular cartilage; the presence of atypical bone matrix in the subchondral plate; bone volume fraction; and osteocyte density. Adaptation of articular cartilage was similar in both groups of horses. Vascularization of articular cartilage was increased in the group of non‐athletic horses. Microcracks, which typically had an oblique orientation to the joint surface, were co‐localized with blood vessels, and resorption spaces. Microcracking was increased in the condylar grooves of athletic horses compared with the other joint regions and was also increased compared with the condylar groove regions of non‐athletic horses. Coalescence of microcracks also led to development of an intracortical articular condylar stress fracture in some joints and targeted remodeling of affected subchondral plate. The subchondral plate of the condyles in athletic horses was sclerotic, and contained atypically stained bone matrix with increased numbers of osteocytes with atypical morphology. However, osteocyte numbers were not significantly different between groups. We conclude that differences in site‐specific microdamage accumulation and associated targeted remodeling between athletic and non‐athletic horses are much greater than differences in subchondral osteocyte morphology. However, the presence of atypical subchondral bone matrix in athletic horses was associated with extensive osteocyte loss. Although osteocyte mechanotransduction is considered important for functional adaptation, in this model, adaptation is likely regulated by multiple mechanotransduction pathways.     

Insertion of the abductor hallucis muscle in feet with and without hallux valgus

Textbooks of human anatomy present different opinions on the insertion of the abductor hallucis muscle which is concerned in etiology as well as in therapy of hallux valgus. In plastic and reconstructive surgery the muscle is taken as a graft for flap-surgery. In this study 109 feet (58 right, 51 left) were examined, 18 of these with clinical hallux valgus. The tendon of the muscle may attach to the tendon of the medial head of the short flexor hallucis muscle where a subtendineous bursa can be found. At the head of the first metatarsal bone the joint capsule is reinforced by fibres arising from the medial sesamoid bone which may be called "medial sesamoidal ligament." The tendon passes the first metatarsophalangeal joint plantarily to its transverse axis. Three types of insertion could be distinguished: type A, insertion at the proximal phalanx (N = 42); type B, insertion at the medial sesamoid ligament and at the medial sesamoid bone (N = 65); type C, insertion at the medial sesamoid bone (N = 2). In all types superficial fibres of the tendon extended to the medial and plantar sides of the base of the proximal phalanx, running in a plantar to dorsal direction. Statistical analysis exposed neither significant differences between both sides nor significant difference between normal feet and feet with hallux valgus. Therefore, a specific pattern of insertion of the abductor hallucis muscle in hallux valgus cannot be stated.     

Sexual dimorphism and age dependence of osteocyte lacunar density for human vertebral cancellous bone

The sexual dimorphism in age-related loss of human vertebral cancellous bone is not fully understood and could be related to dimorphism in the bone cell populations. The objective of this study was to investigate age- and gender-related differences in the osteocyte population and its relationship with bone volume fraction for human vertebral cancellous bone. Histomorphometric techniques were used to quantify osteocyte lacunae (a measure of osteocyte population) and bone volume fraction in male and female human T12 vertebrae, the most common site of vertebral fracture. Two measures of osteocyte population [number of osteocytes per bone area (OtLcDn) and number of osteocytes per total area (OtLcN/TA)] and their relationships with age and bone volume fraction were found to be sexually dimorphic. Dimorphism in osteocyte density may explain the dimorphic patterns of bone loss in human vertebrae due to the sensory and signal communication functions that osteocytes perform.     

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. © 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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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.     

SL-2000骨疲劳损伤实验机的研制与应用

研制专门用于离体骨组织疲劳损伤研究的疲劳损伤实验装置,获得骨微损伤用于分析骨的力学性能。根据工业疲劳机及骨疲劳实验的一般原理,自动控制疲劳实验的主要参数包括负载大小、负载频率、负载次数、温度和湿度,达到疲劳损伤实验条件等。研制的SL-2000骨疲劳损伤实验机在0~200 N负载力量、0~10 H z负载频率、0~999999负载次数、~50℃环境温度和~99%环境湿度范围内连续可调。应用该机对大鼠椎体骨疲劳损伤后可以观察到微破裂、染色性弥散性损伤和染色性交叉岔折三种微损伤类型。骨微破裂密度为19.76±15.05#/mm2,微破裂平均长度为36.74±11.51μm,骨染色性弥散性损伤面积比为0.4117%。实验证明该机适合于骨组织疲劳损伤实验,用于建立骨微损伤模型。