Utility of osteon circularity for determining species and interpreting load history in primates and nonprimates

Keenan, Kendra E.; Mears, Chad S.; Skedros, John G.

doi:10.1002/ajpa.23154

Cited by 33 publications

(40 citation statements)

References 128 publications

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“…; Keenan et al. ). One great value of this model for the translation of mechanotransduction studies to the human skeleton and other larger mammals is that it has abundant secondary osteons (Haversian systems), is relatively simply loaded, and has highly heterogeneous histomorphological organization between cortical regions that strongly correlate with specific strain characteristics of load history (Skedros et al.…”

Section: Introductionmentioning

confidence: 97%

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

Skedros

Knight

et al. 2018

Journal of Anatomy

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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 materialaxis (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 cortexas 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.Journal of ...

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Section: Introductionmentioning

confidence: 97%

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

Skedros

Knight

et al. 2018

Journal of Anatomy

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“…; Keenan et al. ). If, however, there is some unrecognized reason that there is in fact inhomogeneity in the distribution of sealed + partially sealed osteons, then rigorous proof of our assumption that there is no bias can only be obtained in future studies that employ multiple serial sections.…”

Section: Discussionmentioning

confidence: 97%

“…the material is completely homogeneous) and (ii) the plane of the section must be random. In this context our data dealing with the prevalence and size of sealed + partially sealed osteons should be representative and unbiased by our sampling methods (single planar sections and analysis within them in anatomical quadrants) because sealed + partially sealed osteons would be expected to be homogeneously distributed in the bone regions that we analyzed, as also indicated by data of various other secondary osteon variants in many different bones and species (Skedros et al 2007;Keenan et al 2017). If, however, there is some unrecognized reason that there is in fact inhomogeneity in the distribution of sealed + partially sealed osteons, then rigorous proof of our assumption that there is no bias can only be obtained in future studies that employ multiple serial sections.…”

Section: Limitationsmentioning

confidence: 94%

Sealed osteons in animals and humans: low prevalence and lack of relationship with age

et al. 2018

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Sealed osteons are unusual variants of secondary osteons that have received little attention, especially in non-human bones. Sealed osteons are characterized by central canals that are plugged with bone tissue. As with other variants of secondary osteons (e.g. drifting, dumbbell, multi-canal), understanding how and why sealed osteons form can shed light on the mechanisms that regulate normal bone remodeling and how this process can be perturbed with aging and some diseases. In a recent microscopic evaluation of human tibiae obtained after traumatic amputations, 4-5% of the osteons were sealed. It is suggested that this high prevalence reflects occasional localized microscopic ischemia from normal osteonal remodeling; hence sealed osteons are implicated in human skeletal fragility. Therefore, osteon prevalence would be expected to correlate with the bone remodeling seen with aging; for example, showing positive relationships between sealed osteons and the population density of typical secondary osteons (OPD). We evaluated the prevalence of partially sealed (80-99% sealed) and fully sealed osteons with respect to age and variations in OPD in 10 adult human femora (34-71 years) and in various non-human appendicular bones of mature animals that were not of advanced age, including deer calcanei, equine radii and equine third metacarpals. An additional sample of 10 bilateral human femora with unilateral non-cemented total hip replacements (F,+HR) and non-implanted contralateral femora (F,-HR) were evaluated (10 patients; 52-94 years). In non-human bones, sealed + partially sealed osteons were rare (~0.1%) even when having relatively high OPD. When considering sealed + partially sealed osteons in femora from patients without any HR, results showed that 1.6% of the osteons were sealed or partially sealed, which was much lower than anticipated, but this is 10- to 20-fold more than in any of the non-human bones. Additionally, in all bones, sealed + partially sealed osteons were significantly smaller than typical secondary osteons (mean diameters: 125 vs. 272 μm; P < 0.005). In the patients with HR, the percentage of sealed + partially sealed osteons: (i) did not correlate with age, (ii) showed no significant difference between F,-HR and F,+HR (1.9 vs. 2.1%; P = 0.2), and (iii) was positively correlated with OPD (r = 0.67, P = 0.001), which differs from the very weak or lack of correlations in the non-human bones and the other human femur sample. The lack of an age-related relationship, in addition to the very low prevalence of sealed + partially sealed osteons are inconsistent with the idea that they contribute to reduced bone quality seen in aging humans. The small size of sealed and partially sealed osteons, regardless of species affiliation, suggests that they represent closing cones at the termini of some osteons. Available evidence suggests that osteons of primates might have a greater capacity for branching that is associated with closing cones, which might explain the 10-20 times higher prevalence of sealed + partia...

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“…This is because the only foot bones of nonhuman primates in which cross‐sectional geometry has been studied are metatarsals, wherein predictable relationships between strength properties and locomotion have been found in apes and monkeys (e.g., Marchi, , ; Patel et al, ; Patel, Organ, Jashashvili, Bui, & Dunsworth, ). Although the calcaneus is frequently modeled as a beam in ungulates (e.g., Keenan, Mears, & Skedros, ; Skedros, Su, Knight, Bloebaum, & Bachus, ; Su, Skedros, Bachus, & Bloebaum, ), this method has yet to be applied to the distally elongated calcaneus of galagids, which resembles a long bone in both external morphology and in cross section (Hall‐Craggs, ).…”

Section: Introductionmentioning

confidence: 99%

Calcaneal elongation and bone strength in leaping galagids

Lewton

Patel

2019

American J Phys Anthropol

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Objectives: Small-bodied vertical clinging and leaping primates have elongated calcanei which enhance leap performance by optimizing leap velocity, distance, and acceleration, but at the expense of experiencing relatively large forces during takeoff and landing. This study tests the hypothesis that the elongated calcaneus of leaping galagids is adapted to resist larger and more stereotyped bending loads compared to more quadrupedal galagids. Materials and Methods: The calcanei of 14 individuals of Otolemur and 14 individualsof Galago (three species of each genus) were μCT scanned. Calcaneal cross-sectional properties (maximum and minimum second moments of area and polar section modulus) were obtained from a slice representing the 50% position of bone segment length and dimensionless ratios were created for each variable using calcaneal cuboid facet area as a proxy for body mass.Results: There were no significant differences in size-adjusted bending strength between Galago and Otolemur. Galago exhibited more elliptically shaped calcaneal cross sections, however, suggesting that its calcanei are more adapted to stereotyped loading regimes than those of Otolemur. Discussion:The results suggest that the calcaneus of specialized leapers is adapted to more stereotyped loading patterns. The lack of predicted bone strength differences between Galago and Otolemur may be related to body size differences between these taxa, or it may indicate that loads encountered by Galago during naturalistic leaping are not reflected in the available experimental force data.

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Utility of osteon circularity for determining species and interpreting load history in primates and nonprimates

Abstract: Frequent misclassifications in nonhuman comparisons might reflect influences of habitual load complexity and/or strain-mode distributions, or other factors not accounted for by these two considerations.

Cited by 33 publications

References 128 publications

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

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

Sealed osteons in animals and humans: low prevalence and lack of relationship with age

Calcaneal elongation and bone strength in leaping galagids

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