Histovariability in human clavicular cortical bone microstructure and its mechanical implications

Abstract

The human clavicle (i.e. collarbone) is an unusual long bone due to its signature S‐shaped curve and variability in macrostructure observed between individuals. Because of the complex nature of how the upper limb moves, as well as due to its complex musculoskeletal arrangement, the biomechanics, in particular the mechanical loadings, of the clavicle are not fully understood. Given that bone remodeling can be influenced by bone stress, the histologic organization of Haversian bone offers a hypothesis of responses to force distributions experienced across a bone. Furthermore, circularly polarized light microscopy can be used to determine the orientation of collagen fibers, providing additional information on how bone matrix might organize to adapt to direction of external loads. We examined Haversian density and collagen fiber orientation, along with cross‐sectional geometry, to test whether the clavicle midshaft shows unique adaptation to atypical load‐bearing when compared with the sternal (medial) and acromial (lateral) shaft regions. Because fractures are most common at the midshaft, we predicted that the cortical bone structure would show both disparities in Haversian remodeling and nonrandomly oriented collagen fibers in the midshaft compared with the sternal and acromial regions. Human clavicles (n = 16) were sampled via thin‐sections at the sternal, middle, and acromial ends of the shaft, and paired sample t‐tests were employed to evaluate within‐individual differences in microstructural or geometric properties. We found that Haversian remodeling is slightly but significantly reduced in the middle of the bone. Analysis of collagen fiber orientation indicated nonrandom fiber orientations that are overbuilt for tensile loads or torsion but are poorly optimized for compressive loads throughout the clavicle. Geometric properties of percent bone area, polar second moment of area, and shape (Imax/Imin) confirmed the conclusions drawn by existing research on clavicle macrostructure. Our results highlight that mediolateral shape changes might be accompanied by slight changes in Haversian density, but bone matrix organization is predominantly adapted to resisting tensile strains or torsion throughout and may be a major factor in the risk of fracture when experiencing atypical compression.

Similarities and Differences in Bone Mineral Density between Multiple Sites in the Same Individual: An Elderly Cadaveric Study

“…Imamura et al investigated morphological changes in the cortical bone of the femoral diaphysis with age and reported that there was no change in cortical bone thickness in men, but in women, cortical bone thickness was found to decrease with age [ 11 ]. The clavicle has a high proportion of cortical bones [ 43 ]; thus, our finding of a significant negative correlation between the BMD of the clavicle and femoral diaphysis and age in women may suggest that thinning and porosity associated with cortical bone resorption may occur in elderly women.…”

Sex differences in workload in medieval Poland: Patterns of asymmetry and biomechanical adaptation in the upper limb at Giecz

“…See Table S1 for abbreviations. systemic variance, genetic diversity, or some combination of all of these (Agosto & Auerbach, 2022;Crane et al, 2019;Daruwalla et al, 2010;Lambert et al, 2016).…”

“…These clavicle‐specific exceptions highlight that biomechanical factors influencing clavicle morphology should be investigated further. Numerous studies have identified high levels of variation in both morphology and microstructure of the clavicle, but it is still unclear if these can be attributed to elevated developmental plasticity reflecting the absence of constraint, environmental or systemic variance, genetic diversity, or some combination of all of these (Agosto & Auerbach, 2022; Crane et al, 2019; Daruwalla et al, 2010; Lambert et al, 2016).…”

Cortical parameters predict bone strength at the tibial diaphysis, but are underestimated by HR‐pQCT and μCT compared to histomorphometry

“…The trabecularization of the cortex was a prominent feature observed in osteoporotic bone when compared to normal bone. A more detailed histological assessment of the periosteal, central and the endosteal regions further enabled identification of osteons at rest and those actively remodelling (Crane et al, 2019; Imamura et al, 2019). In our study, the definition of the two groups of osteons, those at rest and those actively remodelling, was based on arbitrarily defined intervals for the inner osteon diameter (Figure 4).…”