Secondary osteon size and collagen/lamellar organization (“osteon morphotypes”) are not coupled, but potentially adapt independently for local strain mode or magnitude

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Abstract

In bone, matrix slippage that occurs at cement lines of secondary osteons during loading is an important toughening mechanism. Toughness can also be enhanced by modifications in osteon cross-sectional size (diameter) for specific load environments; for example, smaller osteons in more highly strained “compression” regions vs. larger osteons in less strained “tension” regions. Additional osteon characteristics that enhance toughness are distinctive variations in collagen/lamellar organization (i.e., “osteon morphotypes”). Interactions might exist between osteon diameter and morphotype that represent adaptations for resisting deleterious shear stresses that occur at the cement line. This may be why osteons often have a peripheral ring (or “hoop”) of highly oblique/transverse collagen. We hypothesized that well developed/distinct “hoops” are compensatory adaptations in cases where increased osteon diameter is mechanically advantageous (e.g., larger osteons in “tension” regions would have well developed/distinct “hoops” in order to resist deleterious consequences of co-existing localized shear stresses). We tested this hypothesis by determining if there are correlations between osteon diameters and strongly hooped morphotypes in “tension”, “compression”, and “neutral axis” regions of femora (chimpanzees, humans), radii (horse, sheep) and calcanei (horse, deer). The results reject the hypothesis—larger osteons are not associated with well developed/distinct “hoops”, even in “tension regions” where the effect was expected to be obvious. Although osteon diameter and morphotype are not coupled, osteon diameters seem to be associated with increased strain magnitudes in some cases, but this is inconsistent. By contrast, osteon morphotypes are more strongly correlated with the distribution of tension and compression.

Introduction

One beneficial result of remodeling of compact (cortical) bone with secondary osteons (Haversian systems) in non-elderly individuals is that tissue mechanical properties, especially fatigue resistance and toughness,1 can be improved by the introduction of osteonal interfaces, including cement lines and interlamellar seams (Launey et al., 2010a, Nalla et al., 2005a, Nalla et al., 2005b, Skedros et al., 2005). In this context, the mechanical benefits of increased concentrations of secondary osteons have been compared to the fibers in a fiber-reinforced ceramic matrix composite material (Doblaré et al., 2004, Hogan, 1992, Martin et al., 1998, Mohsin et al., 2006, Najafi et al., 2009, Yeni et al., 1997). An important observation is the finding that the population densities of osteons with specific patterns of lamellar and collagen organization are increased in loading environments that are characterized by local prevalence/predominance of a specific strain mode (tension, compression, or shear) (Riggs et al., 1993a, Skedros, 2012, Skedros et al., 2009, Skedros et al., 2011a). Hence, in addition to the potential for modifying the presence and complexity of their interfaces (Crescimanno and Stout, 2012, Keenan et al., 2010, Robling and Stout, 1999, Skedros et al., 2007a), matrix organization of osteons can be modified in ways that are mechanically adaptive. These specific osteon “types” have been described as “osteon morphotypes”; this characterization is largely based on the completeness and intensity of birefringent rings (or “hoops”) that often occur at their periphery, as seen in circularly polarized light (CPL) images of thin transverse sections (Fig. 1) (Skedros et al., 2011b). The increased birefringence appears as brighter (whiter) gray levels in grayscale CPL images, and this correlates with increased oblique-to-transverse collagen fiber orientation (CFO) (in CPL longitudinal CFO appears dark; compare scores 0 and 5 in Fig. 1) (Boyde and Riggs, 1990, Bromage et al., 2003, Skedros et al., 2009).

When compared to osteons in “compression regions” of bones habitually loaded in bending, “tension regions” have osteon morphotypes with more longitudinal collagen in the majority of their wall and with some degree of peripheral “hoopedness” (i.e., completeness and brightness intensity of a peripheral “hoop” in CPL images; scores 1–4 in Fig. 1). A composite osteon morphotype score (MTS) has been described that strongly correlates with the average CFO of an entire microscopic image (Skedros et al., 2011a, Skedros et al., 2011b), which in turn correlates with the toughness of the bone (Riggs et al., 1993b, Skedros et al., 2006). Consequently, osteon MTSs can be used as an index for identifying microstructural adaptations and may act to enhance toughness for regional variations in habitual strain mode.

In cortical bone, regional strain-mode-specific toughness can also be enhanced by modifications in osteon cross-sectional size. This is indirectly supported by data showing that in some bones smaller osteons occur in regions that receive a history of prevalent/predominant compression (usually higher strains) compared to regions that receive prevalent/predominant tension (usually lower strains)2 (Hiller et al., 2003, Skedros, 2012, van Oers et al., 2008). Potentially adaptable relationships might exist between osteon size and morphotype because physiological loading is not simple, but it produces shear stresses that are potentially more deleterious than tension and compression stresses. In turn, shear stresses can be increased in the vicinity of the cement line when differential motion of the osteons occurs as the yield point is approached (Bigley et al., 2006, Ebacher et al., 2007, Leng et al., 2009, Pope and Murphy, 1974, Zimmermann et al., 2011). It has been speculated that this may help explain why osteons, especially in tension-loaded regions, often have a peripheral ring (or “hoop”) of highly oblique/transverse collagen (Martin et al., 1996, Skedros et al., 2011b). In other words, this modification might help to resist deleterious consequences of these localized shear stresses, including excessive microdamage formation and propagation (Bigley et al., 2006, Mohsin et al., 2006, O’Brien et al., 2005, Skedros et al., 2005, Skedros et al., 2009).

Osteonal debonding, bridging, and pullout have been identified as some of the extrinsic mechanisms that toughen cortical bone by controlling crack propagation and lowering the effective (local) stress intensity actually experienced at the crack tip (Bigley et al., 2006, Currey, 2002, Hiller et al., 2003, Launey et al., 2010a, Zimmermann et al., 2009) (Fig.2, Fig.3). In this perspective, van Oers et al. (2008) offer a mechanically based explanation for why a functional relationship might exist between an osteon’s morphotype and diameter:

Osteon diameter affects the ratio between shear stress in the cement line and tensile stress on the osteon. Given a tensile force F on an osteon with diameter d and pullout length L, the tensile stress σ on the osteon and the shear stress τ in the cement line are given by: σ = F/(π/4·d·d) [or σ = F/(π/(4d2))] and τ = F/(π·d·L). The ratio between σ and τ thus is τ/σ = d/4L. [Pull-out occurs when σ > τ.] Theoretically, pullout is thus more likely when osteons are larger in diameter, because this increases the shear stress in the cement line boundary relative to the tensile stress on the osteon (page 481).

Consequently, in the “tension region” of a bone loaded in habitual bending there is an important tradeoff between potentially deleterious shear stresses at the cement line and the beneficial effects of increased osteon size. We hypothesized that this tradeoff would be recognized as increased “hoopedness” that would occur as an adaptation that resists deleterious shear stresses in cases where increased osteon diameter is mechanically advantageous—larger osteons in “tension” regions would be expected to have fully developed “hoops”. The importance of this hypothesis is that, if supported, it suggests a coordination of different collagenous-matrix assembly activities between peripheral and subsequent deeper osteoblasts during osteon formation that are ultimately mechanically important. While this hypothesis has been considered by some investigators (Kerschnitzki et al., 2011, Marotti, 1996, Parfitt, 1983, Pazzaglia et al., 2011), it has not been tested in large samples of osteons from habitual bending environments and various species. We tested this hypothesis of size/hoop synergism by determining if there are significant correlations between osteon diameters and “hooped” morphotypes in “tension regions” vs. “compression regions” vs. “neutral axis regions” in a variety of limb bones.

Section snippets

Methods

The specimens and tissue preparation methods used in this study have been described in detail in previous studies (Skedros et al., 2009, Skedros et al., 2011b). Briefly, circular polarized light (CPL) microscopic images were obtained at 50× from thin (100 μm) transverse sections from the following samples of adult primate and non-primate bones: (1) deer and equine calcanei, and sheep and equine radii (n = 7 of each bone type) (Skedros et al., 2009); (2) adult chimpanzee femora (n = 8; mean age 25 

Results

Results of the three-way ANCOVA showed significant effects of MTS and species (Table 1). There were statistically significant differences between most species comparisons (p < 0.05). Post-hoc analysis showed that osteon diameter tended to be greater in the hooped morphotypes 3 and 4 when compared to the hooped morphotypes 1 and 2. However, when considering all of the hooped osteons (MTSs 1–4) the results of paired comparisons based on small vs. large osteons showed that the hypothesized

Discussion

The capacity of bones to undergo osteonal remodeling that results in regional differences in microstructural organization, which in turn produces corresponding differences in toughness of cortical bone, is an expected and common occurrence because the shafts of many limb bones are stereotypically loaded in bending during controlled ambulation (Skedros, 2012). In other words, these bones are loaded in such a way that one cortex is almost always loaded in compression while another cortex is

Acknowledgments

The authors thank Erick Anderson, Kyle Gubler, Jaxon Hoopes, Scott Sorenson, Adam Beckstrom, Anna Adondakis, and Chase Jardine for their assistance in completing this study. We are indebted to Pat Campbell and Harlan Amstutz for the use of their laboratory facilities at the Joint Replacement Institute of Orthopaedic Hospital in Los Angeles, California. This research is supported by USA Department of Veterans Affairs medical research funds, and the Doctor’s Education Research Fund (DERF) of

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