Three‐dimensional reconstruction of Haversian systems in human cortical bone using synchrotron radiation‐based micro‐<scp>CT</scp>: morphology and quantification of branching and transverse connections across age

Maggiano, Isabel S.; Maggiano, Corey; Clement, John G.; Thomas, C. David L.; Carter, Yasmin; Cooper, David M.L.

doi:10.1111/joa.12430

Cited by 80 publications

(103 citation statements)

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“…; Maggiano et al. ) and this level of resolution could add new information if used in future studies. Previous research has shown that in vivo micro‐CT can be used to image cortical canals in live rats (Harrison & Cooper, ; Pratt et al.…”

Section: Discussionmentioning

confidence: 97%

The effect of growth rate on the three‐dimensional orientation of vascular canals in the cortical bone of broiler chickens

Pratt

Cooper

2018

Journal of Anatomy

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Vascular canals in cortical bone during growth and development typically show an anisotropic pattern with canals falling into three main categories: circumferential, radial, and longitudinal. Two major hypotheses attempt to explain the preferred orientations in bone: that vascular canal orientation is optimized to resist a predominant strain direction from functional loading, or that it reflects growth requirements and velocity. We use a controlled growth experiment in broiler chickens to investigate the effect of growth rate on vascular canal orientation. Using feed restriction we set up a fast growing control group and a slow growing restricted group. We compared the microstructure in the humerus and the femur at 42 days of age using synchrotron micro‐computed tomography (micro‐CT), a three‐dimensional (3D) method that visualizes the full canal network. We measured the 3D orientation of each canal in the whole cross‐section of the bone cortex using a set of custom imagej scripts. Using these orientations we compute laminar, radial, and longitudinal indices that measure the proportion of circumferential, radial, and longitudinal canals, by unit of length, in the cortex. Following previous studies we hypothesized that vascular canal orientation is related to growth, with radial canals linked to a faster growth rate and related to functional loading through a high laminar index in flight bones which reflects torsional loading resulting from active flight. The control group had final body weights that were nearly twice the final weights of the restricted group and higher absolute growth rates. We found consistent patterns in the comparison between the humerus and the femur in both groups, with the humerus having higher laminar and longitudinal indices, and a lower radial index than the femur. The control group had higher radial indices and lower laminar and longitudinal indices in both the humerus and the femur than the restricted group. The higher radial indices in our control group point to a link between radial canals and faster growth, and between laminar canals and slower growth, while the higher laminar indices in the humerus point to a link between circumferential canals and torsional loading. Overall, our results indicate that the orientation of the cortical canal network in a bone is the consequence of a complex interaction between the growth rate of that bone and functional loading environment.

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Section: Discussionmentioning

confidence: 97%

The effect of growth rate on the three‐dimensional orientation of vascular canals in the cortical bone of broiler chickens

Pratt

Cooper

2018

Journal of Anatomy

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“…In that study, Lanyon and Bourn (1979) (Cohen and Harris, 1958;Maggiano et al, 2016) will be needed because the current capacity of high-resolution 3D computed tomography is not sufficiently accurate (Hennig et al, 2015). In that study, Lanyon and Bourn (1979) (Cohen and Harris, 1958;Maggiano et al, 2016) will be needed because the current capacity of high-resolution 3D computed tomography is not sufficiently accurate (Hennig et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

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

Keenan¹,

Mears²,

Skedros

2017

American J Phys Anthropol

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“…; Maggiano et al. ) and therefore are not a pathological or otherwise ischemia‐related infilling of the Haversian canal with bone tissue. Recent 3D studies suggest the possibility that sealed osteons represent the closing cones of normal secondary osteons.…”

Section: Discussionmentioning

confidence: 98%

“…3). Within the past 10 years, several studies have described sealed osteons in secondary bone (Pazzaglia et al 2010(Pazzaglia et al , 2013(Pazzaglia et al , 2015Congiu & Pazzaglia, 2011;Maggiano et al 2016), yet none has conclusively demonstrated their origin.…”

Section: Introductionmentioning

confidence: 99%

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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Three‐dimensional reconstruction of Haversian systems in human cortical bone using synchrotron radiation‐based micro‐CT: morphology and quantification of branching and transverse connections across age

Cited by 80 publications

References 58 publications

The effect of growth rate on the three‐dimensional orientation of vascular canals in the cortical bone of broiler chickens

The effect of growth rate on the three‐dimensional orientation of vascular canals in the cortical bone of broiler chickens

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

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

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