Proximate mechanisms involved in the formation of Secondary Osteon Morphotypes

Skedros, John G.; Doutré, M. S.; Weaver, Daniel

doi:10.1055/s-0037-1619002

Cited by 8 publications

(3 citation statements)

References 75 publications

(90 reference statements)

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“…By considering single osteon cross-sections, our study is unable to represent three-dimensional irregularities of osteonal structures, such as spiralling osteon boundaries observed along their longitudinal axis [53, 56], and spiralling lamellae formation [59], which could be due to lateral motions of osteoblasts during bone formation [36]. Furthermore, our study did not take consideration of lamellar matrix formation motifs [63, 64]. Different lamellar organisations, such as orthogonal plywood, irregular plywood, and twisted plywood models, could reflect changes in bone formation that may induce wall thickness asymmetries.…”

Section: Discussionmentioning

confidence: 99%

How osteons form: A quantitative hypothesis-testing analysis of cortical pore filling and wall asymmetry

Hegarty-Cremer,

Borggaard,

Andreasen

et al. 2023

Preprint

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Osteon morphology provides valuable information about the interplay between different processes involved in bone remodelling. The correct quantitative interpretation of these morphological features is challenging due to the complexity of interactions between osteoblast behaviour, and the evolving geometry of cortical pores during pore closing. We present a combined experimental and mathematical modelling study to provide insights into bone formation mechanisms during cortical bone remodelling based on histological cross-sections of quiescent human osteons and hypothesis-testing analyses. We introduce wall thickness asymmetry as a measure of the local asymmetry of bone formation within an osteon and examine the frequency distribution of wall thickness asymmetry in cortical osteons from human bone samples from individuals 16--78 years old. Our measurements show that most osteons possess some degree of asymmetry, and that the average degree of osteon asymmetry in cortical bone evolves with age. We then propose a comprehensive mathematical model of cortical pore filling that includes osteoblast secretory activity, osteoblast elimination, osteoblast embedment as osteocytes, and osteoblast crowding and redistribution along the bone surface. The mathematical model is first calibrated to symmetric osteon data, and then used to test three mechanisms of asymmetric wall formation against osteon data: (i) delays in the onset of infilling around the cement line; (ii) heterogeneous osteoblastogenesis around the bone perimeter; and (iii) heterogeneous osteoblast secretory rate around the bone perimeter. Our results suggest that wall thickness asymmetry due to off-centred Haversian pores within osteons, and that nonuniform lamellar thicknesses within osteons are important morphological features that can indicate the prevalence of specific asymmetry-generating mechanisms. This has significant implications for the study of disruptions of bone formation.

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Section: Discussionmentioning

confidence: 99%

How osteons form: A quantitative hypothesis-testing analysis of cortical pore filling and wall asymmetry

Hegarty-Cremer,

Borggaard,

Andreasen

et al. 2023

Preprint

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“…[ 17 ] Though these proposals are very different one from another, they share the premise that the fibrillar layout in MB is created by or through forces generated by the formative osteoblast cells. Importantly, whereas observations from the literature might explain 2D lateral fibrillar packing, [ 18 ] none of the existing theories provides experimental evidence for the appearance of the long‐range and 3D twisted fibril arrangements, [ 19 , 20 , 21 , 22 , 23 ] with a geometry often compared to cholesteric (helicoidal) liquid crystals (LC). [ 24 ] An alternative yet complementary possibility is that a LC state of matter is created in bone.…”

Section: Introductionmentioning

confidence: 99%

“…[ 24 ] An alternative yet complementary possibility is that a LC state of matter is created in bone. [ 16 , 19 , 25 ]…”

Section: Introductionmentioning

confidence: 99%

Acidic Osteoid Templates the Plywood Structure of Bone Tissue

Robin,

Djediat,

Bardouil

et al. 2023

Advanced Science

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Bone is created by osteoblasts that secrete osteoid after which an ordered texture emerges, followed by mineralization. Plywood geometries are a hallmark of many trabecular and cortical bones, yet the origin of this texturing in vivo has never been shown. Nevertheless, extensive in vitro work revealed how plywood textures of fibrils can emerge from acidic molecular cholesteric collagen mesophases. This study demonstrates in sheep, which is the preferred model for skeletal orthopaedic research, that the deeper non‐fibrillar osteoid is organized in a liquid‐crystal cholesteric geometry. This basophilic domain, rich in acidic glycosaminoglycans, exhibits low pH which presumably fosters mesoscale collagen molecule ordering in vivo. The results suggest that the collagen fibril motif of twisted plywood matures slowly through self‐assembly thermodynamically driven processes as proposed by the Bouligand theory of biological analogues of liquid crystals. Understanding the steps of collagen patterning in osteoid‐maturation processes may shed new light on bone pathologies that emerge from collagen physico‐chemical maturation imbalances.

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Mechanobiology of human pisiform formation as a model for endochondral ossification

Bhramdat

Daegling

2023

The Anatomical Record

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The role of mechanical stimuli in promoting endochondral ossification during somatic growth and maturation remains an active area of research. This study employs a pisiform model of endochondral ossification to investigate the potential role of mechanobiological signals in the appearance and development of ossification centers and to develop theoretical applications to the primate basicranium. We constructed finite element models based on the structure of a human pisiform within the flexor carpi ulnaris tendon. The pisiform was assigned initial material properties of hyaline cartilage, and tendon properties were based on in situ observations drawn from the literature. A macaque growth model was used to simulate increased load over time as a function of body mass. A load case of uniaxial tension from the tendon was applied over 208 iterations, to simulate weekly growth over a 4‐year span. The mechanical signal was defined as shear stress. Element stresses were evaluated in each iteration, with elements exceeding the yield threshold subsequently assigned a higher elastic modulus to mimic mechanically driven mineralization. Three unique mineralization rates were tested. Regardless of rate, all ossification simulations predict a pisiform with heterogeneous stiffness through alternating periods of material stasis and active mineralization/ossification. Assuming metabolic processes underlying endochondral ossification are similar throughout the body, our model suggests that a mechanical signal alone is an insufficient stimulus in the etiology of bone formation through endochondral ossification. Consequently, given the general validity of the simulation, endochondral ossification cannot be fully explained in terms of mechanical stimuli.

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Proximate mechanisms involved in the formation of Secondary Osteon Morphotypes

Cited by 8 publications

References 75 publications

How osteons form: A quantitative hypothesis-testing analysis of cortical pore filling and wall asymmetry

How osteons form: A quantitative hypothesis-testing analysis of cortical pore filling and wall asymmetry

Acidic Osteoid Templates the Plywood Structure of Bone Tissue

Mechanobiology of human pisiform formation as a model for endochondral ossification

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