Interconnectivity Explains High Canalicular Network Robustness between Neighboring Osteocyte Lacunae in Human Bone

Bortel, Emely; Grover, Liam M.; Eisenstein, Neil; Seim, Christian; Suhonen, Heikki; Pacureanu, Alexandra; Westenberger, Peter; Raum, Kay; Langer, Max; Peyrin, Françoise; Addison, Owen; Hesse, Bernhard

doi:10.1002/anbr.202100090

Cited by 12 publications

(19 citation statements)

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“…To date, however, virtually all simulations of permeability of human bone porosities have been limited to vascular and LCN pores. (22,44,58,59) The discovery of a subcanalicular network in bone reported in the present study is an additional factor in this context. It should be noted that nanoscale porosity that gives rise to bone poroelasticity and interstitial fluid permeability has been noted in the published literature.…”

Section: Discussionsupporting

confidence: 52%

“…The LCN volume and surface area have implications for bone mineralization as they provide extracellular matrix access to ions and small molecules. (20) 3D imaging of the bone LCN using synchrotron radiation phase-contrast nano-CT (21,22) and confocal microscopy (23) has revealed that 50% of the mineralized tissue in the human skeleton is located within $1.5 μm of the closest LCN boundary and 80% within 2 to 3 μm. Further, a recent FIB-SEM examination of forming human bone suggests co-diffusion of mineralization precursors, promotors, and inhibitors from the LCN to the bone matrix, (24) an observation highlighting the role of the LCN in supporting and achieving mineral homeostasis.…”

Section: Introductionmentioning

confidence: 99%

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Subcanalicular Nanochannel Volume Is Inversely Correlated With Calcium Content in Human Cortical Bone

Tang

Landis

Blouin

et al. 2020

Journal of Bone and Mineral Research

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The spatial distribution of mineralization density is an important signature of bone growth and remodeling processes, and its alterations are often related to disease. The extracellular matrix of some vertebrate mineralized tissues is known to be perfused by a lacunocanalicular network (LCN), a fluid‐filled unmineralized structure that harbors osteocytes and their fine processes and transports extracellular fluid and its constituents. The current report provides evidence for structural and compositional heterogeneity at an even smaller, subcanalicular scale. The work reveals an extensive unmineralized three‐dimensional (3D) network of nanochannels (~30 nm in diameter) penetrating the mineralized extracellular matrix of human femoral cortical bone and encompassing a greater volume fraction and surface area than these same parameters of the canaliculi comprising the LCN. The present study combines high‐resolution focused ion beam‐scanning electron microscopy (FIB‐SEM) to investigate bone ultrastructure in 3D with quantitative backscattered electron imaging (qBEI) to estimate local bone mineral content. The presence of nanochannels has been found to impact qBEI measurements fundamentally, such that volume percentage (vol%) of nanochannels correlates inversely with weight percentage (wt%) of calcium. This mathematical relationship between nanochannel vol% and calcium wt% suggests that the nanochannels could potentially provide space for ion and small molecule transport throughout the bone matrix. Collectively, these data propose a reinterpretation of qBEI measurements, accounting for nanochannel presence in human bone tissue in addition to collagen and mineral. Further, the results yield insight into bone mineralization processes at the nanometer scale and present the possibility for a potential role of the nanochannel system in permitting ion and small molecule diffusion throughout the extracellular matrix. Such a possible function could thereby lead to the sequestration or occlusion of the ions and small molecules within the extracellular matrix. © 2022 The Authors. Journal of Bone and Mineral Research published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research (ASBMR).

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Section: Discussionsupporting

confidence: 52%

Section: Introductionmentioning

confidence: 99%

Subcanalicular Nanochannel Volume Is Inversely Correlated With Calcium Content in Human Cortical Bone

Tang

Landis

Blouin

et al. 2020

Journal of Bone and Mineral Research

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“…Contrarily, if all angles were randomly distributed, there would be no peak in the histogram, and thus the variance would be the smallest. Since the angles are interrelated, we define the product of the variances as a descriptor for the alignment, called the level of alignment (LOA) (Bortel et al, 2022).…”

Section: Arrangement Of the Intracortical Pore Systemmentioning

confidence: 99%

“…Through Darcy's law, the fluid and flow were computed. To numerically estimate the absolute permeability, the Stokes equations are applied (Bortel et al, 2022).…”

Section: Fluid Simulationmentioning

confidence: 99%

Comparison of the 3D-Microstructure Between Alveolar and Iliac Bone for Enhanced Bioinspired Bone Graft Substitutes

Rothweiler

Groß

Bortel³

et al. 2022

Front. Bioeng. Biotechnol.

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In oral- and maxillofacial bone augmentation surgery, non-vascularized grafts from the iliac crest demonstrate better clinical performance than alveolar bone grafts. The underlying mechanisms are not fully understood but are essential for the enhancement of bone regeneration scaffolds. Synchrotron Radiation µ-CT at a pixel size of 2.3 μm was used to characterize the gross morphology and the vascular and osteocyte lacuna porosity of patient-matched iliac crest/alveolar bone samples. The results suggest a difference in the spatial distribution of the vascular pore system. Fluid simulations reveal the permeability tensor to be more homogeneous in the iliac crest, indicating a more unidirectional fluid flow in alveolar bone. The average distance between bone mineral and the closest vessel pore boundary was found to be higher in alveolar bone. At the same time, osteocyte lacunae density is higher in alveolar bone, potentially compensating for the longer average distance between the bone mineral and vessel pores. The present study comprehensively quantified and compared the 3D microarchitecture of intraindividual human alveolar and iliac bone. The identified difference in pore network architecture may allow a bone graft from the iliac crest to exhibit higher regeneration potential due to an increased capacity to connect with the surrounding pore network of the residual bone. The results may contribute to understanding the difference in clinical performance when used as bone grafts and are essential for optimization of future scaffold materials.

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“…Although the LCN contributes less to overall bone porosity compared with blood vessel pores (Haversian and Volkmann canals), the surface area formed by the LCN is more than one order of magnitude larger than the surface formed by blood vessel pores (Hesse et al, 2015). Mineral exchange is likely to occur at all bone interfaces including blood vessel pores and at the LCN (Ayoubi et al, 2020;Bortel et al, 2021;Vahidi et al, 2021). The role of the osteocyte network, housed inside the LCN, is not only to contribute to mineral homeostasis through exchange of ions at their mineral interfaces but also in mechano-transduction and subsequent triggering of osteoblast/osteoclast remodeling (Cao et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Evaluation of imaging setups for quantitative phase contrast nanoCT of mineralized biomaterials

Suuronen¹,

Hesse²,

Langer³

et al. 2022

J Synchrotron Rad

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X-ray nano-tomography with phase contrast (nanoCT) using synchrotron radiation is a powerful tool to non-destructively investigate 3D material properties at the nanoscale. In large bone lesions, such as severe bone fractures, bone cancer or other diseases, bone grafts substituting the lost bone might be necessary. Such grafts can be of biological origin or be composed of a synthetic bone substitute. The long-term functioning of artificial bone substitutes depends on many factors. Synchrotron nanoCT imaging has great potential to contribute to further the understanding of integration of implants into bone tissue by imaging the spatial interaction between bone tissue and implant, and by accessing the interface between implant material and bone tissue. With this aim, a methodology for evaluating the image quality is presented for in-line phase contrast nanoCT images of bone scaffold samples. A PMMA-embedded tricalcium phosphate scaffold was used with both a closed and an open porosity structure and bone ingrowths as a representative system of three known materials. Parameters such as spatial resolution and signal-to-noise ratio were extracted and used to explore and quantitatively compare the effects of implementation choices in the imaging setup, such as camera technology and imaging energy, on the resulting image quality. Increasing the X-ray energy from 17.5 keV to 29.6 keV leads to a notable improvement in image quality regardless of the camera technology used, with the two tested camera setups performing at a comparable level when the recorded intensity was kept constant.

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Interconnectivity Explains High Canalicular Network Robustness between Neighboring Osteocyte Lacunae in Human Bone

Cited by 12 publications

References 50 publications

Subcanalicular Nanochannel Volume Is Inversely Correlated With Calcium Content in Human Cortical Bone

Subcanalicular Nanochannel Volume Is Inversely Correlated With Calcium Content in Human Cortical Bone

Comparison of the 3D-Microstructure Between Alveolar and Iliac Bone for Enhanced Bioinspired Bone Graft Substitutes

Evaluation of imaging setups for quantitative phase contrast nanoCT of mineralized biomaterials

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