Investigation of the three-dimensional orientation of mineralized collagen fibrils in human lamellar bone using synchrotron X-ray phase nano-tomography

Варга, П.; Pacureanu, Alexandra; Langer, Max; Suhonen, Heikki; Hesse, Bernhard; Grimal, Quentin; Cloetens, Peter; Raum, Kay; Peyrin, Françoise

doi:10.1016/j.actbio.2013.05.015

Cited by 101 publications

(92 citation statements)

References 52 publications

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“…Imaging bone at this scale provides useful information on other structural features, such as the collagen -mineral interface [21], mineral platelet sizes and shapes [13,14] or collagen D-period [7,263] for very high-resolution techniques such as TEM and AFM, and offers data revealing structural details of the lacuno-canalicular network [245] and bone remodelling sites [270] for high-resolution techniques such as SEM. X-ray phase-contrast techniques such as ptychographic CT [225] or X-ray phase nanotomography [226] operate at similar scales to volume SEM, and in addition offer the important advantage of tomographic (i.e. non-destructive) assessment.…”

Section: Assessment At Different Hierarchical Levels and Additional Imentioning

confidence: 99%

“…Regarding imaging techniques, volume electron microscopy techniques, such as FIB SEM [208] or SBF SEM [206], provide information by serially removing thin sections and imaging the underlying surface, to reconstruct volumes of tens of micrometres in size. Finally, through phase-contrast techniques, such as ptychographic CT [225] and phase-contrast nanotomography [226], bone tissue samples at overall dimensions of tens of micrometres can be imaged in a tomographic and thus non-destructive way, with spatial resolutions at the nanometre scale. Whereas both volume electron microscopy and phase-contrast techniques use post-processing algorithms, such as FT, to provide the 3D orientation and arrangement of mineralized collagen fibrils at the nanoscale [226,247], phase-contrast approaches have the important advantage of being non-destructive, hence allowing further investigations on the tissue post hoc.…”

Section: Quantitative Assessment Of Three-dimensional Orientation Andmentioning

confidence: 99%

“…The applications of phase-contrast X-ray imaging techniques are rapidly increasing [222] and specific imaging modalities such as X-ray phase nanotomography [224] and ptychographic (or lensless) CT [225] have been used to image bone with spatial resolutions at the nanometre scale. The first studies on bone ultrastructure organization have been performed on volumes at the micrometre level [226] ( figure 12). Considering the capabilities of ptychographic CT for quantitative analysis of materials and tissues [227] at spatial resolutions below 20 nm [228], where single collagen fibrils could be resolved, phase-contrast methods offer the potential for a direct insight into bone ultrastructure organization of single osteons or trabeculae.…”

Section: Phase-contrast X-ray Imagingmentioning

confidence: 99%

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Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils

Georgiadis

Müller

Schneider

2016

J. R. Soc. Interface.

113

100

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Bone's remarkable mechanical properties are a result of its hierarchical structure. The mineralized collagen fibrils, made up of collagen fibrils and crystal platelets, are bone's building blocks at an ultrastructural level. The organization of bone's ultrastructure with respect to the orientation and arrangement of mineralized collagen fibrils has been the matter of numerous studies based on a variety of imaging techniques in the past decades. These techniques either exploit physical principles, such as polarization, diffraction or scattering to examine bone ultrastructure orientation and arrangement, or directly image the fibrils at the sub-micrometre scale. They make use of diverse probes such as visible light, X-rays and electrons at different scales, from centimetres down to nanometres. They allow imaging of bone sections or surfaces in two dimensions or investigating bone tissue truly in three dimensions, in vivo or ex vivo, and sometimes in combination with in situ mechanical experiments. The purpose of this review is to summarize and discuss this broad range of imaging techniques and the different modalities of their use, in order to discuss their advantages and limitations for the assessment of bone ultrastructure organization with respect to the orientation and arrangement of mineralized collagen fibrils.

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Section: Assessment At Different Hierarchical Levels and Additional Imentioning

confidence: 99%

Section: Quantitative Assessment Of Three-dimensional Orientation Andmentioning

confidence: 99%

Section: Phase-contrast X-ray Imagingmentioning

confidence: 99%

See 1 more Smart Citation

Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils

Georgiadis

Müller

Schneider

2016

J. R. Soc. Interface.

113

100

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“…Details of canalicular structure and branching, collagen fibre orientation and degrees of local bone mineralisation beyond microscopic scales were mapped in this study. X-ray phase nanotomography has also been applied by the same group to study the 3D orientation of mineralised collagen fibrils in human lamellar bone (Varga et al, 2013).…”

Section: Pm Goggin Et Almentioning

confidence: 99%

High-resolution 3D imaging of osteocytes and computational modelling in mechanobiology: insights on bone development, ageing, health and disease

Goggin

Zygalakis

Oreffo³

et al. 2016

eCM

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Osteocytes are involved in mechanosensation and mechanotransduction in bone and hence, are key to bone adaptation in response to development, ageing and disease. Thus, detailed knowledge of the three-dimensional (3D) structure of the osteocyte network (ON) and the surrounding lacuno-canalicular network (LCN) is essential. Enhanced understanding of the ON&LCN will contribute to a better understanding of bone mechanics on cellular and sub-cellular scales, for instance through improved computational models of bone mechanotransduction. Until now, the location of the ON within the hard bone matrix and the sub-µm dimensions of the ON&LCN have posed significant challenges for 3D imaging. This review identifies relevant microstructural phenotypes of the ON&LCN in health and disease and summarises how light microscopy, electron microscopy and X-ray imaging techniques have been used in studies of osteocyte anatomy, pathology and mechanobiology to date. In this review, we assess the requirements for ON&LCN imaging and examine the state of the art in the fields of imaging and computational modelling as well as recent advances in high-resolution 3D imaging. Suggestions for future investigations using volume electron microscopy are indicated and we present new data on the ON&LCN using serial block-face scanning electron microscopy. A correlative approach using these high-resolution 3D imaging techniques in conjunction with in silico modelling in bone mechanobiology will increase understanding of osteocyte function and, ultimately, lead to improved pathways for diagnosis and treatment of bone diseases such as osteoporosis.Keywords: Osteocyte, 3D imaging, microscopy, b i o m e c h a n i c s , l a c u n o -c a n a l i c u l a r n e t w o r k , mechanobiology, mechanosensation, mechanotransduction, osteoporosis. IntroductionThrough bone adaptation, the skeleton adapts continuously to changed mechanical loading patterns due to development, growth, ageing, disease, disuse or exercise, by removing existing and adding new bone tissue. It has been recognised that osteocytes are the key cells which orchestrate bone adaptation (Tatsumi et al., 2007). Osteocytes are ovoid cells approximately 10 µm long, surrounded by a pericellular matrix (PCM). The osteocytes and their processes form the osteocyte network (ON), which is housed within the lacuno-canalicular network (LCN), a system of voids and channels in the calcified bone matrix (Fig. 1). Neve et al., 2012). Knowledge of the three-dimensional (3D) structure of the ON&LCN would inform conclusions about the function and malfunction of osteocytes for different bone states in development, ageing, disease, disuse or exercise. More specifically, enhanced knowledge would improve the predictive power and accuracy of computational models, which attempt to elucidate the mechanisms of mechanotransduction using 3D geometries for the ON&LCN. Recent finite element and fluid-structure interaction models have used relatively low resolution image data and made a priori assumptions about the ...

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“…Using a combination of histology and holotomography, the authors characterized the artificial bone scaffold as well as the infused vessels showing that the experimental bone defect was filled with highly vascularized compact bone rather than with physiologically spongy bone. Exploiting projection geometries and nanoCT, holotomography was successfully used in bone to analyze spatial variations in mineralization at the micrometer length scale (in and around osteocyte cell lacunae) and collagen-fibril orientation variations (Varga et al, 2013). More recently, nanoCT-based holotomography was used as a basis for mechanical modeling of stresses and strains around osteocyte cells in bone .…”

mentioning

confidence: 99%

Combining Coherent Hard X-Ray Tomographies with Phase Retrieval to Generate Three-Dimensional Models of Forming Bone

et al. 2017

Self Cite

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Holotomography, a phase-sensitive synchrotron-based (µCT) modality, is a quantitative 3D imaging method. By exploiting partial spatial X-ray coherence, bones can be imaged volumetrically with high resolution coupled with impressive density sensitivity. This tomographic method reveals the main characteristics of the important tissue compartments in forming bones, including the rapidly changing soft tissue and the partially or fully mineralized bone regions, while revealing subtle density differences in 3D. Here, we show typical results observed within the growing femur bone midshafts of healthy mice that are 1, 3, 7, 10, and 14 days old (postpartum). Our results make use of partially coherent synchrotron radiation employing inline Fresnel propagation in multiple tomographic datasets obtained in the imaging beamline ID19 of the European Synchrotron Radiation Facility. The exquisite detail creates maps of the juxtaposed soft, partially mineralized and highly mineralized bone revealing the environment in which bone cells create and shape the matrix. This high-resolution 3D data can be used to create detailed computational models to study the dynamic processes involved in bone tissue formation and adaptation. Such data can enhance our understanding of the important biomechanical interactions directing maturation and shaping of the bone micro-and macro-geometries.

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Investigation of the three-dimensional orientation of mineralized collagen fibrils in human lamellar bone using synchrotron X-ray phase nano-tomography

Cited by 101 publications

References 52 publications

Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils

Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils

High-resolution 3D imaging of osteocytes and computational modelling in mechanobiology: insights on bone development, ageing, health and disease

Combining Coherent Hard X-Ray Tomographies with Phase Retrieval to Generate Three-Dimensional Models of Forming Bone

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