Opportunities for biomineralization research using multiscale computed X-ray tomography as exemplified by bone imaging

Wittig, Nina Kølln; Østergaard, Maja; Palle, Jonas; Christensen, Thorbjørn Erik Køppen; Langdahl, Bente; Rejnmark, Lars; Hauge, Ellen‐Margrethe; Brüel, Annemarie; Thomsen, Jesper Skovhus; Birkedal, Henrik

doi:10.1016/j.jsb.2021.107822

Cited by 16 publications

(14 citation statements)

References 29 publications

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“…One suitable approach is the use of X-ray imaging techniques that have developed tremendously over the past decade or so, see Withers et al (2021) for an introduction. In particular, the prospects of multimodal and/or multiscale X-ray imaging are exciting, as was recently reported using high-energy synchrotron X-ray phase contrast imaging (Walsh et al, 2021) or by combination of laboratory and synchrotron instrumentation (Wittig et al, 2022) (Fig. 2).…”

Section: Composition and Hierarchiesmentioning

confidence: 90%

“…2019), in particular, 3D focussed ion beam SEM (FIB-SEM) imaging (Weiner et al, 2021), atomic force microscopy (AFM), that additionally affords local mechanical information (Rux et al, 2022;Zhang et al, 2015), or confocal laser scanning microscopy (CLSM) on dye infused bone (Kerschnitzki et al, 2011(Kerschnitzki et al, , 2013van Tol et al, 2020), have been very useful. On larger length scales, where focus is mainly on osteocyte lacunae, both laboratory and synchrotron 3D X-ray imaging is useful (Wittig et al, 2022) (Fig. 2).…”

Section: Nanoscale Features Of the Osteocyte Lacunocanalicular Networkmentioning

confidence: 99%

“…The cellular network in bone is challenging to study in the full context of the biomineralized tissue since the cells are entombed in the poorly transparent bone matrix (Goggin et al, 2016). X-ray imaging is in principle well suited for this purpose (Palle et al, 2019;Wittig et al, 2022), as illustrated in Fig. 2, but have only over the past decade or two reached resolutions that allow mapping of the full network, including the 100s of nm wide canaliculi.…”

Section: Nanoscale Features Of the Osteocyte Lacunocanalicular Networkmentioning

confidence: 99%

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Bone hierarchical structure: spatial variation across length scales

Wittig¹,

Birkedal²

2022

Acta Crystallogr B Struct Sci Cryst Eng Mater

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Bone is a complex hierarchical biomineralized material, which is special amongst biominerals because it is replete with cells, namely, osteocytes. While bone has been scrutinized for centuries, many questions remain open and new research hints that the ultrastructure of bone, encompassing both the bone matrix itself and the embedded cell network, is much more heterogeneous than hitherto realized. A number of these new findings have been made thanks to the enormous developments in X-ray imaging that have occurred in recent decades, and there is promise that they will also allow many of the remaining open questions to be addressed. X-ray absorption or phase imaging affords high three-dimensional (3D) resolution and allows traversing the length scales of bone all the way down to the fine details of the lacuno-canalicular network housing the osteocytes. Multimodal X-ray imaging provides combined information covering both the length scales defined by the size of the measured volume and tomographic resolution, as well as those probed by the signal that is measured. In X-ray diffraction computed tomography (XRD-CT), for example, diffraction signals can be reconstructed tomographically, which offers detailed information about the spatial variations in the crystallographic properties of the bone biomineral. Orientational information can be obtained by tensor tomography. The combination of both small-angle X-ray scattering (SAXS) and wide-angle X-ray scattering (WAXS) tensor tomography gives information on the orientation of bone nanostructure and crystals, respectively. These new technical developments promise that great strides towards understanding bone structure can be expected in the near future. In this review, recent findings that have resulted from X-ray imaging are highlighted and speculation is given on what can be expected to follow.

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Section: Composition and Hierarchiesmentioning

confidence: 90%

Section: Nanoscale Features Of the Osteocyte Lacunocanalicular Networkmentioning

confidence: 99%

Section: Nanoscale Features Of the Osteocyte Lacunocanalicular Networkmentioning

confidence: 99%

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Bone hierarchical structure: spatial variation across length scales

Wittig¹,

Birkedal²

2022

Acta Crystallogr B Struct Sci Cryst Eng Mater

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“…Thanks to the high X-ray photon flux and spatial coherence achieved at modern fourth-generation synchrotron sources and careful design of the sample preparation and imaging protocol, it is now possible to image complete, large, partially dehydrated human organs in their entirety at micrometer resolution using hierarchical phase-contrast tomography (HiP-CT) 26 . The technique integrates a multiscale imaging workflow 4 , 27 – 30 into a single setup, utilizing propagation phase contrast obtained from high-energy, polychromatic X-rays and tunable detection settings. Therefore, scanning an entire human organ (with a size of 5–30 cm in each dimension) at multiple resolutions can be executed without dissecting the sample or requiring to transport to different instrument locations or facilities 27 , 28 , 30 .…”

Section: Background and Summarymentioning

confidence: 99%

“…The technique integrates a multiscale imaging workflow 4 , 27 – 30 into a single setup, utilizing propagation phase contrast obtained from high-energy, polychromatic X-rays and tunable detection settings. Therefore, scanning an entire human organ (with a size of 5–30 cm in each dimension) at multiple resolutions can be executed without dissecting the sample or requiring to transport to different instrument locations or facilities 27 , 28 , 30 . HiP-CT features a customized flat-field correction, an attenuation scanning protocol, along with an efficient tomographic sampling and stitching pipeline to cover large, soft-tissue organs entirely, without staining 27 , 31 or clearing 10 .…”

Section: Background and Summarymentioning

confidence: 99%

A multiscale X-ray phase-contrast tomography dataset of a whole human left lung

et al. 2022

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Technological advancements in X-ray imaging using bright and coherent synchrotron sources now allows the decoupling of sample size and resolution while maintaining high sensitivity to the microstructures of soft, partially dehydrated tissues. The continuous developments in multiscale X-ray imaging resulted in hierarchical phase-contrast tomography, a comprehensive approach to address the challenge of organ-scale (up to tens of centimeters) soft tissue imaging with resolution and sensitivity down to the cellular level. Using this technique, we imaged ex vivo an entire human left lung at an isotropic voxel size of 25.08 μm along with local zooms down to 6.05–6.5 μm and 2.45–2.5 μm in voxel size. The high tissue contrast offered by the fourth-generation synchrotron source at the European Synchrotron Radiation Facility reveals the complex multiscale anatomical constitution of the human lung from the macroscopic (centimeter) down to the microscopic (micrometer) scale. The dataset provides comprehensive organ-scale 3D information of the secondary pulmonary lobules and delineates the microstructure of lung nodules with unprecedented detail.

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Bone Hierarchical Structure: Heterogeneity and Uniformity

Rodriguez‐Palomo,

Østergaard,

Birkedal

2023

Adv Funct Materials

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Bone has a complex hierarchical structure with structural integration from nm to cm. The understanding of bone structure is developing rapidly due to improvements in available methodologies that allow unravelling structures across several length scales. These methods include advances in electron microscopy, in particular, focused ion beam scanning electron microscopy (FIB‐SEM), confocal laser scanning microscopy techniques, X‐ray imaging, X‐ray diffraction tomography (XRD‐CT), and tensor tomography (small angle X‐ray scattering tensor tomgraphy, SAXS‐TT and wide angle X‐ray scattering tensor tomgraphy, WAXS‐TT). Special emphasis is placed on the latter X‐ray techniques that are emerging into powerful tools. Through a review of selected recent results on the structure of the bone matrix as well as the lacuno‐canalicular network housing the osteocyte cells of bone, it is proposed that bone is more heterogeneous than typically described and that local variation in composition and crystallography may play a significant role in bone biology in health and disease.

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Opportunities for biomineralization research using multiscale computed X-ray tomography as exemplified by bone imaging

Cited by 16 publications

References 29 publications

Bone hierarchical structure: spatial variation across length scales

Bone hierarchical structure: spatial variation across length scales

A multiscale X-ray phase-contrast tomography dataset of a whole human left lung

Bone Hierarchical Structure: Heterogeneity and Uniformity

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