Quantitative 3D structural analysis of the cellular microstructure of sea urchin spines

Significance 

Microstructures of natural cellular solids are diverse; they include honeycombs, closed-cell foams and open-cell foams. These structures are often used for mechanics-related functions by organisms, for example, the porous trabecular bony skeletons in organisms provide body support while the cellular structures in wood or other plants provide stiffness and strength to resist mechanical deformation and failure. In particular, the mechanical robustness of the biomineralized porous structures in sea urchin spines has long been recognized. Existing literature reveals that such mineralized skeletons of echinoderms are characterized by their complex, open-cell porous microstructure (also known as stereom), which exhibits vast variations in pore sizes, branch morphology, and three-dimensional (3D) organization patterns among different species. However, quantitative cellular network representation and analysis of this class of natural cellular solids are still limited. This constrains our capability to fully understand the mechanical properties and design strategies in sea urchin spines and other similar echinoderms’ porous skeletal structures.

Biological cellular materials have been a valuable source of inspiration for the design of lightweight engineering structures. As acknowledged in part one of the study, a quantitative understanding of the biological cellular materials from the individual branch and node level to the global network level in 3D for sea urchins is required. Previous investigations on the cellular structures of sea urchin spines have been mainly based on 2D measurements or 3D quantification of small volumes with limited structural parameters. This limits our understanding of the interplay between the 3D microstructural variations and the mechanical properties in sea urchin spines, which hence constrains the derivation of the underlying principles for bio-inspired designs.

On this account, Virginia Tech scientists: Ting Yang, Ziling Wu, Zhifei Deng, Hongshun Chen, Professor Yunhui Zhu and Professor Ling Li, proposed a new framework for analyzing such structures based on high-resolution 3D tomography data. Their studies were comprehensive and covered into two articles: one focused on methodology where the team focused on developing a viable methodology for investigating the multiscale 3D cellular network structure, and in the second sequel publication, the authors discussed large-volume structural analysis where the team adopted the multiscale cellular network analysis workflow demonstrated in the first paper to analyze the biomineralized porous structure of sea urchin spines from the species Heterocentrotus mammillatus over a large volume (ca. 0.32mm3). The two research papers are currently published in the research journal, Acta Biomaterialia.

In their approach, they combined high-resolution tomography and computer vision-based structural analysis. This enabled them present a multiscale 3D network analysis framework, which allowed for extraction, registration, and quantification of sea urchin spines’ complex porous structure from the individual branch and node level to the global network level. This was presented as part I (i.e. methodology) of the two publications, and it mainly encompassed the development of a detailed framework for data analysis pipeline with the hope of demonstrating its capability in analyzing a representative volume from sea urchin spines. Remarkably, the researchers reported that their analysis was able to reveal the porous structure of sea urchin spines; which was primarily composed of three- and four-branched nodes, that resembled ideal branched structures that span 3D space maximally. Additionally, it was reported that the thickness and length of branches were highly correlated with their orientation, whereby shorter and thicker branches were aligned with the longitudinal direction of the spines in the analyzed regions close to the center of the spines.

In part II of their research work, the developed multiscale 3D network analysis framework was used to quantitatively delineate the long-range microstructural variation from the spine center to the edge region. Moreover, structural analysis was performed on isolated septa, a key structural motif for the porous stereom structure in H. mammillatus spines, to investigate the interconnection characteristics between adjacent septa. The cellular network information obtained from this multiscale analysis was also used to investigate the spatial variation of the mechanical properties across the entire volume of interest via finite element modeling of the extracted cellular networks. Based on the implemented analysis, it was shown that the branches of the assessed sea urchins gradually elongate (~50% increase) and thicken (~100% increase) from the spine center to edge, which dictates the spatial variation of relative density (from ~12% to ~40%). The branch morphology and network organization patterns were also reported to vary gradually with their positions and orientations. Additionally, the analysis of the cellular network of individual septum provided the interconnection characteristics between adjacent septa, which are again connected through low-connectivity nodes (three- or four-branched nodes).

In summary, the methodology (part I) presented a computational tomography analysis pipeline for multiscale structural representation and quantification of biological cellular materials by using sea urchin spines as an example; while as, the second publication adopted the multiscale network analysis algorithm developed in the first paper to conduct, to the best of the authors’ knowledge, the first comprehensive, quantitative analysis of the cellular network on the H. mamillatus spines over a large volume in 3D. Overall, it was anticipated that the network analysis demonstrated could be of great interest to the fields of biomineralization, functional biological materials, and bio-inspired material design.

In a statement to Advances in Engineering, Professor Ling Li said their findings could provide new insights in the development of bio-inspired lightweight structures with structural controls at multiple length scales. Further, Professor Ling Li and colleagues envisioned that the presented large-scale cellular network analysis approach could be readily applied to other sea urchin spines for potential inter-species structural comparison, or other echinoderms’ porous skeletal elements, or other natural and engineering cellular materials in general.

Quantitative 3D structural analysis of the cellular microstructure of sea urchin spines  - Advances in Engineering
A scanning electron microscopy image showing the porous microstructure of a sea urchin. The image measures 1 mm in size. Credit: Dr. James C. Weaver.

References

Ting Yang, Ziling Wu, Hongshun Chen, Yunhui Zhu, Ling Li. Quantitative 3D structural analysis of the cellular microstructure of sea urchin spines (I): Methodology. Acta Biomaterialia, volume 107 (2020) 204–217

Go To Acta Biomaterialia

Hongshun Chen, Ting Yang, Ziling Wu, Zhifei Deng, Yunhui Zhu, Ling Li. Quantitative 3D structural analysis of the cellular microstructure of sea urchin spines (II): Large-volume structural analysis. Acta Biomaterialia, volume 107 (2020) 218–231.

Go To Acta Biomaterialia

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