Correlative multiscale tomography of biological materials
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Introduction Biological materials are generally characterized as having complex three-dimensional (3D) hierarchical microstructures,1 giving rise to interesting combinations of anisotropic mechanical properties that, in many cases, surpass those of manmade materials.2 Consequently, much can be learned from a detailed study of their structure–property relationships.3 As discussed by Vincent,4 these materials are often composites of organic and inorganic components that exploit strong fibers, such as cellulose (e.g., wood, spider silk, and cuticle), or ceramics based around calcium carbonate (e.g., nacre), silica (e.g., the skeleton of Euplectella, a genus of deep water sponges), or hydroxyapatite (e.g., bone).5 The resultant combinations of properties are all the more surprising since the constituent components typically exhibit relatively ordinary properties in isolation.6 The overall properties of biological materials rely on the use of hard and soft materials in combination with carefully controlled interfacial properties, as well as morphological optimization across many length scales, as illustrated in Figure 1. A better understanding of these hierarchical structures requires a multiscale correlative imaging approach, which brings together 3D information at each length scale.7 Multiscale imaging is highly challenging because no single technique can provide all the information. Optical techniques are suitable for translucent tissues,8 while 3D scanning electron microscopy
(SEM) serial sectioning techniques achieve resolutions of tens of nanometers, but only over 100-μm volumes, and are not amenable to temporal 3D studies of the same specimen. In this respect, x-ray computed tomography (CT) is uniquely placed as a noninvasive technique able to provide 3D images across a wide range of resolutions from hundreds of micrometers to tens of nanometers. However, the technique has traditionally been limited by poor contrast for soft tissues. A further challenge for biological imaging is the x-ray dose. For in vivo imaging of mammals, the dose needs to be limited to 1.5 kGy) for insects, which are much more radiation tolerant.9 In general, the required dose to achieve a given contrast-to-noise ratio increases as the fourth power of resolution.10 Higher doses can be used for ex vivo samples, with cryo-preservation techniques able to mitigate against dose effects for imaging down to ∼30-nm resolution.11 Higher resolutions can be achieved by coherent diffraction imaging techniques (“lensless” imaging). Howells et al.10 postulated that an ultimate dose limit exists due to damage to proteins of ∼108 Gy per nanometer of resolution. This article reviews recent advances in x-ray imaging techniques for studying the role of hierarchical structures in controlling the mechanical behavior of biomaterials. In particular, new opportunities to study the relationship between microstructurally controlled propagation of damage and performance through time-lapse 3D imaging are highlighted.
Robert S. Bradley, The University of Manchester, UK
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