Human bone is a complex hierarchical material. Understanding bone structure and its corresponding composition at the nanometer scale is critical for elucidating mechanisms of biomineralization under healthy and pathological states. However, the three-dimensional structure and chemical nature of bone remains largely unexplored at the nanometer scale due to the challenges associated with characterizing both the structural and chemical integrity of bone simultaneously. Here, we use correlative transmission electron microscopy and atom probe tomography for the first time, to our knowledge, to reveal structures in human bone at the atomic level. This approach provides an overlaying chemical map of the organic and inorganic constituents of bone on its structure. This first use of atom probe tomography on human bone reveals local gradients, trace element detection of Mg, and the co-localization of Na with the inorganic-organic interface of bone mineral and collagen fibrils, suggesting the important role of Na-rich organics in the structural connection between mineral and collagen. Our findings provide the first insights into the hierarchical organization and chemical heterogeneity in human bone in three-dimensions at its smallest length scale – the atomic level. We demonstrate that atom probe tomography shows potential for new insights in biomineralization research on bone.

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At an implant biointerface, where an engineered material merges into a biological environment, complex biophysicochemical interactions occur. One typical biointerface is the bond between human bone and dental or orthopedic implants, which is based on the biomineralization of essential bone components such as hydroxyapatite, at the implant surface. However, the exact bonding mechanism between bone and implants is still unclear. The distribution of both the mineralized and organic components of bone at the interface, and their origins, requires improved characterization. Here, the first correlative characterization is reported using multiple‐length‐scale tomography and spectroscopy techniques to probe the chemical structure of the biointerface between human bone and commercial titanium dental implant down to the atomic scale in four dimensions (4D). The existence of an intervening transition zone bonding mature bone tissue is demonstrated to implant at multiple length scales, where the phase of bone mineral differs immediately adjacent to the implant and atomic‐scale osseointegration is confirmed. The correlative 4D electron energy loss spectroscopy tomography and atom probe tomography workflow established herein is transferable to other applications in materials or biological sciences.

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