Focused ion beam-SEM 3D analysis of mineralized osteonal bone: lamellae and cement sheath structures

Currey, 1984 Gebhardt, 1905, Ueber funktionell wichtige Anordnungsweisen der eineren und groberen Bauelemente des Wirbeltierknochens.II. Spezieller Teil Der Bau der Haversschen Lamellensysteme und seine funktionelle Bedeutung, Arch. Entwickl. Mech. Org, 20, 187, 10.1007/BF02162810 Giraud-Guille, 1988, Twisted plywood architecture of collagen fibrils in human compact bone osteons, Calcif. Tissue Int., 167, 10.1007/BF02556330 Reznikov, 2014, Three-dimensional structure of human lamellar bone: the presence of two different materials and new insights into the hierarchical organization, Bone, 59, 93, 10.1016/j.bone.2013.10.023 Marotti, 1993, A new theory of bone lamellation, Calcif. Tissue Int., 101 Weiner, 1997, Rotated plywood structure of primary lamellar bone in the rat: orientations of the collagen fibril arrays, Bone, 20, 271, 10.1016/S8756-3282(97)00053-7 Varga, 2013, Investigation of the three-dimensional orientation of mineralized collagen fibrils in human lamellar bone using synchrotron X-ray phase nano-tomography, Acta Biomater, 9, 8118, 10.1016/j.actbio.2013.05.015 Wagermaier, 2006, Spiral twisting of fiber orientation inside bone lamellae, Biointerphases, 1, 1, 10.1116/1.2178386 Palle, 2020, Nanobeam X-ray fluorescence and diffraction computed tomography on human bone with a resolution better than 120 nm, J. Struct. Biol, 212, 10.1016/j.jsb.2020.107631 Georgiadis, 2015, 3D scanning SAXS: a novel method for the assessment of bone ultrastructure orientation, Bone, 71, 45, 10.1016/j.bone.2014.10.002 Grünewald, 2020, Mapping the 3D orientation of nanocrystals and nanostructures in human bone: Indications of novel structural features, Science Adv., 6, 10.1126/sciadv.aba4171 Schaff, 2015, Six-dimensional real and reciprocal space small-angle X-ray scattering tomography, Nature, 527, 353, 10.1038/nature16060 Liebi, 2015, Nanostructure surveys of macroscopic specimens by small-angle scattering tensor tomography, Nature, 527, 349, 10.1038/nature16056 Reznikov, 2015, The 3D structure of the collagen fibril network in human trabecular bone: relation to trabecular organization, Bone, 71, 189, 10.1016/j.bone.2014.10.017 Reznikov, 2014, Bone hierarchical structure in three dimensions, Acta Biomaterialia, 10, 3815, 10.1016/j.actbio.2014.05.024 Earl, 2010, Characterization of dentine structure in three dimensions using FIB-SEM, J. Microsc, 240, 1, 10.1111/j.1365-2818.2010.03396.x Schneider, 2011, Serial FIB/SEM imaging for quantitative 3D assessment of the osteocyte lacuno-canalicular network, Bone, 49, 304, 10.1016/j.bone.2011.04.005 Heymann, 2006, Site-specific 3D imaging of cells and tissues with a dual beam microscope, J. Struct. Biol., 155, 63, 10.1016/j.jsb.2006.03.006 Stokes, 2006, A new approach to studying biological and soft materials using focused ion beam scanning electron microscopy (FIB SEM), J. Phys. Conf. Ser, 26, 50, 10.1088/1742-6596/26/1/012 Zou, 2020, Three-dimensional structural interrelations between cells, extracellular matrix, and mineral in normally mineralizing avian leg tendon, Proc. Natl. Acad. Sci. USA, 117, 14102, 10.1073/pnas.1917932117 Buss, 2020, Crossfibrillar mineral tessellation in normal and Hyp mouse bone as revealed by 3D FIB-SEM microscopy, J. Struct. Biol., 212, 10.1016/j.jsb.2020.107603 Georgiadis, 2017, Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils, J. R. Soc. Interface, 13 Shahar, 2018, Open questions on the 3D structures of collagen containing vertebrate mineralized tissues: A perspective, J. Struct. Biol., 201, 187, 10.1016/j.jsb.2017.11.008 Weiner, 1998, The material bone: structure- mechanical function relations, Ann. Rev. Mat. Sci., 28, 271, 10.1146/annurev.matsci.28.1.271 Raguin, 2020, Unique three-dimensional structure of a fish mandible bone subjected to unusually high mechanical loads, J. Struct. Biol., 211, 10.1016/j.jsb.2020.107530 Giannuzzi, 2005 V. von Ebner. in Akad. Wiss. Wien. Math-naturwiss. 90 (1875). Hattner, 1965, Suggested sequential mode of control of changes in cell behaviour in adult bone remodelling, Nature, 206, 489, 10.1038/206489a0 Jaffe, 1929, The structure of bone with particular relevance to its fibrillar nature and the relationship of function to internal architecture, Archives Surgery, 19, 24, 10.1001/archsurg.1929.01150010027002 Burr, 1988, Composition of the cement line and its possible mechanical role as a local interface in human compact bone, J. Biomech., 21, 939, 10.1016/0021-9290(88)90132-7 Jepsen, 1999, The role of the lamellar interface during torsional yielding of human cortical bone, J. Biomech, 32, 303, 10.1016/S0021-9290(98)00179-1 Amprino, 1952, Studies on Xray absorption and diffraction of bone tissue, Acta Anat, 15, 1, 10.1159/000140734 Philipson, 1965, Composition of cement lines in bone, J. Histochem. Cytochem., 13, 270, 10.1177/13.4.270 Skedros, 2005, Cement lines of secondary osteons in human bone are not mineral-deficient: New data in a historical perspective, Anat. Rec., 286A, 781, 10.1002/ar.a.20214 Smith, 1963, Age changes in the organic fraction of bone, J. Bone Joint Surg, 45B, 761, 10.1302/0301-620X.45B4.761 Milovanovic, 2018, Bone tissue aging affects mineralization of cement lines, Bone, 110, 187, 10.1016/j.bone.2018.02.004 Langer, 2012, X-ray phase nanotomography resolves the 3D human bone ultrastructure, PloS ONE, 7, e35691, 10.1371/journal.pone.0035691 Schaffler, 1987, Morphology of the osteonal cement line in human bone, Anat. Rec., 217, 223, 10.1002/ar.1092170302 Dempster, 1960, Tensile strength of bone along and across the grain, J. Appl. Physiol., 16, 355, 10.1152/jappl.1961.16.2.355 Frasca, 1981, Strain and frequency dependence of shear modulus for human single osteons and cortical bone microsamples - size and hydration effects, J. Biomech, 14, 679, 10.1016/0021-9290(81)90050-6 Beaupre, 1990, An approach for time-dependent bone modeling and remodeling-application: a preliminary remodeling simulation, J. Orthop. Res., 8, 662, 10.1002/jor.1100080507 Zuiderveld, 1994, 474 Clemons, 2018, Coherency image analysis to quantify collagen architecture: implications in scar assessment, RSC Adv., 8, 9661, 10.1039/C7RA12693J K.U. Barthel, in 1st ImageJ User and Developer Conference, Luxembourg, Luxembourg, 2006. Liu, 1991, Scale space approach to directional analysis of images, Appl. Opt., 30, 1369, 10.1364/AO.30.001369 Arsenault, 1991, Image analysis of collagen-associated mineral distribution in cryogenically prepared turkey leg tendons, Calc. Tissue Intl., 48, 56, 10.1007/BF02555796 Arsenault, 1983, Quantitative spatial distributions of calcium, phosphorus, and sulfur in calcifying epiphysis by high resolution electron spectroscopic imaging, Proc. Natl. Acad. Sci. USA, 80, 1322, 10.1073/pnas.80.5.1322 Almany-Magal, 2014, Three-dimensional structure of minipig fibrolamellar bone: Adaptation to axial loading, J. Struct. Biol, 186, 10.1016/j.jsb.2014.03.007 Reznikov, 2013, Three-dimensional imaging of collagen fibril organization in rat circumferential lamellar bone using a dual beam electron microscope reveals ordered and disordered sub-lamellar structures, Bone, 52, 676, 10.1016/j.bone.2012.10.034 Silvent, 2017, Zebrafish skeleton development: high resolution micro-CT imaging and FIB-SEM block surface serial imaging for phenotype identification, PLoS ONE, 12, 10.1371/journal.pone.0177731 Atkins, 2015, The three-dimensional structure of anosteocytic lamellated bone of fish, Acta Biomaterialia, 13, 311, 10.1016/j.actbio.2014.10.025 Hasegawa, 2017, Biological application of focus ion beam-scanning electron microscopy (FIB-SEM) to the imaging of cartilaginous fibrils and osteoblastic cytoplasmic processes, J. Oral Bioscience, 59, 55, 10.1016/j.job.2016.11.004 Wittig, 2019, Bone biomineral properties vary across human osteonal bone, ACS Nano, 13, 12949, 10.1021/acsnano.9b05535 Landis, 1991, Early mineral deposition in calcifying tendon characterized by high voltage electron microscopy and three-dimensional graphic imaging, J. Struct. Biol., 107, 116, 10.1016/1047-8477(91)90015-O McKee, 1996, Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair, Microsc. Res. Technique, 33, 141, 10.1002/(SICI)1097-0029(19960201)33:2<141::AID-JEMT5>3.0.CO;2-W Milovanovic, 2013, Osteocytic canalicular networks: morphological implications for altered mechanosensitivity, ACS NANO, 7, 7542, 10.1021/nn401360u Hirose, 2007, A histological assessment on the distribution of the osteocytic lacunar canalicular system using silver staining, J. Bone Miner. Metab., 25, 374, 10.1007/s00774-007-0764-x Curtis, 1985, Canalicular communication in the cortices of human long bones, Anat Rec, 212, 336, 10.1002/ar.1092120403 Kerschnitzki, 2016, Bone mineralization pathways during the rapid growth of embryonic chicken long bones, J. Struct. Biol, 195, 82, 10.1016/j.jsb.2016.04.011 Reznikov, 2020, Deep learning and 3D imaging in structural biology, J. Struct. Biol, 212, 10.1016/j.jsb.2020.107598 Haimov, 2020, Mineralization pathways in the active murine epiphyseal growth plate, Bone, 130, 10.1016/j.bone.2019.115086 Akiva, 2019, Intercellular pathways from the vasculature to the forming bone in the zebrafish larval caudal fin: Possible role in bone formation, J. Struct. Biol., 206, 139, 10.1016/j.jsb.2019.02.011