Micro- and nano-CT for the study of bone ultrastructure

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Peyrin, Françoise^1,2,3,4,5,6; Dong, Pei^1,2,3,4,5,6; Pacureanu, Alexandra⁶; Langer, Max^1,2,3,4,5,6

Micro- and nano-CT for the study of bone ultrastructure

Curr Osteoporos Rep. December 2014;12(4):465-474

©2014 Springer Science+Business Media New York

Affiliations

¹INSERM U1044, CREATIS, 69621 Villeurbanne, France

²INSA-Lyon, 69621 Villeurbanne, France

³CNRS UMR 5220, 69621 Villeurbanne, France

⁴Université de Lyon, 69622 Lyon, France

⁵Université Lyon 1, 69622 Villeurbanne, France

⁶European Synchrotron Radiation Facility, BP 220, 38043 Grenoble, Cedex, France
Abstract and keywords

Micro-computed tomography (micro-CT)—a version of X-ray CT operating at high spatial resolution—has had a considerable success for the investigation of trabecular bone micro-architecture. Currently, there is a lot of interest in exploiting CT techniques at even higher spatial resolutions to assess bone tissue at the cellular scale. After recalling the basic principles of micro-CT, we review the different existing system, based on either standard X-ray tubes or synchrotron sources. Then, we present recent applications of micro- and nano-CT for the analysis of osteocyte lacunae and the lacunar-canalicular network. We also address the question of the quantification of bone ultrastructure to go beyond the sole visualization.

Keywords: Computerized tomography; Synchrotron imaging; Micro-CT; Nano-CT; X-ray phase CT; Bone ultrastructure; Osteocyte lacunae; Canaliculi; Lacunar canalicular network; Bone quality; Lacunar density; Quantification
Links

DOI: 10.1007/s11914-014-0233-0

PubMed: 25292366

WoS: 000347284400011
History

Online: 2014-10-08

Cited Works (32)

Year	Entry
2002	Nuzzo S, Peyrin F, Cloetens P, Baruchel J, Boivin G. Quantification of the degree of mineralization of bone in three dimensions using synchrotron radiation microtomography. Med Phys. November 2002;29(11):2672-2681.
2007	Schneider P, Stauber M, Voide R, Stampanoni M, Donahue LR, Müller R. Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro‐ and nano‐CT. J Bone Miner Res. October 2007;22(10):1557-1570.
1993	Engelke K, Graeff W, Meiss L, Hahn M, Delling G. High spatial resolution imaging of bone mineral using computed microtomography: comparison with microradiography and undecalcified histologic sections. Invest Radiol. April 1993;28(4):341-349.
1996	Rüegsegger P, Koller B, Müller R. A microtomographic system for the nondestructive evaluation of bone architecture. Calcif Tiss Int. 1996;58(1):24-29.
2012	Sharma D. Effects of Estrogen Deficiency on the Osteocyte Lacunar-Canalicular Network [PhD thesis]. New York, NY: The City University of New York; 2012.
2004	Bousson V, Peyrin F, Bergot C, Hausard M, Sautet A, Laredo J. Cortical bone in the human femoral neck: three‐dimensional appearance and porosity using synchrotron radiation. J Bone Miner Res. May 2004;19(5):794-801.
2004	Knothe Tate ML, Adamson JR, Tami AE, Bauer TW. The osteocyte. Int J Biochem Cell Biol. January 2004;36(1):1-8.
2005	Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. December 2005;90(12):6508-6515.
2014	Carriero A, Doube M, Vogt M, Busse B, Zustin J, Levchuk A, Schneider P, Müller R, Shefelbine SJ. Altered lacunar and vascular porosity in osteogenesis imperfecta mouse bone as revealed by synchrotron tomography contributes to bone fragility. Bone. April 2014;61:116-124.
2005	Sugawara Y, Kamioka H, Honjo T, Tezuka K-i, Takano-Yamamoto T. Three-dimensional reconstruction of chick calvarial osteocytes and their cell processes using confocal microscopy. Bone. May 2005;36(5):877-883.
2008	Vatsa A, Breuls RG, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J. Osteocyte morphology in fibula and calvaria: is there a role for mechanosensing? Bone. September 2008;43(3):452-458.
2011	Barth HD, Zimmermann EA, Schaible E, Tang SY, Alliston T, Ritchie RO. Characterization of the effects of x-ray irradiation on the hierarchical structure and mechanical properties of human cortical bone. Biomaterials. December 2011;32(34):8892-8904.
2010	Barth HD, Launey ME, MacDowell AA, Ager JW III, Ritchie RO. On the effect of X-ray irradiation on the deformation and fracture behavior of human cortical bone. Bone. June 2010;46(6):1475-1485.
1998	Peyrin F, Salome M, Cloetens P, Laval-Jeantet AM, Ritman E, Rüegsegger P. Micro-ct examinations of trabecular bone samples at different resolutions: 14, 7 and 2 micron level. Technol Health Care. 1998;6(5-6):391-401.
2006	Bonewald LF. Mechanosensation and transduction in osteocytes. BoneKEy Osteovision. October 2006;3(10):7-15.
2013	Kerschnitzki M, Kollmannsberger P, Burghammer M, Duda GN, Weinkamer R, Wagermaier W, Fratzl P. Architecture of the osteocyte network correlates with bone material quality. J Bone Miner Res. December 2013;28(8):1837-1845.
2011	Cooper DML, Erickson B, Peele AG, Hannah K, Thomas CDL, Clement JG. Visualization of 3D osteon morphology by synchrotron radiation micro-CT. J Anat. October 2011;219(4):481-489.
2009	van Hove RP, Nolte PA, Vatsa A, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J. Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density: is there a role for mechanosensing? Bone. August 2009;45(2):321-329.
2010	Schneider P, Meier M, Wepf R, Müller R. Towards quantitative 3d imaging of the osteocyte lacuno-canalicular network. Bone. November 2010;47(5):848-858.
1984	Feldkamp LA, Davis LC, Kress JW. Practical cone-beam algorithm. J Opt Soc Am. 1984;A1(6):612-619.
2014	Reznikov N, Shahar R, Weiner S. Three-dimensional structure of human lamellar bone: the presence of two different materials and new insights into the hierarchical organization. Bone. February 2014;59:93-104.
2004	McCreadie BR, Hollister SJ, Schaffler MB, Goldstein SA. Osteocyte lacuna size and shape in women with and without osteoporotic fracture. J Biomech. April 2004;37(4):563-572.
2007	Taylor D, Hazenberg JG, Lee TC. Living with cracks: damage and repair in human bone. Nat Mater. April 2007;6(4):263-268.
2012	Verbruggen SW, Vaughan TJ, McNamara LM. Strain amplification in bone mechanobiology: a computational investigation of the in vivo mechanics of osteocytes. J R Soc Interface. October 7, 2012;9(75):2735-2744.
2008	Seeman E. Bone quality: the material and structural basis of bone strength. J Bone Min Metab. 2008;26(1):1-8.
2001	Kamioka H, Honjo T, Takano-Yamamoto T. A three-dimensional distribution of osteocyte processes revealed by the combination of confocal laser scanning microscopy and differential interference contrast microscopy. Bone. February 2001;28(2):145-149.
2013	Carter Y, Thomas CDL, Clement JG, Peele AG, Hannah K, Cooper DM. Variation in osteocyte lacunar morphology and density in the human femur: a synchrotron radiation micro-CT study. Bone. January 2013;52(1):126-132.
1999	Burger EH, Klein-Nulend J. Mechanotransduction in bone: role of the lacunocanalicular network. FASEB J. May 1999;12(9001):S101-S112.
2011	Bonewald LF. The amazing osteocyte. J Bone Miner Res. 2011;26(2):229-238.
1996	Mullender MG, van der Meer DD, Huiskes R, Lips P. Osteocyte density changes in aging and osteoporosis. Bone. February 1996;18(2):109-113.
2011	Schneider P, Meier M, Wepf R, Müller R. Serial FIB/SEM imaging for quantitative 3D assessment of the osteocyte lacuno-canalicular network. Bone. August 2011;49(2):304-311.
2013	Klein-Nulend J, Bakker AD, Bacabac RG, Vatsa A, Weinbaum S. Mechanosensation and transduction in osteocytes. Bone. June 2013;54(2):182-190.

Cited By (17)

Year	Entry
2021	Ahn T, Gidley DW, Thornton AW, Wong-Foy AG, Orr BG, Kozloff KM, Banaszak Holl MM. Hierarchical nature of nanoscale porosity in bone revealed by positron annihilation lifetime spectroscopy. ACS Nano. March 23, 2021;15(3):4321-4334.
2021	Vahidi G, Rux C, Sherk VD, Heveran CM. Lacunar-canalicular bone remodeling: impacts on bone quality and tools for assessment. Bone. February 2021;143:115663.
2022	Rux CJ, Vahidi G, Darabi A, Cox LM, Heveran CM. Perilacunar bone tissue exhibits sub-micrometer modulus gradation which depends on the recency of osteocyte bone formation in both young adult and early-old-age female C57Bl/6 mice. Bone. April 2022;157:116327.
2020	Maghsoudi-Ganjeh M, Wang X, Zeng X. Nanomechanics and ultrastructure of bone: a review. Comput Model Eng Sci. 2020;125(1):1-32.
2020	Le Cann S, Tudisco E, Tägil M, Hall SA, Isaksson H. Bone damage evolution around integrated metal screws using x-ray tomography: in situ pullout and digital volume correlation. Front Bioeng Biotechnol. August 5, 2020;8:934.
2020	Obata Y, Bale HA, Barnard HS, Parkinson DY, Alliston T, Acevedo C. Quantitative and qualitative bone imaging: a review of synchrotron radiation microtomography analysis in bone research. J Mech Behav Biomed Mater. October 2020;110:103887.
2020	Andronowski JM, Davis RA, Holyoke CW. A sectioning, coring, and image processing guide for high-throughput cortical bone sample procurement and analysis for synchrotron micro-CT. JOVE. June 2020;160:e61081.
2016	Georgiadis M, Müller R, Schneider P. Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils. J R Soc Interface. June 1, 2016;13(119):20160088.
2020	Binkley DM, Deering J, Yuan H, Gourrier A, Grandfield K. Ellipsoidal mesoscale mineralization pattern in human cortical bone revealed in 3D by plasma focused ion beam serial sectioning. J Struct Biol. November 1, 2020;212(2):107615.
2020	Krupski W, Kruk-Bachonko J, Tatara MR. Computed tomography diagnostic of uncommon case of osteopetrosis in 80-year-old man: case report. Medicina. October 2020;56(10):518.
2019	Nascimento EHL, Gâeta-Araujo H, Brasil DM, Madlum DV, Freitas DQ, Haiter-Neto F, Oliveira-Santos C. Impact of micro-computed tomography reconstruction protocols on bone microarchitecture analysis. Oral Surg Oral Med Oral Pathol Oral Radiol. October 2019;128(4):411-417.
2017	Paschalis EP, Gamsjaeger S, Klaushofer K. Vibrational spectroscopic techniques to assess bone quality. Osteoporos Int. August 2017;28(8):2275-2291.
2024	Tang T, Casagrande T, Mohammadpour P, Landis W, Lievers B, Grandfield K. Characterization of human trabecular bone across multiple length scales using a correlative approach combining X-ray tomography with LaserFIB and plasma FIB-SEM. Sci Rep. September 16, 2024;14:21604.
2019	Binkley DM. Electron and Ion Beam Imaging of Human Bone Structure Across the Nano- and Mesoscale [Master's thesis]. Hamilton, ON: McMaster University; June 2019.
2016	Chang N. Structural Deterioration of Human Articular Cartilage and Subchondral Plate [PhD thesis]. San Diego (UCSD), University of California; 2016.
2022	Schurman CA. The Role of TGFβ Mediated Osteocytic Perilacunar/canalicular Remodeling in Age-Related Bone Fragility [PhD thesis]. San Francisco, University of California; 2022.
2018	Pratt I. Interpreting the 3D Orientation of Vascular Canals in Cortical Bone in Birds and Bats [PhD thesis]. University of Saskatchewan; September 2018.