High resolution imaging in bone tissue research-review

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Akhter, M. P.¹; Recker, R. R.¹

High resolution imaging in bone tissue research-review

Bone. February 2021;143:115620

©2020 Elsevier Inc. All rights reserved.

Affiliations

¹Creighton University Osteoporosis Research Center, Omaha, NE, United States of America
Abstract and keywords

This review article focuses on imaging of bone tissue to understand skeletal health with regards to bone quality. Skeletal fragility fractures are due to bone diseases such as osteoporosis which result in low bone mass and bone mineral density (BMD) leading to high risk of fragility fractures. Recent advances in imaging and analysis technologies have highly benefitted the field of biological sciences. In particular, their application in skeletal health has been of significant importance in understanding bone mechanical behavior (structure and properties) at the tissue level. While synchrotron based microCT technique has remained the gold standard for non-destructive evaluation of structure in material and biological sciences, several lab based microCT systems have been developed to provide high resolution imaging of specimens with greater access, and ease of use in laboratory settings. Lab based microCT scanners are widely used in the bone field as a standard tool to evaluate three-dimensional (3D) morphologies of bone structure at image resolutions appropriate for bone samples from small animals to bone biopsy specimens from humans. Both synchrotron and standard lab based microCT systems provide high resolution imaging ex vivo for a small sized specimen. A few X-ray based systems are also commercially available for in vivo scanning at relatively low image resolutions. Synchrotron-based CT microscopy is being used for various ultra-high-resolution image analyses using complex 3D software. However, the synchrotron-based CT technology is in high demand, allows only limited numbers of specimens, expensive, requires complex additional instrumentation, and is not easily available to researchers as it requires access to a synchrotron source which is always limited. Therefore, desktop laboratory scanners (microXCT, Zeiss/Xradia, Scanco, SkyScan. etc.), mimicking the synchrotron based CT technology or image resolution, have been developed to solve the accessibility issues. These lab based scanners have helped both material science, and the bone field to investigate bone tissue morphologies at submicron mage resolutions. Considerable progress has been made in both in vivo and ex vivo imaging towards providing high resolution images of bone tissue. Both clinical and research imaging technologies will continue to improve and help understand osteoporosis and other related skeletal issues in order to develop targeted treatments for bone fragility. This review summarizes the high resolution imaging work in bone research.

Keywords: Micro-CT; Synchrotron; High resolution imaging; Bone tissue
Links

DOI: 10.1016/j.bone.2020.115620

PubMed: 32866682

WoS: 000604738600003
History

Received: 2020-05-19

Revised: 2020-08-24

Accepted: 2020-08-24

Online: 2020-08-29

Cited Works (39)

Year	Entry
1995	Riggs BL, Melton LJ III. The worldwide problem of osteoporosis: insights afforded by epidemiology. Bone. November 1995;17(5)(suppl 1):S505-S511.
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.
2007	MacNeil JA, Boyd SK. Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys. December 2007;29(10):1096-1105.
1996	Müller R, Hahn M, Vogel M, Delling G, Rüegsegger P. Morphometric analysis of noninvasively assessed bone biopsies: comparison of high-resolution computed tomography and histologic sections. Bone. March 1996;18(3):215-220.
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.
2013	Dallas SL, Prideaux M, Bonewald LF. The osteocyte: an endocrine cell … and more. Endocr Rev. October 2013;34(4):658-690.
2017	Núñez JA, Goring A, Hesse E, Thurner PJ, Schneider P, Clarkin CE. Simultaneous visualisation of calcified bone microstructure and intracortical vasculature using synchrotron X-ray phase contrast-enhanced tomography. Sci Rep. October 16, 2017;7:13289.
2003	Crawford RP, Rosenberg WS, Keaveny TM. Quantitative computed tomography-based finite element models of the human lumbar vertebral body: effect of element size on stiffness, damage, and fracture strength predictions. J Biomech Eng. August 2003;125(4):434-438.
2000	Turner CH, Hsieh Y, Müller R, Bouxsein ML, Baylink DJ, Rosen CJ, Grynpas MD, Donahue LR, Beamer WG. Genetic regulation of cortical and trabecular bone strength and microstructure in inbred strains of mice. J Bone Miner Res. June 2000;15(6):1126-1131.
2002	Borah B, Dufresne TE, Chmielewski PA, Gross GJ, Prenger MC, Phipps RJ. Risedronate preserves trabecular architecture and increases bone strength in vertebra of ovariectomized minipigs as measured by three‐dimensional microcomputed tomography. J Bone Miner Res. July 2002;17(7):1139-1147.
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.
1998	Müller R, Van Campenhout H, Van Damme B, Van der Perre G, Dequeker J, Hildebrand T, Rüegsegger P. Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and micro-computed tomography. Bone. July 1998;23(1):59-66.
2008	Kazakia GJ, Burghardt AJ, Cheung S, Majumdar S. Assessment of bone tissue mineralization by conventional x-ray microcomputed tomography: comparison with synchrotron radiation microcomputed tomography and ash measurements. Med Phys. 2008;35(7):3170-3179.
1997	Ulrich D, Hildebrand T, Van Rietbergen B, Müller R, Rüegsegger P. The quality of trabecular bone evaluated with micro-computed tomography, FEA and mechanical testing. Stud Health Technol Inform. 1997;40:97-112.
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.
2001	Laib A, Kumer JL, Majumdar S, Lane NE. The temporal changes of trabecular architecture in ovariectomized rats assessed by MicroCT. Osteoporos Int. November 2001;12(11):936-941.
2002	Cummings SR, Melton LJ III. Epidemiology and outcomes of osteoporotic fractures. Lancet. May 18, 2002;359(9319):1761-1767.
1988	Layton MW, Goldstein SA, Goulet RW, Feldkamp LA, Kubinski DJ, Bole GG. Examination of subchondral bone architecture in experimental osteoarthritis by microscopic computed axial tomography. Arthritis Rheum. November 1988;31(11):1400-1405.
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.
2010	Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. July 2010;25(7):1468-1486.
2002	Nuzzo S, Lafage‐Proust MH, Martin‐Badosa E, Boivin G, Thomas T, Alexandre C, Peyrin F. Synchrotron radiation microtomography allows the analysis of three‐dimensional microarchitecture and degree of mineralization of human iliac crest biopsy specimens: effects of etidronate treatment. J Bone Miner Res. August 2002;17(8):1372-1382.
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.
2004	Recker R, Lappe J, Davies KM, Heaney R. Bone remodeling increases substantially in the years after menopause and remains increased in older osteoporosis patients. J Bone Miner Res. October 2004;19(10):1628-1633.
1998	Ito M, Nakamura T, Matsumoto T, Tsurusaki K, Hayashi K. Analysis of trabecular microarchitecture of human iliac bone using microcomputed tomography in patients with hip arthrosis with or without vertebral fracture. Bone. August 1998;23(2):163-169.
2009	Voide R, Schneider P, Stauber M, Wyss P, Stampanoni M, Sennhauser U, van Lenthe GH, Müller R. Time-lapsed assessment of microcrack initiation and propagation in murine cortical bone at submicrometer resolution. Bone. August 2009;45(2):164-173.
2014	Dong P, Haupert S, Hesse B, Langer M, Gouttenoire P-J, Bousson V, Peyrin F. 3D osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-CT images. Bone. March 2014;60:172-185.
1989	Feldkamp LA, Goldstein SA, Parfitt MA, Jesion G, Kleerekoper M. The direct examination of three‐dimensional bone architecture in vitro by computed tomography. J Bone Miner Res. 1989;4(1):3-11.
2006	Lane NE, Yao W, Balooch M, Nalla RK, Balooch G, Habelitz S, Kinney JH, Bonewald LF. Glucocorticoid‐treated mice have localized changes in trabecular bone material properties and osteocyte lacunar size that are not observed in placebo‐treated or estrogen‐deficient mice. J Bone Miner Res. March 2006;21(3):466-476.
2012	Qing H, Ardeshirpour L, Pajevic PD, Dusevich V, Jähn K, Kato S, Wysolmerski J, Bonewald LF. Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J Bone Miner Res. May 2012;27(5):1018-1029.
2019	Comini F, Palanca M, Cristofolini L, Dall’Ara E. Uncertainties of synchrotron microCT-based digital volume correlation bone strain measurements under simulated deformation. J Biomech. March 27, 2019;86:232-237.
2011	Larrue A, Rattner A, Peter Z-A, Olivier C, Laroche N, Vico L, Peyrin F. Synchrotron radiation micro-CT at the micrometer scale for the analysis of the three-dimensional morphology of microcracks in human trabecular bone. PLoS One. 2011;6(7):e21297.
2009	Morgan EF, Mason ZD, Chien KB, Pfeiffer AJ, Barnes GL, Einhorn TA, Gerstenfeld LC. Micro-computed tomography assessment of fracture healing: relationships among callus structure, composition, and mechanical function. Bone. February 2009;44(2):335-344.
2000	Akhter MP, Iwaniec UT, Covey MA, Cullen DM, Kimmel DB, Recker RR. Genetic variations in bone density, histomorphometry, and strength in mice. Calcif Tiss Int. October 2000;67(4):337-344.
2007	Akhter MP, Lappe JM, Davies KM, Recker RR. Transmenopausal changes in the trabecular bone structure. Bone. July 2007;41(1):111-116.
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.
2011	Bonewald LF. The amazing osteocyte. J Bone Miner Res. 2011;26(2):229-238.
2007	Burge R, Dawson‐Hughes B, Solomon DH, Wong JB, King A, Tosteson A. Incidence and economic burden of osteoporosis‐related fractures in the United States, 2005–2025. J Bone Miner Res. March 2007;22(3):465-475.
2005	Bouxsein ML, Myers KS, Shultz KL, Donahue LR, Rosen CJ, Beamer WG. Ovariectomy‐induced bone loss varies among inbred strains of mice. J Bone Miner Res. July 2005;20(7):1085-1092.

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Year	Entry
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