Cortical bone in the human femoral neck: three‐dimensional appearance and porosity using synchrotron radiation

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Bousson, Valérie^1,2; Peyrin, Françoise³; Bergot, Catherine¹; Hausard, Marc³; Sautet, Alain⁴; Laredo, Jean‐Denis^1,2

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 American Society for Bone and Mineral Research

Affiliations

¹Laboratoire de Radiologie Expérimentale, Faculté de Médecine Lariboisière‐Saint Louis, Paris, France

²Service de Radiologie Ostéoarticulaire‐Assistance Publique‐Hôpitaux de Paris, Hôpital Lariboisière, Paris, France

³CREATIS, ESRF, Grenoble Cedex, France

⁴Service de Chirurgie Orthopédique, Hôpital Saint‐Antoine, Paris, France
Abstract and keywords

A high‐resolution CT system using synchrotron radiation allowed visualization of the 3D cortical bone microarchitecture and measurement of intracortical porosity of femoral neck cortical bone specimens from 19 female cadavers imaged at 10.13‐μm resolution. 3D reconstruction of specimens showed osteonal system arrangement. Mean porosity was 15.88%. This technique will provide insights into the mechanisms involved in osteoporotic hip fractures.

Introduction: The purpose of this study was to show that a high‐resolution CT system using synchrotron radiation (SR) allows visualization of the 3D cortical bone microarchitecture of the human femoral neck and quantification of intracortical porosity.

Materials and Methods: Bone specimens from the inferior femoral neck were obtained from 19 female cadavers with no hip fracture (mean, 86.9 ± 8.3 years). The specimens, consisting of embedded ∼7 × 7 × 12‐mm cortical bone parallelepipeds, were imaged using SR at 10.13‐μm resolution. Commercial software was used to visualize both the 660 × 660 × 660‐voxel volumes and the 2D axial slices through each volume. Qualitative examination of 2D axial slices focused on the appearance of the vessel canal system, presence of small bright zones (fully mineralized tissue) in the osseous matrix, and presence of cracks. A method was developed to automatically measure 3D intracortical porosity after separating pure bone from pores and cortical bone from trabecular bone.

Results and Conclusions: 3D reconstruction of the specimens showed the entire structure and arrangement of the osteonal systems, parallel to the axis of the femoral neck. Bright zones were seen in the outer cortex. No cracks were observed. Porosity values varied widely from 4.96% to 38.87% (mean, 15.88 ± 9.87%). This study establishes that SR microtomography can be used to display the 3D bone microstructure of the human femoral neck cortex and to quantify intracortical porosity. This technique will provide insights into the mechanisms involved in cortical bone loss and osteoporotic hip fractures.

Keywords: 3D microtomography; synchrotron radiation; femoral neck; cortical bone; bone microarchitecture
Links

DOI: 10.1359/jbmr.040124

PubMed: 15068503

WoS: 000220962100014
History

Received: 2003-02-7

Revised: 2003-10-14

Accepted: 2004-01-16

Online: 2004-01-19

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.
2001	Bousson V, Meunier A, Bergot C, Vicaut É, Rocha MA, Morais MH, Laval‐Jeantet A, Laredo J. Distribution of intracortical porosity in human midfemoral cortex by age and gender. J Bone Miner Res. July 2001;16(7):1308-1317.
2001	Wachter NJ, Augat P, Krischak GD, Mentzel M, Kinzl L, Claes L. Prediction of cortical bone porosity in vitro by microcomputed tomography. Calcif Tiss Int. January 2001;68(1):38-42.
1999	Laib A, Rüegsegger P. Calibration of trabecular bone structure measurements of in vivo three-dimensional peripheral quantitative computed tomography with 28-μm-resolution microcomputed tomography. Bone. January 1999;24(1):35-39.
1999	Stein MS, Feik SA, Thomas CDL, Clement JG, Wark JD. An automated analysis of intracortical porosity in human femoral bone across age. J Bone Miner Res. April 1999;14(4):624-632.
1977	Tappen NC. Three‐dimensional studies of resorption spaces and developing osteons. Am J Anat. July 1977;149(3):301-331.
2001	Bell KL, Loveridge N, Reeve J, Thomas CDL, Feik SA, Clement JG. Super‐osteons (remodeling clusters) in the cortex of the femoral shaft: influence of age and gender. Anat Rec. December 1, 2001;264(4):378-386.
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.
1993	Squillante RG, Williams JL. Videodensitometry of osteons in females with femoral neck fractures. Calcif Tiss Int. April 1993;52(4):273-277.
1999	Bell KL, Loveridge N, Power J, Garrahan N, Meggitt BF, Reeve J. Regional differences in cortical porosity in the fractured femoral neck. Bone. January 1999;24(1):57-64.
1990	Mazess RB. Fracture risk: a role for compact bone. Calcif Tiss Int. October 1990;47(4):191-193.
1969	Currey JD. The mechanical consequences of variation in the mineral content of bone. J Biomech. March 1969;2(1):1-11.
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.
1993	Boyce TM, Bloebaum RD. Cortical aging differences and fracture implications for the human femoral neck. Bone. September–October 1993;14(5):769-778.
1996	Petrtýl M, Heřt J, Fiala P. Spatial organization of the haversian bone in man. J Biomech. February 1996;29(2):161-169.
1980	Martin RB, Pickett JC, Zinaich S. Studies of skeletal remodeling in aging men. Clin Orthop Relat Res. June 1980;149:268-282.
1994	Bonse U, Busch F, Günnewig O, Beckmann F, Pahl R, Delling G, Hahn M, Graeff W. 3D computed X-ray tomography of human cancellous bone at 8 μm spatial and 10⁻⁴ energy resolution. Bone Miner. April 1994;25(1):25-38.
1996	Hangartner TN, Gilsanz V. Evaluation of cortical bone by computed tomography. J Bone Miner Res. October 1996;11(10):1518-1525.
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.
2000	Yeni YN, Norman TL. Fracture toughness of human femoral neck: effect of microstructure, composition, and age. Bone. May 2000;26(5):499-504.
1995	Lotz JC, Cheal EJ, Hayes WC. Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporos Int. July 1995;5(3):252-261.
1997	Hildebrand T, Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc (Oxford). 1997;185(1):67-75.
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.
1999	Bell KL, Loveridge N, Power J, Garrahan N, Stanton M, Lunt M, Meggitt BF, Reeve J. Structure of the femoral neck in hip fracture: cortical bone loss in the inferoanterior to superoposterior axis. J Bone Miner Res. January 1999;14(1):111-119.
1958	Cohen J, Harris WH. The three-dimensional anatomy of Haversian systems. J Bone Joint Surg. April 1958;40A(2):419-434.
1994	Odgaard A, Andersen K, Ullerup R, Frich LH, Melsen F. Three-dimensional reconstruction of entire vertebral bodies. Bone. May–June 1994;15(3):335-342.
1990	Kuhn JL, Goldstein SA, Feldkamp LA, Goulet RW, Jesion G. Evaluation of a microcomputed tomography system to study trabecular bone structure. J Orthop Res. 1990;8(6):833-842.
2000	Jordan GR, Loveridge N, Bell KL, Power J, Rushton N, Reeve J. Spatial clustering of remodeling osteons in the femoral neck cortex: a cause of weakness in hip fracture? Bone. March 2000;26(3):305-313.
1993	McCalden RW, McGeough JA, Barker MB, Court-Brown CM. Age-related changes in the tensile properties of cortical bone: the relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg. 1993;75A(8):1193-1205.
1960	Jowsey J. Age changes in human bone. Clin Orthop. 1960;17:210-218.
1992	Barth RW, Williams JL, Kaplan FS. Osteon morphometry in females with femoral neck fractures. Clin Orthop Relat Res. October 1992;283:178-186.
2001	Crabtree N, Loveridge N, Parker M, Rushton N, Power J, Bell KL, Beck TJ, Reeve J. Intracapsular hip fracture and the region-specific loss of cortical bone: analysis by peripheral quantitative computed tomography. J Bone Miner Res. July 2001;16(7):1318-1328.

Cited By (25)

Year	Entry
2007	Cooper DML, Thomas CDL, Clement JG, Turinsky AL, Sensen CW, Hallgrímsson B. Age-dependent change in the 3D structure of cortical porosity at the human femoral midshaft. Bone. April 2007;40(5):957-965.
2011	Voide R, Schneider P, Stauber M, van Lenthe GH, Stampanoni M, Müller R. The importance of murine cortical bone microstructure for microcrack initiation and propagation. Bone. December 2011;49(6):1186-1193.
2021	Akhter MP, Recker RR. High resolution imaging in bone tissue research-review. Bone. February 2021;143:115620.
2011	Burghardt AJ, Link TM, Majumdar S. High-resolution computed tomography for clinical imaging of bone microarchitecture. Clin Orthop Relat Res. August 2011;469:2179-2193.
2014	Peyrin F, Dong P, Pacureanu A, Langer M. Micro- and nano-CT for the study of bone ultrastructure. Curr Osteoporos Rep. December 2014;12(4):465-474.
2013	Chen H, Zhou X, Fujita H, Onozuka M, Kubo K-Y. Age-related changes in trabecular and cortical bone microstructure. Int J Endocrinol. March 18, 2013;2013:213234.
2020	Zhou J, Cui Z, Sevostianov I. Effect of saturation on the elastic properties and anisotropy of cortical bone. Int J Eng Sci. October 2020;155:103362.
2011	Grimal Q, Rus G, Parnell WJ, Laugier P. A two-parameter model of the effective elastic tensor for cortical bone. J Biomech. May 17, 2011;44(8):1621-1625.
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	Skedros JG, Baucomb SL. Mathematical analysis of trabecular “trajectories” in apparent trajectorial structures: the unfortunate historical emphasis on the human proximal femur. J Theo Biol. January 7, 2007;244(1):15-45.
2010	Chen H, Zhou X, Shoumura S, Emura S, Bunai Y. Age- and gender-dependent changes in three-dimensional microstructure of cortical and trabecular bone at the human femoral neck. Osteoporos Int. April 2010;21(4):627-636.
2013	Cesar R, Boffa RS, Fachine LT, Leivas TP, Silva AMH, Pereira CAM, Reiff RBM, Rollo JMDA. Evaluation of trabecular microarchitecture of normal osteoporotic and osteopenic human vertebrae. Procedia Eng. 2013;59:6-15.
2008	Techawiboonwong A, Song HK, Leonard MB, Wehrli FW. Cortical bone water: in vivo quantification with ultrashort echo-time MR imaging. Radiology. September 2008;248(3):824-833.
2007	Schneider P. Ultrastructural Phenotyping of Murine Bone Using Synchrotron Micro- and Nano-Computed Tomography [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2007.
2007	Voide R. Functional Phenotyping of Bone: A Hierarchical Assessment of Bone Failure Characteristics [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2007.
2016	Currier EJ. Predicting Peak Load of the Femoral Neck Using Structural Parameters [Master's thesis]. University of Illinois at Urbana-Champaign; 2016.
2017	Bakalova LP. Relating Cortical Bone Mechanics to Intracortical Pore Morphology, Distribution and Remodeling History Within the Fibula Diaphysis [Master's thesis]. University of Illinois at Urbana-Champaign; 2017.
2012	Pacureanu AJ. Imaging the Bone Cell Network With Nanoscale Synchrotron Computed Tomography [PhD thesis]. Institut national des sciences appliquées de Lyon (INSA Lyon); 2012.
2010	Deuerling JM. Effects of Ultrastructural Organization on the Mechanical Properties and Anisotropy of Human Cortical Bone [PhD thesis]. University of Notre Dame; December 2010.
2014	Colombo A. La micro-architecture de l’os trabéculaire en croissance: Variabilité tridimensionnelle normale et pathologique analysée par microtomodensitométrie [PhD thesis]. Université de Bordeaux; December 15, 2014.
2005	Cooper DML. 3D Micro-CT Imaging of Human Cortical Bone Porosity: A Novel Method for Estimating Age At Death [PhD thesis]. Calgary, AB: University of Calgary; December 2005.
2019	Surowiec R. Novel Models to Image and Quantify Bone Drug Efficacy and Disease Progression in Vivo: Addressing the Fragility Phenotype [PhD thesis]. University of Michigan; 2019.
2012	Hennig C. Determinants of Osteon Geometric Parameters and Their Relation With Age in Cortical Bone [Master's thesis]. University of Saskatchewan; December 2012.
2021	Harrison KD. A Novel in Vivo Synchrotron Radiation Micro-CT Imaging Platform for the Direct Tracking of Remodeling Events in Cortical Bone [PhD thesis]. University of Saskatchewan; December 2021.
2022	Sales EdS. The Spatio-Temporal Behavior of Basic Multicellular Units in a PTH-Induced Cortical Bone Remodeling Rabbit Model [Master's thesis]. University of Saskatchewan; August 2022.