Synchrotron radiation microtomography allows the analysis of three‐dimensional microarchitecture and degree of mineralization of human iliac crest biopsy specimens: effects of etidronate treatment

wbldb

Nuzzo, S.^1,2; Lafage‐Proust, M. H.³; Martin‐Badosa, E.^1,4; Boivin, G.⁵; Thomas, T.³; Alexandre, C.³; Peyrin, F.^1,2

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

©2002 American Society for Bone and Mineral Research

Affiliations

¹ESRF, BP 220, Grenoble Cedex, France

²CREATIS, Bat Blaise Pascal, INSA, Villeurbanne Cedex, France

³INSERM E9901, St. Etienne Cedex 2, France

⁴Laboratori d’“ptica, Departament de Física Aplicada i ”ptica, Universitat de Barcelona, Barcelona, Spain

⁵INSERM U403, Lyon Cedex 08, France
Abstract and keywords

Quantitative microcomputed tomography using synchrotron radiation (SR μCT) was used to assess the effects of a sequential etidronate therapy on both three‐dimensional (3D) microarchitecture and degree of mineralization of bone (DMB) in postmenopausal osteoporosis. Thirty‐two iliac crest biopsy specimens were taken from 14 patients with osteoporosis (aged 64 ± 1.8 years) before (baseline) and after 1 year of etidronate treatment, and after 2 years of treatment for four of the patients. The samples were imaged at high spatial resolution (voxel size = 10 μm) using the microtomography system developed at the European Synchrotron Radiation Facility (ESRF), Grenoble, France. Three‐dimensional microarchitecture parameters were calculated and compared with those obtained from conventional histomorphometry. In addition, the DMB was evaluated also in 3D. No significant statistical changes regarding bone mass and structural parameters were observed in histomorphometry or 3D analyses. The distribution of the DMB in cortical and trabecular bone showed a trend to a shift toward highest mineralization values after 1 year of etidronate treatment (3.88% and 1.24% in cortical and trabecular bone, respectively). This trend was more evident after 2 years. The study also showed that SR μCT is an accurate technique and the only one for quantifying both the mineralization and the microarchitecture of bone samples at the same time in 3D.

Keywords: bone architecture; degree of mineralization of bone; osteoporosis; quantitative microtomogra-phy; etidronate
Links

DOI: 10.1359/jbmr.2002.17.8.1372

PubMed: 12162491

WoS: 000177048900005

Cited Works (32)

Year	Entry
1998	Thomsen JS, Ebbesen EN, Mosekilde L. Relationships between static histomorphometry and bone strength measurements in human iliac crest bone biopsies author links open overlay panel. Bone. February 1998;22(2):153-163.
1992	Parfitt AM. Implications of architecture for the pathogenesis and prevention of vertebral fracture. Bone. 1992;13(suppl 2):S41-S47.
2000	Boivin GY, Chavassieux PM, Santora AC, Yates J, Meunier PJ. Alendronate increases bone strength by increasing the mean degree of mineralization of bone tissue in osteoporotic women. Bone. November 2000;27(5):687-694.
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.
2000	Kinney JH, Haupt DL, Balooch M, Ladd AJC, Ryaby JT, Lane NE. Three‐dimensional morphometry of the L6 vertebra in the ovariectomized rat model of osteoporosis: biomechanical implications. J Bone Miner Res. October 2000;15(10):1981-1991.
1997	Odgaard A. Three-dimensional methods for quantification of cancellous bone architecture. Bone. 1997;20(4):315-328.
1985	Kleerekoper M, Villanueva AR, Stanciu J, Rao DS, Parfitt AM. The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif Tiss Int. 1985;37(6):594-597.
1994	Goulet RW, Goldstein SA, Ciarelli MJ, Kuhn JL, Brown MB, Feldkamp LA. The relationship between the structural and orthogonal compressive properties of trabecular bone. J Biomech. April 1994;27(4):375-389.
1997	Chavassieux PM, Arlot ME, Reda C, Wei L, Yates AJ, Meunier PJ. Histomorphometric assessment of the long-term effects of alendronate on bone quality and remodeling in patients with osteoporosis. J Clin Invest. September 15, 1997;100(6):1475-1480.
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.
1987	Mosekilde L, Mosekilde L, Danielsen CC. Biomechanical competence of vertebral trabecular bone in relation to ash density and age in normal individuals. Bone. 1987;8(2):79-85.
1999	Ulrich D, van Rietbergen B, Laib A, Rüegsegger P. The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone. 1999;25(1):55-60.
1994	Müller R, Hildebrand T, Rüegsegger P. Non-invasive bone biopsy: a new method to analyse and display the three-dimensional structure of trabecular bone. Phys Med Biol. January 1994;39(1):145-164.
1998	Wang XD, Masilamani NS, Mabrey JD, Alder ME, Agrawal CM. Changes in the fracture toughness of bone may not be reflected in its mineral density, porosity, and tensile properties. Bone. July 1998;23(1):67-72.
1998	Kinney JH, Ladd AJC. The relationship between three-dimensional connectivity and the elastic properties of trabecular bone. J Bone Miner Res. May 1998;13(5):839-845.
1997	Meunier PJ, Boivin G. Bone mineral density reflects bone mass but also the degree of mineralization of bone: therapeutic implications. Bone. November 1997;21(5):373-377.
1989	Melton LJ III, Kan SH, Frye MA, Wahner HW, O'Fallon WM, Riggs BL. Epidemiology of vertebral fractures in women. Am J Epidemiol. May 1989;129(5):1000-1011.
1983	Parfitt AM, Mathews CH, Villanueva AR, Kleerekoper M, Frame B, Rao DS. Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis: implications for the microanatomic and cellular mechanisms of bone loss. J Clin Invest. October 1983;72(4):1396-1409.
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.
1999	Harris ST, Watts NB, Genant HK, McKeever CD, Hangartner T, Keller M, Chesnut CH III, Brown J, Eriksen EF, Hoseyni MS, Axelrod DW, Miller PD; Vertebral Efficacy With Risedronate Therapy (VERT) Study Group. Effects of risedronate treatment on vertebral and nonvertebral fractures in women with postmenopausal osteoporosis: a randomized controlled trial. JAMA. October 13, 1999;282(14):1344-1352.
1987	Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: standardization of nomenclature, symbols, and units: report of the ASBMR histomorphometry nomenclature committee. J Bone Miner Res. December 1987;2(6):595-610.
1987	Goldstein SA. The mechanical properties of trabecular bone: dependence on anatomic location and function. J Biomech. 1987;20(11-12):1055-1061.
1990	Watts NB, Harris ST, Genant HK, Wasnich RD, Miller PD, Jackson RD, Licata AA, Ross P, Woodson GC III, Yanover MJ, Mysiw WJ, Kohse L, Rao MB, Steiger P, Richmond B, Chesnut CH III. Intermittent cyclical etidronate treatment of postmenopausal osteoporosis. NEJM. July 12, 1990;323(2):73-79.
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.
1996	Black DM, Cummings SR, Karpf DB, Cauley JA, Thompson DE, Nevitt MC, Bauer DC, Genant HK, Haskell WL, Marcus R, Ott SM, Torner JC, Quandt SA, Reiss TF, Ensrud KE. Randomised trial of effect of alendronate on risk of fracture in women with existing vertebral fractures. Lancet. December 7, 1996;348(9041):1535-1541.
1990	Storm T, Thamsborg G, Steiniche T, Genant HK, Sørensen OH. Effect of intermittent cyclical etidronate therapy on bone mass and fracture rate in women with postmenopausal osteoporosis. NEJM. May 3, 1990;322(18):1265-1271.
1999	Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res. July 1999;14(7):1167-1174.
1995	Majumdar S, Newitt D, Jergas M, Gies A, Chiu E, Osman D, Keltner J, Keyak J, Genant H. Evaluation of technical factors affecting the quantification of trabecular bone structure using magnetic resonance imaging. Bone. October 1995;17(4):417-430.
1993	Odgaard A, Gundersen HJG. Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone. March–April 1993;14(2):173-182.
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.
1997	Beck JD, Canfield BL, Haddock SM, Chen TJH, Kothari M, Keaveny TM. Three-dimensional imaging of trabecular bone using the computer numerically controlled milling technique. Bone. 1997;21(3):281-287.

Cited By (25)

Year	Entry
2003	Roschger P, Gupta HS, Berzlanovich A, Ittner G, Dempster DW, Fratzl P, Cosman F, Parisien M, Lindsay R, Nieves JW, Klaushofer K. Constant mineralization density distribution in cancellous human bone. Bone. March 2003;32(3):316-323.
2005	Borah B, Ritman EL, Dufresne TE, Jorgensen SM, Liu S, Sacha J, Phipps RJ, Turner RT. The effect of risedronate on bone mineralization as measured by micro-computed tomography with synchrotron radiation: correlation to histomorphometric indices of turnover. Bone. July 2005;37(1):1-9.
2007	Ruffoni D, Fratzl P, Roschger P, Klaushofer K, Weinkamer R. The bone mineralization density distribution as a fingerprint of the mineralization process. Bone. May 2007;40(5):1308-1319.
2008	Roschger P, Paschalis EP, Fratzl P, Klaushofer K. Bone mineralization density distribution in health and disease. Bone. March 2008;42(3):456-466.
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.
2021	Akhter MP, Recker RR. High resolution imaging in bone tissue research-review. Bone. February 2021;143:115620.
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	Lerebours C, Weinkamer R, Roschger A, Buenzli PR. Mineral density differences between femoral cortical bone and trabecular bone are not explained by turnover rate alone. Bone Rep. December 1, 2020;13:100731.
2003	Dufresne TE, Chmielewski PA, Manhart MD, Johnson TD, Borah B. Risedronate preserves bone architecture in early postmenopausal women in 1 year as measured by three-dimensional microcomputed tomography. Calcif Tiss Int. November 2003;73(5):423-432.
2008	Burghardt AJ, Kazakia GJ, Laib A, Majumdar S. Quantitative assessment of bone tissue mineralization with polychromatic micro-computed tomography. Calcif Tiss Int. 2008;83(2):129-138.
2021	Pimentel A, Ureña-Torres P, Bover J, Fernandez-Martín JL, Cohen-Solal M. Bone fragility fractures in CKD patients. Calcif Tiss Int. April 2021;108(4):539-550.
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.
2011	Renders GAP, Mulder L, van Ruijven LJ, Langenbach GEJ, van Eijden TMGJ. Mineral heterogeneity affects predictions of intratrabecular stress and strain. J Biomech. February 3, 2011;44(3):402-407.
2010	Donnelly E, Boskey AL, Baker SP, van der Meulen MCH. Effects of tissue age on bone tissue material compositionand nanomechanical properties in the rat cortex. J Biomed Mater Res. March 1, 2010;A92(3):1048-1056.
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.
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.
2011	Hartmann MA, Dunlop JWC, Bréchet YJM, Fratzl P, Weinkamer R. Trabecular bone remodelling simulated by a stochastic exchange of discrete bone packets from the surface. J Mech Behav Biomed Mater. August 2011;4(6):879-887.
2010	Nogueira LP, Braz D, Barroso RC, Oliveira LF, Pinheiro CJG, Dreossi D, Tromba G. 3D histomorphometric quantification of trabecular bones by computed microtomography using synchrotron radiation. Micron. 2010;41(8):990-996.
2007	Schneider P. Ultrastructural Phenotyping of Murine Bone Using Synchrotron Micro- and Nano-Computed Tomography [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2007.
2019	Groetsch A. Micro- and Nanomechanics of Mineralised Collagen Fibre Elasto-Plasticity [PhD thesis]. Ebinburgh, Scotland: Heriot-Watt University; November 2019.
2002	Follet H. Caractérisation Biomécanique Et Modélisation 3D Par Imagerie X Et IRM Haute Résolution De L’os Spongieux Humain: Evaluation Du Risque Fracturaire [PhD thesis]. Institut national des sciences appliquées de Lyon (INSA Lyon); 2002.
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.
2014	Jameson JR. Characterization of Bone Material Properties and Microstructure in Osteogenesis Imperfecta/brittle Bone Disease [PhD thesis]. Marquette University; December 2014.
2012	Brennan MA. Close to the Bone: Investigations Into Bone Tissue Mineralisation and Mechanobiology of Osteoporosis [PhD thesis]. University of Southampton; January 2012.
2007	Ruffoni D. Modeling of Material and Architectural Quality of Trabecular Bone [PhD thesis]. Liège, Belgique: Université de Liège; September 2007.