Regional variations of vertebral trabecular bone microstructure with age and gender

wbldb

Chen, H.¹; Shoumura, S.²; Emura, S.³; Bunai, Y.⁴

Regional variations of vertebral trabecular bone microstructure with age and gender

Osteoporos Int. October 2008;19(10):1473-1483

Affiliations

¹Department of Anatomy, Gifu University Graduate School of Medicine, 1-1 Yanagido, Gifu 501-1194, Japan

²Department of Physical Therapy, Chubu Gakuin University School of Rehabilitation, Gifu 501-3993, Japan

³Nursing Course, Gifu University School of Medicine, Gifu 501-1194, Japan

⁴Department of Legal Medicine, Gifu University Graduate School of Medicine, 1–1 Yanagido, Gifu 501-1194, Japan
Abstract and keywords

The vertebral trabecular bone has a complex three-dimensional (3D) microstructure, with inhomogeneous morphology. A thorough understanding of regional variations in the microstructural properties is crucial for evaluating age- and gender-related bone loss of the vertebra, and may help us to gain more insight into the mechanism of the occurrence of vertebral osteoporosis and the related fracture risks.

Introduction: The aim of this study was to identify regional differences in 3D microstructure of vertebral trabecular bone with age and gender, using micro-computed tomography (micro-CT) and scanning electron microscopy (SEM).

Methods: We used 56 fourth lumbar vertebral bodies from 28 women and men (57-98 years of age) cadaver donors. The subjects were chosen to give an even age and gender distribution. Both women and men were divided into three age groups, 62-, 77- and 92-year-old groups. Five cubic specimens were prepared from anterosuperior, anteroinferior, central, posterosuperior and posteroinferior regions at sagittal section. Bone specimens were examined by using micro-CT and SEM.

Results: Reduced bone volume (BV/TV), trabecular number (Tb.N) and connectivity density (Conn.D), and increased structure model index (SMI) were found between ages 62 and 77 years, and between ages 77 and 92 years. As compared with women, men had higher Tb.N in the 77-year-old group and higher Conn.D in the 62- and 77-year-old groups. The central and anterosuperior regions had lower BV/TV and Conn.D than their corresponding posteroinferior region. Increased resorbing surfaces, perforated or disconnected trabeculae and microcallus formations were found with age.

Conclusion: Vertebral trabeculae are microstructurally heterogeneous. Decreases in BV/TV and Conn.D with age are similar in women and men. Significant differences between women and men are observed at some microstructural parameters. Age-related vertebral trabecular bone loss may be caused by increased activity of resorption. These findings illustrate potential mechanisms underlying vertebral fractures.

Keywords: Aging; Micro-CT; Microstructural properties; Regional variation; Scanning electron microscopy; Vertebral body
Links

DOI: 10.1007/s00198-008-0593-3

PubMed: 18330606

WoS: 000259820100011
History

Received: 2007-09-05

Accepted: 2008-02-05

Online: 2008-03-11

Cited Works (38)

Year	Entry
2006	Khosla S, Riggs BL, Atkinson EJ, Oberg AL, McDaniel LJ, Holets M, .Peterson JM, Melton LJ III. Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res. January 2006;21(1):124-131.
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.
1998	Silva MJ, Keaveny TM, Hayes WC. Computed tomography-based finite element analysis predicts failure loads and fracture patterns for vertebral sections. J Orthop Res. May 1998;16(3):300-308.
2002	Thomsen JS, Ebbesen EN, Mosekilde L. Predicting human vertebral bone strength by vertebral static histomorphometry. Bone. March 2002;30(3):502-508.
1987	Lorensen WE, Cline HE. Marching cubes: a high resolution 3D surface construction algorithm. Comput Graph. 1987;21(4):163-169.
1988	Bergot C, Laval-Jeantet A-M, Prêteux F, Meunier A. Measurement of anisotropic vertebral trabecular bone loss during aging by quantitative image analysis. Calcif Tiss Int. September 1988;43(3):143-149.
2006	Adams MA, Pollintine P, Tobias JH, Wakley GK, Dolan P. Intervertebral disc degeneration can predispose to anterior vertebral fractures in the thoracolumbar spine. J Bone Miner Res. September 2006;21(9):1409-1416.
2006	Sigurdsson G, Aspelund T, Chang M, Jonsdottir B, Sigurdsson S, Eiriksdottir G, Gudmundsson A, Harris TB, Gudnason V, Lang TF. Increasing sex difference in bone strength in old age: the age, gene/environment susceptibility-Reykjavik study (AGES-REYKJAVIK). Bone. September 2006;39(3):644-651.
1997	Hildebrand T, Rüegsegger P. Quantification of bone microarchitecture with the structure model index. Comput Methods Prog Biomed. 1997;1(1):15-23.
2007	Eckstein F, Matsuura M, Kuhn V, Priemel M, Müller R, Link TM, Lochmüller E. Sex differences of human trabecular bone microstructure in aging are site‐dependent. J Bone Miner Res. June 2007;22(6):817-824.
2007	McDonnell P, McHugh PE, O’Mahoney D. Vertebral osteoporosis and trabecular bone quality. Ann Biomed Eng. February 2007;35(2):170-189.
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.
1998	Ebbesen EN, Thomsen JS, Beck-Nielsen H, Nepper-Rasmussen HJ, Mosekilde L. Vertebral bone density evaluated by dual-energy X-ray absorptiometry and quantitative computed tomography in vitro. Bone. September 1998;23(3):283-290.
1995	Hahn M, Vogel M, Amling M, Ritzel H, Delling G. Microcallus formations of the cancellous bone: a quantitative analysis of the human spine. J Bone Miner Res. September 1995;10(9):1410-1416.
2002	Ding M, Odgaard A, Linde F, Hvid I. Age-related variations in the microstructure of human tibial cancellous bone. J Orthop Res. May 2002;20(3):615-621.
2007	Hulme PA, Boyd SK, Ferguson SJ. Regional variation in vertebral bone morphology and its contribution to vertebral fracture strength. Bone. December 2007;41(6):946-957.
1995	Grote HJ, Amling M, Vogel M, Hahn M, Pösl M, Delling G. Intervertebral variation in trabecular microarchitecture throughout the normal spine in relation to age. Bone. March 1995;16(3):301-308.
1988	Hui SL, Slemenda CW, Johnston CC Jr. Age and bone mass as predictors of fracture in a prospective study. J Clin Invest. June 1988;81(6):1804-1809.
2005	Gong H, Zhang M, Yeung HY, Qin L. Regional variations in microstructural properties of vertebral trabeculae with aging. J Bone Min Metab. March 2005;23(2):174-180.
2001	Banse X, Devogelaer JP, Munting E, Delloye C, Cornu O, Grynpas M. Inhomogeneity of human vertebral cancellous bone: systematic density and structure patterns inside the vertebral body. Bone. 2001;28(5):563-571.
1984	Harrigan TP, Mann RW. Characterization of microstructural anisotropy in orthotropic materials using a second rank tensor. J Mater Sci. March 1984;19(3):761-767.
2006	Gong H, Zhang M, Qin L, Lee KKH, Guo X, Shi S-Q. Regional variations in microstructural properties of vertebral trabeculae with structural groups. Spine. January 2006;31(1):24-32.
2001	Grant JP, Oxland TR, Dvorak MF. Mapping the structural properties of the lumbosacral vertebral endplates. Spine. April 15, 2001;26(8):889-896.
2000	Ding M. Age variations in the properties of human tibial trabecular bone and cartilage. Acta Orthop Scand. 2000;71(suppl 292):1-45.
1984	Parfitt AM. Age-related structural changes in trabecular and cortical bone: cellular mechanisms and biomechanical consequences. Calcif Tiss Int. 1984;36(suppl 1):S123-S128.
2000	Legrand E, Chappard D, Pascaretti C, Duquenne M, Krebs S, Rohmer V, Basle M, Audran M. Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J Bone Miner Res. January 2000;15(1):13-19.
1988	Mosekilde L. Age-related changes in vertebral trabecular bone architecture—assessed by a new method. Bone. 1988;9(4):247-250.
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.
2006	Stauber M, Müller R. Age-related changes in trabecular bone microstructures: global and local morphometry. Osteoporos Int. April 2006;17(4):616-626.
1993	Mosekilde L. Vertebral structure and strength in vivo and in vitro. Calcif Tiss Int. February 1993;53(suppl 1):S121-S126.
1987	Weinstein RS, Hutson MS. Decreased trabecular width and increased trabecular spacing contribute to bone loss with aging. Bone. 1987;8(3):137-142.
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.
1997	Odgaard A. Three-dimensional methods for quantification of cancellous bone architecture. Bone. 1997;20(4):315-328.
1997	Burr DB, Forwood MR, Fyhrie DP, Martin RB, Schaffler MB, Turner CH. Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res. January 1997;12(1):6-15.
2005	Riggs BL, Parfitt AM. Drugs used to treat osteoporosis: the critical need for a uniform nomenclature based on their action on bone remodeling. J Bone Miner Res. February 2005;20(2):177-184.
1997	McCalden RW, McGeough JA, Court-Brown CM. Age-related changes in the compressive strength of cancellous bone: the relative importance of changes in density and trabecular architecture. J Bone Joint Surg. March 1997;79A(3):421-427.
2002	Thomsen JS, Ebbesen EN, Mosekilde L. Age-related differences between thinning of horizontal and vertical trabeculae in human lumbar bone as assessed by a new computerized method. Bone. July 2002;31(1):136-142.
2006	Bouxsein ML, Melton LJ III, Riggs BL, Muller J, Atkinson EJ, Oberg AL, Robb RA, Camp JJ, Rouleau PA, McCollough CH, Khosla S. Age‐ and sex‐specific differences in the factor of risk for vertebral fracture: a population‐based study using QCT. J Bone Miner Res. September 2006;21(9):1475-1482.

Cited By (21)

Year	Entry
2019	Zenzes M, Bortel EL, Fratzl P, Mundlos S, Schuetz M, Schmidt H, Duda GN, Witte F, Zaslansky P. Normal trabecular vertebral bone is formed via rapid transformation of mineralized spicules: a high-resolution 3D ex-vivo murine study. Acta Biomater. March 1, 2019;86:429-440.
2021	Schröder G, Jabke B, Schulze M, Wree A, Martin H, Sahmel O, Doerell A, Kullen CM, Andresen R, Schober H-C. A comparison, using X-ray micro-computed tomography, of the architecture of cancellous bone from the cervical, thoracic and lumbar spine using 240 vertebral bodies from 10 body donors. Anat Cell Biol. March 31, 2021;54(1):25-34.
2010	Viguet-Carrin S, Follet H, Gineyts E, Roux JP, Munoz F, Chapurlat R, Delmas PD, Bouxsein ML. Association between collagen cross-links and trabecular microarchitecture properties of human vertebral bone. Bone. February 2010;46(2):342-347.
2019	vom Scheidt A, Hemmatian H, Püschel K, Krause M, Amling M, Busse B. Bisphosphonate treatment changes regional distribution of trabecular microstructure in human lumbar vertebrae. Bone. October 2019;127:482-487.
2020	McKay M, Jackman TM, Hussein AI, Guermazi A, Liu J, Morgan EF. Association of vertebral endplate microstructure with bone strength in men and women. Bone. February 2020;131:115147.
2022	Lamarche BA, Thomsen JS, Andreasen CM, Lievers WB, Andersen TL. 2D size of trabecular bone structure units (BSU) correlate more strongly with 3D architectural parameters than age in human vertebrae. Bone. July 2022;160:116399.
2016	Fan R, Gong H, Zhang X, Liu J, Jia Z, Zhu D. Modeling the mechanical consequences of age-related trabecular bone loss by XFEM simulation. Computat Math Methods Med. 2016;2016:3495152.
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.
2009	Mc Donnell P, Harrison N, Liebschner MAK, Mc Hugh PE. Simulation of vertebral trabecular bone loss using voxel finite element analysis. J Biomech. 2009;42(16):2789-2796.
2010	Poukalova M, Yakacki CM, Guldberg RE, Lin A, Saing M, Gillogly SD, Gall K. Pullout strength of suture anchors: effect of mechanical properties of trabecular bone. J Biomech. April 19, 2010;43(6):1660-1665.
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.
2015	Thomsen JS, Jensen MV, Niklassen AS, Ebbesen EN, Brüel A. Age-related changes in vertebral and iliac crest 3D bone microstructure: differences and similarities. Osteoporos Int. January 2015;26(1):219-228.
2020	Aguirre TG. Bio-Inspired Design for Engineering Applications: Empirical and Finite Element Studies of Biomechanically Adapted Porous Bone Architectures [PhD thesis]. Colorado State University; Summer 2020.
2020	Lamarche BA. Morphometric Changes With Age in Human Trabecular Bone Structural Units (BSU) of the Lumbar Spine [Master's thesis]. Sudbury, ON: Laurentian University; 2020.
2022	Rahovich P. Effects of Bone Structural Unit (BSU) Geometry and Material Properties on Crack Growth Through Idealized Trabecular Microstructures [Master's thesis]. Sudbury, ON: Laurentian University; 2022.
2014	Holub O. Biomechanics of Spinal Metastases [PhD thesis]. University of Leeds; April 2014.
2011	Wagnac É. Expérimentation et modélisation détaillée de la colonne vertébrale pour étudier le rôle de facteurs anatomiques et biomécaniques sur les traumatismes rachidiens [PhD thesis]. École polytechnique de Montréal; November 2011.
2015	Bianco R. Biomécanique de l'ancrage de vis pédiculaires pour l'instrumentation du rachis [PhD thesis]. École polytechnique de Montréal; December 2015.
2011	Ahmed F. Multiscale Quantitative Imaging of Human Femoral Heads Using X-Ray Microtomography [PhD thesis]. Queen Mary University of London; 2011.
2010	Rodriguez AG. Human Endplate Permeability and Microstructure and Their Relationship to Disc Degeneration [PhD thesis]. San Francisco, University of California; 2010.
2024	Benais R. Computational Modeling of Trabecular Bone Indentation and Development of a New Test Method to Perform Unconstrained Load-Induced Subsidence of an Intervertebral Body Fusion Device [Master's thesis]. University of Waterloo; 2024.