Age-related changes of vertical and horizontal lumbar vertebral trabecular 3D bone microstructure is different in women and men.

The study presents a 3D method for subdividing a trabecular network into horizontal and vertical oriented bone. This method was used to investigate the age related changes of the bone volume fraction and thickness of horizontal and vertical trabeculae in human lumbar vertebral bone estimated with unbiased 3D methods in women and men over a large age-range. The study comprised second lumbar vertebral body bone samples from 40 women (aged 21.7-96.4years, median 56.6years) and 39 men (aged 22.6-94.6years, median 55.6years). The bone samples were μCT scanned and the 3D microstructure was quantified. A voxel based algorithm inspecting the local neighborhood is presented and used to segment the trabecular network into horizontal and vertical oriented bone. For both women and men BV/TV decreased significantly with age, Tb.Th* was independent of age, while SMI increased significantly with age. Vertical (BV.vert/TV) and horizontal (BV.horz/TV) bone volume fraction decreased significantly with age for both sexes. BV.vert/TV decreased significantly faster with age for women than for men. Vertical (Tb.Th*.vert) and horizontal (Tb.Th*.horz) trabecular thickness were independent of age, while Tb.Th*.horz/Tb.Th*.vert decreased significantly with age for both sexes. Additionally, the 95th percentile of the trabecular thickness distribution increased significantly with age for vertical trabeculae in women, whereas it was independent of age in men. In conclusion, we have shown that vertical and horizontal oriented bone density decreases with age in both women and men, and that vertical oriented bone is lost more quickly in women than in men. Furthermore, vertical and horizontal trabecular thickness were independent of age, whereas the horizontal to vertical trabecular thickness ratio decreased significantly with age indicating a relatively more pronounced thinning of horizontal trabeculae. Finally, the age-related loss of trabecular elements appeared to result in a compensatory hypertrophy of vertical trabeculae in women, but not in men.

[1]  M. Kleerekoper,et al.  The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures , 1985, Calcified Tissue International.

[2]  R. Müller,et al.  Vertebral body bone strength: the contribution of individual trabecular element morphology , 2012, Osteoporosis International.

[3]  L. Mosekilde,et al.  Sex differences in age-related loss of vertebral trabecular bone mass and structure--biomechanical consequences. , 1989, Bone.

[4]  E. F. Morgan,et al.  The effect of intravertebral heterogeneity in microstructure on vertebral strength and failure patterns , 2013, Osteoporosis International.

[5]  H. Beck-Nielsen,et al.  Vertebral bone density evaluated by dual-energy X-ray absorptiometry and quantitative computed tomography in vitro. , 1998, Bone.

[6]  Ralph Müller,et al.  Guidelines for assessment of bone microstructure in rodents using micro–computed tomography , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[7]  R. Müller,et al.  A sensitivity analysis of the volumetric spatial decomposition algorithm , 2007, Computer methods in biomechanics and biomedical engineering.

[8]  Jack Bresenham,et al.  Algorithm for computer control of a digital plotter , 1965, IBM Syst. J..

[9]  Jesper Skovhus Thomsen,et al.  Zone-dependent changes in human vertebral trabecular bone: clinical implications. , 2002, Bone.

[10]  Ralph Müller,et al.  Volumetric spatial decomposition of trabecular bone into rods and plates--a new method for local bone morphometry. , 2006, Bone.

[11]  X Edward Guo,et al.  Contributions of trabecular rods of various orientations in determining the elastic properties of human vertebral trabecular bone. , 2007, Bone.

[12]  A. Tietze,et al.  Changes in 3‐dimensional bone structure indices in hypoparathyroid patients treated with PTH(1‐84): A randomized controlled study , 2012, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[13]  Sharmila Majumdar,et al.  A Local Adaptive Threshold Strategy for High Resolution Peripheral Quantitative Computed Tomography of Trabecular Bone , 2007, Annals of Biomedical Engineering.

[14]  Paul Sajda,et al.  Complete Volumetric Decomposition of Individual Trabecular Plates and Rods and Its Morphological Correlations With Anisotropic Elastic Moduli in Human Trabecular Bone , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[15]  G. H. Bell,et al.  Variations in strength of vertebrae with age and their relation to osteoporosis , 2005, Calcified Tissue Research.

[16]  Guo-min Liu,et al.  Age-related differences in microstructure, density and biomechanics of vertebral cancellous bone of Chinese males , 2012, The aging male : the official journal of the International Society for the Study of the Aging Male.

[17]  J. Wark,et al.  Failure strength of human vertebrae: prediction using bone mineral density measured by DXA and bone volume by micro-CT. , 2012, Bone.

[18]  P. Papadopoulos,et al.  Vertebral fragility and structural redundancy , 2012, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[19]  Heather M. Macdonald,et al.  Age‐related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: A population‐based HR‐pQCT study , 2011, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[20]  F Eckstein,et al.  The osteoporotic vertebral structure is well adapted to the loads of daily life, but not to infrequent "error" loads. , 2004, Bone.

[21]  M. Grynpas,et al.  Inhomogeneity of human vertebral cancellous bone: systematic density and structure patterns inside the vertebral body. , 2001, Bone.

[22]  J S Thomsen,et al.  A new method of comprehensive static histomorphometry applied on human lumbar vertebral cancellous bone. , 2000, Bone.

[23]  Paul Sajda,et al.  Quantification of the Roles of Trabecular Microarchitecture and Trabecular Type in Determining the Elastic Modulus of Human Trabecular Bone , 2006, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[24]  Felix Eckstein,et al.  Strength through structure: visualization and local assessment of the trabecular bone structure , 2008 .

[25]  D. Dempster Bone microarchitecture and strength , 2003, Osteoporosis International.

[26]  Ralph Müller,et al.  Importance of Individual Rods and Plates in the Assessment of Bone Quality and Their Contribution to Bone Stiffness , 2006, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[27]  L. Mosekilde,et al.  A model of vertebral trabecular bone architecture and its mechanical properties. , 1990, Bone.

[28]  William H. Press,et al.  The Art of Scientific Computing Second Edition , 1998 .

[29]  C. Casuccio An Introduction to the Study of Osteoporosis (Biochemical and Biophysical Research in Bone Ageing) , 1962, Proceedings of the Royal Society of Medicine.

[30]  Tony M Keaveny,et al.  Influence of Vertical Trabeculae on the Compressive Strength of the Human Vertebra , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[31]  L. Mosekilde,et al.  Static histomorphometry of human iliac crest and vertebral trabecular bone: a comparative study. , 2002, Bone.

[32]  Heike Scherf,et al.  A new high-resolution computed tomography (CT) segmentation method for trabecular bone architectural analysis. , 2009, American journal of physical anthropology.

[33]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[34]  D R Sumner,et al.  Parallel plate model for trabecular bone exhibits volume fraction-dependent bias. , 2000, Bone.

[35]  H. Weinans,et al.  Mechanical Consequences of Bone Loss in Cancellous Bone , 2001, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[36]  M. Kleerekoper,et al.  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. , 1983, The Journal of clinical investigation.

[37]  W. Kalender,et al.  Global and regional variations in the spinal trabecular bone: single and dual energy examinations. , 1991, The Journal of clinical endocrinology and metabolism.

[38]  J S Thomsen,et al.  Lumbar vertebral body compressive strength evaluated by dual-energy X-ray absorptiometry, quantitative computed tomography, and ashing. , 1999, Bone.

[39]  L. Vico,et al.  3D micro-computed tomography of trabecular and cortical bone architecture with application to a rat model of immobilisation osteoporosis , 2000, Medical and Biological Engineering and Computing.

[40]  P. Rüegsegger,et al.  Direct Three‐Dimensional Morphometric Analysis of Human Cancellous Bone: Microstructural Data from Spine, Femur, Iliac Crest, and Calcaneus , 1999, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[41]  J S Thomsen,et al.  Age-related differences between thinning of horizontal and vertical trabeculae in human lumbar bone as assessed by a new computerized method. , 2002, Bone.

[42]  TOR Hildebrand,et al.  Quantification of Bone Microarchitecture with the Structure Model Index. , 1997, Computer methods in biomechanics and biomedical engineering.

[43]  T Dufresne,et al.  Segmentation techniques for analysis of bone by three-dimensional computed tomographic imaging. , 1998, Technology and health care : official journal of the European Society for Engineering and Medicine.

[44]  F. Prêteux,et al.  Measurement of anisotropic vertebral trabecular bone loss during aging by quantitative image analysis , 1988, Calcified Tissue International.

[45]  N. Harrison,et al.  Simulation of vertebral trabecular bone loss using voxel finite element analysis. , 2009, Journal of biomechanics.

[46]  J S Thomsen,et al.  Age‐ and Gender‐Related Differences in Vertebral Bone Mass, Density, and Strength , 1999, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[47]  H. Frost On the Trabecular “Thickness”‐Number Problem , 1999, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[48]  R. Müller,et al.  Age-related changes in trabecular bone microstructures: global and local morphometry , 2005, Osteoporosis International.

[49]  C. Slemenda,et al.  Age and bone mass as predictors of fracture in a prospective study. , 1988, The Journal of clinical investigation.

[50]  S Prohaska,et al.  Stereological measures of trabecular bone structure: comparison of 3D micro computed tomography with 2D histological sections in human proximal tibial bone biopsies , 2005, Journal of microscopy.

[51]  J S Thomsen,et al.  Relationships between static histomorphometry and bone strength measurements in human iliac crest bone biopsies. , 1998, Bone.

[52]  P. Rüegsegger,et al.  A new method for the model‐independent assessment of thickness in three‐dimensional images , 1997 .

[53]  P Rüegsegger,et al.  Comparison of structure extraction methods for in vivo trabecular bone measurements. , 1999, Computerized medical imaging and graphics : the official journal of the Computerized Medical Imaging Society.

[54]  H. Gundersen,et al.  Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. , 1993, Bone.

[55]  Sheila J. Jones,et al.  Three-dimensional photographic study of cancellous bone in human fourth lumbar vertebral bodies , 1994, Anatomy and Embryology.

[56]  P. J. Atkinson Variation in trabecular structure of vertebrae with age , 2005, Calcified Tissue Research.