Three-dimensional methods for quantification of cancellous bone architecture.

Recent development in three-dimensional (3-D) imaging of cancellous bone has made possible true 3-D quantification of trabecular architecture. This provides a significant improvement of the tools available for studying and understanding the mechanical functions of cancellous bone. This article reviews the different techniques for 3-D imaging, which include serial sectioning, X-ray tomographic methods, and NMR scanning. Basic architectural features of cancellous bone are discussed, and it is argued that connectivity and architectural anisotropy (fabric) are of special interest in mechanics-architecture relations. A full characterization of elastic mechanical properties is, with traditional mechanical testing, virtually impossible, but 3-D reconstruction in combination with newly developed methods for large-scale finite element analysis allow calculations of all elastic properties at the cancellous bone continuum level. Connectivity has traditionally been approached by various 2-D methods, but none of these methods have any known relation to 3-D connectivity. A topological approach allows unbiased quantification of connectivity, and this further allows expressions of the mean size of individual trabeculae, which has previously also been approached by a number of uncertain 2-D methods. Anisotropy may be quantified by fundamentally different methods. The well-known mean intercept length method is an interface-based method, whereas the volume orientation method is representative of volume-based methods. Recent studies indicate that volume-based methods are at least as good as interface-based methods in predicting mechanical anisotropy. Any other architectural property may be quantified from 3-D reconstructions of cancellous bone specimens as long as an explicit definition of the property can be given. This challenges intuitive and vaguely defined architectural properties and forces bone scientists toward 3-D thinking.

[1]  Kanatani Ken-Ichi DISTRIBUTION OF DIRECTIONAL DATA AND FABRIC TENSORS , 1984 .

[2]  N L Fazzalari,et al.  Direct calculation of the surface-to-volume ratio for human cancellous bone. , 1993, Journal of biomechanics.

[3]  H. Hadwiger,et al.  Normale Körper im euklidischen Raum und ihre topologischen und metrischen Eigenschaften , 1959 .

[4]  Michael F. Ashby,et al.  The mechanical properties of cellular solids , 1983 .

[5]  Edward D. Pittman,et al.  Use of Pore Casts and Scanning Electron Microscope to Study Pore Geometry , 1970 .

[6]  S. Goldstein The mechanical properties of trabecular bone: dependence on anatomic location and function. , 1987, Journal of biomechanics.

[7]  Hwj Rik Huiskes,et al.  The role of trabecular architecture in the anisotropic mechanical properties of bone , 1995 .

[8]  R. Newcombe,et al.  Structural mechanisms of trabecular bone loss in man. , 1989, Bone and mineral.

[9]  Davis,et al.  Topology and elastic properties of depleted media. , 1988, Physical review. B, Condensed matter.

[10]  I. Singh The architecture of cancellous bone. , 1978, Journal of anatomy.

[11]  R. Martin,et al.  Determinants of the mechanical properties of bones. , 1991, Journal of biomechanics.

[12]  F. Linde,et al.  The effect of constraint on the mechanical behaviour of trabecular bone specimens. , 1989, Journal of biomechanics.

[13]  J. Currey,et al.  Density and temperature effects on some mechanical properties of cancellous bone. , 1988, Engineering in medicine.

[14]  F. Linde,et al.  The effect of different storage methods on the mechanical properties of trabecular bone. , 1993, Journal of biomechanics.

[15]  S. Goldstein,et al.  Evaluation of a microcomputed tomography system to study trabecular bone structure , 1990, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[16]  R M Rose,et al.  The distribution and anisotropy of the stiffness of cancellous bone in the human patella. , 1975, Journal of biomechanics.

[17]  T. McMahon,et al.  Trabecular bone exhibits fully linear elastic behavior and yields at low strains. , 1994, Journal of biomechanics.

[18]  C. S. Yust,et al.  Some fundamental ideas in topology and their application to problems in metallography , 1970 .

[19]  C. Turner,et al.  Yield behavior of bovine cancellous bone. , 1989, Journal of biomechanical engineering.

[20]  K Andersen,et al.  Three-dimensional reconstruction of entire vertebral bodies. , 1994, Bone.

[21]  R. Huiskes,et al.  Fabric and elastic principal directions of cancellous bone are closely related. , 1997, Journal of biomechanics.

[22]  H. Giger,et al.  Grundgleichungen der Stereologie I , 1970 .

[23]  F. Wehrli,et al.  High‐resolution variable flip angle 3D MR imaging of trabecular microstructure in vivo , 1993, Magnetic resonance in medicine.

[24]  L. Mosekilde Age-related changes in vertebral trabecular bone architecture--assessed by a new method. , 1988, Bone.

[25]  D. Marshall,et al.  Review of progress in quantitative non-destructive evaluation: edited by D. O. Thompson and D. E. Chimenti; published by Plenum, New York, 1983; 1853 pp.; price, U.S. $225.00 , 1985 .

[26]  J. Koplik,et al.  Conductivity and permeability from microgeometry , 1984 .

[27]  M. C. Nichols,et al.  X-Ray Tomographic Microscopy (XTM) Using Synchrotron Radiation , 1992 .

[28]  H. Hadwiger Vorlesungen über Inhalt, Oberfläche und Isoperimetrie , 1957 .

[29]  D M Spengler,et al.  Multiplanar variations in the structural characteristics of cancellous bone. , 1994, Bone.

[30]  E. C. Larke,et al.  Resistance of copper and copper alloys to homogeneous deformation in compression , 1945 .

[31]  S C Cowin,et al.  Errors induced by off-axis measurement of the elastic properties of bone. , 1988, Journal of biomechanical engineering.

[32]  Frank Linde,et al.  The effect of specimen geometry on the mechanical behaviour of trabecular bone specimens. , 1992, Journal of biomechanics.

[33]  M. Drezner,et al.  Bone histomorphometry: Standardization of nomenclature, symbols, and units: Report of the asbmr histomorphometry nomenclature committee , 1987, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[34]  F. Linde,et al.  Compressive axial strain distributions in cancellous bone specimens. , 1989, Journal of biomechanics.

[35]  A. Odgaard,et al.  Poisson's ratio in tibial trabecular bone , 1990 .

[36]  J. Currey,et al.  Effects of Structural Variation on Young's Modulus of Non-Human Cancellous Bone , 1990, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[37]  F Melsen,et al.  A direct method for fast three‐dimensional serial reconstruction , 1990, Journal of microscopy.

[38]  J. Mcelhaney,et al.  Mechanical properties on cranial bone. , 1970, Journal of biomechanics.

[39]  Vladimir A. Kovalevsky,et al.  Finite topology as applied to image analysis , 1989, Comput. Vis. Graph. Image Process..

[40]  M M Vrijhoef,et al.  On the interaction between specimen and testing machine in mechanical testing procedures. , 1971, Journal of biomechanics.

[41]  L. Gibson The mechanical behaviour of cancellous bone. , 1985, Journal of biomechanics.

[42]  Lutz Muche A remark on the area orientation distribution , 1993 .

[43]  Savio Lau-Yuen Woo,et al.  Biomechanics of diarthrodial joints , 1990 .

[44]  Stephen C. Cowin,et al.  Dependence of elastic constants of an anisotropic porous material upon porosity and fabric , 1987 .

[45]  H J Gundersen,et al.  Unbiased stereologic estimation of surface density in bone using vertical sections. , 1987, Bone.

[46]  W. Hayes,et al.  A 20-year perspective on the mechanical properties of trabecular bone. , 1993, Journal of biomechanical engineering.

[47]  Nicholas I. Fisher,et al.  Statistical Analysis of Spherical Data. , 1987 .

[48]  L. Feldkamp,et al.  Practical cone-beam algorithm , 1984 .

[49]  P. Meunier,et al.  Age-related changes in cancellous bone structure. A two-dimensional study in the transiliac and iliac crest biopsy sites. , 1988, Bone and mineral.

[50]  W. Hayes,et al.  Theoretical analysis of the experimental artifact in trabecular bone compressive modulus. , 1993, Journal of biomechanics.

[51]  J. Kinney,et al.  In vivo, three‐dimensional microscopy of trabecular bone , 1995, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[52]  Stephen C. Cowin,et al.  FABRIC DEPENDENCE OF AN ANISOTROPIC STRENGTH CRITERION , 1986 .

[53]  U. Bonse,et al.  3D computed X-ray tomography of human cancellous bone at 8 microns spatial and 10(-4) energy resolution. , 1994, Bone and mineral.

[54]  H. Amstutz,et al.  The structure of the vertebral spongiosa. , 1969, The Journal of bone and joint surgery. British volume.

[55]  J. Wolff Das Gesetz der Transformation der Knochen , 1893 .

[56]  D M Spengler,et al.  Effects of specimen load-bearing and free surface layers on the compressive mechanical properties of cellular materials. , 1994, Journal of biomechanics.

[57]  R. Huiskes,et al.  Direct mechanics assessment of elastic symmetries and properties of trabecular bone architecture. , 1996, Journal of biomechanics.

[58]  Wilson C. Hayes,et al.  Alterations in trabecular structure induced by changing bone density in the lumbar vertebral body , 1988 .

[59]  S A Goldstein,et al.  Morphometric and anisotropic symmetries of the canine distal femur , 1990, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[60]  R. Martin,et al.  Bone structure and remodeling , 1996 .

[61]  Sia Nemat-Nasser,et al.  Some experimentally based fundamental results on the mechanical behaviour of granular materials , 1980 .

[62]  J. Compston,et al.  Measurement of mean trabecular plate thickness by a new computerized method. , 1987, Bone.

[63]  F. Linde,et al.  Elastic and viscoelastic properties of trabecular bone by a compression testing approach. , 1994, Danish medical bulletin.

[64]  T. Brown,et al.  Mechanical property distributions in the cancellous bone of the human proximal femur. , 1980, Acta orthopaedica Scandinavica.

[65]  M. Ashby,et al.  Cellular solids: Structure & properties , 1988 .

[66]  J. Compston,et al.  A new method for the two‐dimensional analysis of bone structure in human iliac crest biopsies , 1986, Journal of microscopy.

[67]  M. C. Nichols,et al.  X-ray Tomographic Study of Chemical Vapor Infiltration Processing of Ceramic Composites , 1993, Science.

[68]  S. Goldstein,et al.  The direct examination of three‐dimensional bone architecture in vitro by computed tomography , 1989, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[69]  Frank Linde,et al.  Three-axial strain controlled testing applied to bone specimens from the proximal tibial epiphysis. , 1990, Journal of biomechanics.

[70]  U. Bonse,et al.  Optimization of CCD-based energy-modulated x-ray microtomography , 1989 .

[71]  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.

[72]  Rik Huiskes,et al.  Mechanical properties of trabecular bone, an experimental and finite element study , 1985 .

[73]  P. Knauß,et al.  Materialkennwerte und Festigkeitsverhalten des spongiösen Knochengewebes am coxalen Human-Femur - Material Properties and Strength Behaviour of Spongy Bone Tissue at the Coxal Human Femur , 1981 .

[74]  Horace Ho-Shing Ip Detection and three-dimensional reconstruction of a vascular network from serial sections , 1983, Pattern Recognit. Lett..

[75]  S A Goldstein,et al.  The relationship between the structural and orthogonal compressive properties of trabecular bone. , 1994, Journal of biomechanics.

[76]  James C. Wang Young's modulus of porous materials , 1984 .

[77]  E. Philofsky,et al.  On the measurement of the orientation distribution of lineal and areal arrays , 1969 .

[78]  H J Gundersen,et al.  Direct stereological estimation of three-dimensional connectivity in rat vertebrae: effect of estrogen, etidronate and risedronate following ovariectomy. , 1995, Bone.

[79]  R M Rose,et al.  Trabecular architecture of the human patella. , 1975, Journal of biomechanics.

[80]  L. A. Feldkamp,et al.  3-D X-Ray Computed Tomography , 1986 .

[81]  S. Cowin,et al.  On the dependence of the elasticity and strength of cancellous bone on apparent density. , 1988, Journal of biomechanics.

[82]  P Rüegsegger,et al.  Non-invasive bone biopsy: a new method to analyse and display the three-dimensional structure of trabecular bone. , 1994, Physics in medicine and biology.

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

[84]  K. Kanatani Stereological determination of structural anisotropy , 1984 .

[85]  W. J. Whitehouse The quantitative morphology of anisotropic trabecular bone , 1974, Journal of microscopy.

[86]  R Van Audekercke,et al.  The mechanical characteristics of cancellous bone at the upper femoral region. , 1983, Journal of biomechanics.

[87]  S C Cowin,et al.  The fabric dependence of the orthotropic elastic constants of cancellous bone. , 1990, Journal of biomechanics.

[88]  C. Hirsch,et al.  Factors affecting the determination of the physical properties of femoral cortical bone. , 1966, Acta orthopaedica Scandinavica.

[89]  Masanobu Oda,et al.  ELASTIC COMPLIANCE FOR ROCK-LIKE MATERIALS WITH RANDOM CRACKS , 1984 .

[90]  P. Gaunt,et al.  Three dimensional reconstruction in biology , 1978 .

[91]  R. Mann,et al.  Characterization of microstructural anisotropy in orthotropic materials using a second rank tensor , 1984 .

[92]  A. Vesterby,et al.  Star volume in bone research. A histomorphometric analysis of trabecular bone structure using vertical sections , 1993, The Anatomical record.

[93]  W H Harris,et al.  Limitations of the continuum assumption in cancellous bone. , 1988, Journal of biomechanics.

[94]  N. Kikuchi,et al.  A homogenization sampling procedure for calculating trabecular bone effective stiffness and tissue level stress. , 1994, Journal of biomechanics.

[95]  N. K. Tovey,et al.  A digital computer technique for orientation analysis of micrographs of soil fabric , 1980 .

[96]  H J Gundersen,et al.  Unbiased estimation of vertebral trabecular connectivity in calcium-restricted ovariectomized minipigs. , 1995, Bone.

[97]  George W.C. Hung,et al.  Stereological methods, vol. 2: Theoretical foundations: By Ewald R. Weibel. Academic Press, New York, 1980. xiv + 340 pp., $62.50 , 1984 .

[98]  C. K. Jackson,et al.  The scanning electron microscope in studies of trabecular bone from a human vertebral body. , 1971, Journal of anatomy.

[99]  R. Huiskes,et al.  Mechanical and textural properties of pelvic trabecular bone. , 1993, Journal of biomechanics.

[100]  Steven D. Kugelmass,et al.  Quantitative analysis of trabecular microstructure by 400 MHz nuclear magnetic resonance imaging , 1995, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[101]  H. Gundersen,et al.  Biologically meaningful determinants of the in vitro strength of lumbar vertebrae. , 1991, Bone.

[102]  R. Lindsay,et al.  A simple method for correlative light and scanning electron microscopy of human iliac crest bone biopsies: Qualitative observations in normal and osteoporotic subjects , 1986, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[103]  David P. Fyhrie,et al.  Structural transformations indistinquishable by point-count stereology , 1992 .

[104]  P Rüegsegger,et al.  Analysis of mechanical properties of cancellous bone under conditions of simulated bone atrophy. , 1996, Journal of biomechanics.

[105]  M. Oda INITIAL FABRICS AND THEIR RELATIONS TO MECHANICAL PROPERTIES OF GRANULAR MATERIAL , 1972 .

[106]  J R Nyengaard,et al.  The Conneulor: unbiased estimation of connectivity using physical disectors under projection. , 1993, Bone.

[107]  J. E. Hilliard,et al.  Determination of Structural Anisotropy , 1967 .

[108]  Michael C. Hall The architecture of bone , 1966 .

[109]  S. Majumdar,et al.  Fractal geometry and vertebral compression fractures , 1994, Journal of Bone and Mineral Research.

[110]  I. Hvid,et al.  Bone mineral assay: its relation to the mechanical strength of cancellous bone. , 1985, Engineering in medicine.

[111]  Søren E. Larsen,et al.  Characterizing anisotropy: A new concept☆ , 1992 .

[112]  J. Lewis,et al.  Properties and an anisotropic model of cancellous bone from the proximal tibial epiphysis. , 1982, Journal of biomechanical engineering.

[113]  Nicholas I. Fisher,et al.  Statistical Analysis of Spherical Data. , 1987 .

[114]  S. Cross,et al.  Trabecular bone does not have a fractal structure on light microscopic examination , 1993, The Journal of pathology.

[115]  W C Hayes,et al.  Trabecular bone modulus and strength can depend on specimen geometry. , 1993, Journal of biomechanics.

[116]  J. Currey,et al.  The Effect of Variation in Structure on the Young's Modulus of Cancellous Bone: A Comparison of Human and Non-Human Material , 1990, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[117]  S. Cowin,et al.  Wolff's law of trabecular architecture at remodeling equilibrium. , 1986, Journal of biomechanical engineering.

[118]  W. C. Hayes,et al.  Multiaxial Structure-Property Relations in Trabecular Bone , 1990 .

[119]  P. Doyen,et al.  Permeability, conductivity, and pore geometry of sandstone , 1988 .

[120]  M. Underweiser,et al.  On the fractal nature of trabecular structure. , 1994, Medical physics.

[121]  K. Mardia Statistics of Directional Data , 1972 .

[122]  Dietrich Stoyan,et al.  Anisotropy analysis for particle systems , 1991 .

[123]  W. Hayes,et al.  The compressive behavior of bone as a two-phase porous structure. , 1977, The Journal of bone and joint surgery. American volume.

[124]  Rik Huiskes,et al.  Cancellous bone mechanical main directions can be predicted by trabecular anisotropy , 1996 .

[125]  Richard H. Gallagher,et al.  Finite Elements in Biomechanics , 1982 .

[126]  R M Rose,et al.  Quantitative studies of human subchondral cancellous bone. Its relationship to the state of its overlying cartilage. , 1974, The Journal of bone and joint surgery. American volume.

[127]  R. Huiskes,et al.  A new method to determine trabecular bone elastic properties and loading using micromechanical finite-element models. , 1995, Journal of biomechanics.

[128]  I. T. Young,et al.  Quantitative Microscopy , 1984, Definitions.

[129]  W M O'Fallon,et al.  Effect of fluoride treatment on the fracture rate in postmenopausal women with osteoporosis. , 1990, The New England journal of medicine.

[130]  M. Peacock,et al.  The architecture of cancellous and cortical bone in femoral neck fracture. , 1990, Bone and mineral.

[131]  John C. Koch,et al.  The laws of bone architecture , 1917 .

[132]  Noboru Kikuchi,et al.  The Mechanical and Remodeling Properties of Trabecular Bone , 1990 .

[133]  R. T. DeHoff,et al.  Quantitative serial sectioning analysis: preview , 1983 .

[134]  R. Kapadia,et al.  Magnetic resonance microscopy in rat skeletal research , 1993, Magnetic resonance in medicine.

[135]  M Vogel,et al.  Trabecular bone pattern factor--a new parameter for simple quantification of bone microarchitecture. , 1992, Bone.

[136]  R M Rose,et al.  A structural model for the mechanical behavior of trabecular bone. , 1973, Journal of biomechanics.

[137]  S. Majumdar,et al.  Evaluation of technical factors affecting the quantification of trabecular bone structure using magnetic resonance imaging. , 1995, Bone.

[138]  J. Aaron,et al.  The microanatomy of trabecular bone loss in normal aging men and women. , 1987, Clinical orthopaedics and related research.

[139]  L. Mosekilde,et al.  Biomechanical competence of vertebral trabecular bone in relation to ash density and age in normal individuals. , 1987, Bone.

[140]  Pierre M. Adler,et al.  Computerized characterization of the geometry of real porous media: their discretization, analysis and interpretation , 1993 .

[141]  J. Kinney,et al.  Intermittent treatment with human parathyroid hormone (hPTH[1‐34]) increased trabecular bone volume but not connectivity in osteopenic rats , 1995, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[142]  I. F. Macdonald,et al.  Three‐dimensional reconstruction of porous media from serial section data , 1990 .

[143]  J. Compston,et al.  Age-related changes in iliac crest trabecular microanatomic bone structure in man. , 1987, Bone.

[144]  H J Gundersen,et al.  Estimation of structural anisotropy based on volume orientation. A new concept , 1990, Journal of microscopy.

[145]  Ioannis Chatzis,et al.  Two‐phase flow in porous media: obtaining sharp digitized images of serial sections for subsequent quantitative analysis , 1988 .

[146]  H. Gundersen,et al.  Stereological estimation of the volume‐weighted mean volume of arbitrary particles observed on random sections * , 1985, Journal of microscopy.

[147]  F. Linde,et al.  The underestimation of Young's modulus in compressive testing of cancellous bone specimens. , 1991, Journal of biomechanics.

[148]  S C Cowin,et al.  Identification of the elastic symmetry of bone and other materials. , 1989, Journal of biomechanics.

[149]  William M. O'Fallon,et al.  Effect of fluoride treatment on the fracture rate in postmenopausal women with osteoporosis. , 1990 .

[150]  W. Hayes,et al.  Finite element analysis of a three-dimensional open-celled model for trabecular bone. , 1985, Journal of biomechanical engineering.

[151]  Kanatani Ken-Ichi,et al.  Procedures for stereological estimation of structural anisotropy , 1985 .

[152]  C. J. Hilditch,et al.  Linear Skeletons From Square Cupboards , 1969 .