Structure Model Index Does Not Measure Rods and Plates in Trabecular Bone

Structure model index (SMI) is widely used to measure rods and plates in trabecular bone. It exploits the change in surface curvature that occurs as a structure varies from spherical (SMI = 4), to cylindrical (SMI = 3) to planar (SMI = 0). The most important assumption underlying SMI is that the entire bone surface is convex and that the curvature differential is positive at all points on the surface. The intricate connections within the trabecular continuum suggest that a high proportion of the surface could be concave, violating the assumption of convexity and producing regions of negative differential. We implemented SMI in the BoneJ plugin and included the ability to measure the amounts of surface that increased or decreased in area after surface mesh dilation, and the ability to visualize concave and convex regions. We measured SMI and its positive (SMI+) and negative (SMI−) components, bone volume fraction (BV/TV), the fraction of the surface that is concave (CF), and mean ellipsoid factor (EF) in trabecular bone using 38 X-ray microtomography (XMT) images from a rat ovariectomy model of sex steroid rescue of bone loss, and 169 XMT images from a broad selection of 87 species’ femora (mammals, birds, and a crocodile). We simulated bone resorption by eroding an image of elephant trabeculae and recording SMI and BV/TV at each erosion step. Up to 70%, and rarely <20%, of the trabecular surface is concave (CF 0.155–0.700). SMI is unavoidably influenced by aberrations induced by SMI−, which is strongly correlated with BV/TV and CF. The plate-to-rod transition in bone loss is an erroneous observation resulting from the close and artifactual relationship between SMI and BV/TV. SMI cannot discern between the distinctive trabecular geometries typical of mammalian and avian bone, whereas EF clearly detects birds’ more plate-like trabeculae. EF is free from confounding relationships with BV/TV and CF. SMI results reported in the literature should be treated with suspicion. We propose that EF should be used instead of SMI for measurements of rods and plates in trabecular bone.

[1]  T. Rantalainen,et al.  BoneJ: BoneJ version 1.4.1 , 2015 .

[2]  P. Zysset,et al.  Bone Volume Fraction and Fabric Anisotropy Are Better Determinants of Trabecular Bone Stiffness Than Other Morphological Variables , 2015, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[3]  X. Guo,et al.  Trabecular plates and rods determine elastic modulus and yield strength of human trabecular bone. , 2015, Bone.

[4]  T. Wright,et al.  Trabecular bone microarchitecture and characteristics in different regions of the glenoid. , 2015, Orthopedics.

[5]  M. Doube The Ellipsoid Factor for Quantification of Rods, Plates, and Intermediate Forms in 3D Geometries , 2015, Front. Endocrinol..

[6]  X. S. Liu,et al.  A closer look at the immediate trabecula response to combined parathyroid hormone and alendronate treatment. , 2013, Bone.

[7]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[8]  J. Ward RELATIONSHIPS OF LONG-TERM BISPHOSPHONATE TREATMENT WITH MEASURES OF BONE MICROARCHITECTURE AND MECHANICAL COMPETENCE , 2014 .

[9]  D. Mahapatra,et al.  Osteoprotective effect of propranolol in ovariectomized rats: a comparison with zoledronic acid and alfacalcidol , 2013, Journal of orthopaedic science : official journal of the Japanese Orthopaedic Association.

[10]  P. Trivedi,et al.  Withaferin A: a proteasomal inhibitor promotes healing after injury and exerts anabolic effect on osteoporotic bone , 2013, Cell Death and Disease.

[11]  M. Bouxsein,et al.  The predictive value of trabecular bone score (TBS) on whole lumbar vertebrae mechanics: an ex vivo study , 2013, Osteoporosis International.

[12]  Manoj Kumar,et al.  Discovery of coumarin-dihydropyridine hybrids as bone anabolic agents. , 2013, Journal of medicinal chemistry.

[13]  Kerstin Pingel,et al.  50 Years of Image Analysis , 2012 .

[14]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[15]  R. Bloebaum,et al.  Do regional modifications in tissue mineral content and microscopic mineralization heterogeneity adapt trabecular bone tracts for habitual bending? Analysis in the context of trabecular architecture of deer calcanei , 2012, Journal of anatomy.

[16]  Sandra J. Shefelbine,et al.  Trabecular bone scales allometrically in mammals and birds , 2011, Proceedings of the Royal Society B: Biological Sciences.

[17]  D. Scharnweber,et al.  The bone architecture is enhanced with combined PTH and alendronate treatment compared to monotherapy while maintaining the state of surface mineralization in the OVX rat. , 2011, Bone.

[18]  S. Majumdar,et al.  Teriparatide in Bisphosphonate-Resistant Osteoporosis: Microarchitectural Changes and Clinical Results After 6 and 18 months , 2011, Calcified Tissue International.

[19]  P. Zysset,et al.  Increased bone resorption and impaired bone microarchitecture in short-term and extended high-fat diet-induced obesity. , 2011, Metabolism: clinical and experimental.

[20]  S. Boyd,et al.  Bone quality is partially recovered after the discontinuation of RANKL administration in rats by increased bone mass on existing trabeculae: an in vivo micro-CT study , 2011, Osteoporosis International.

[21]  Sandra J Shefelbine,et al.  BoneJ: Free and extensible bone image analysis in ImageJ. , 2010, Bone.

[22]  Jacques P. Brown,et al.  Effects of denosumab on bone histomorphometry: The FREEDOM and STAND studies , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[23]  R. Guldberg,et al.  The effect of the trabecular microstructure on the pullout strength of suture anchors. , 2010, Journal of biomechanics.

[24]  Olivier Guyen,et al.  Role of Trabecular Microarchitecture and Its Heterogeneity Parameters in the Mechanical Behavior of Ex Vivo Human L3 Vertebrae , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[25]  Benjamin Schmid,et al.  A high-level 3D visualization API for Java and ImageJ , 2010, BMC Bioinformatics.

[26]  G. Niebur,et al.  Effects of trabecular type and orientation on microdamage susceptibility in trabecular bone. , 2010, Bone.

[27]  R. Müller,et al.  Three dimensional cancellous bone structure in hypoparathyroidism. , 2010, Bone.

[28]  Z.-M. Zhang,et al.  Micro-CT and mechanical evaluation of subchondral trabecular bone structure between postmenopausal women with osteoarthritis and osteoporosis , 2010, Osteoporosis International.

[29]  N. L. Fazzalari,et al.  Detecting early bone changes using in vivo micro-CT in ovariectomized, zoledronic acid-treated, and sham-operated rats , 2010, Osteoporosis International.

[30]  B. Latimer,et al.  Trabecular Microarchitecture of Hominoid Thoracic Vertebrae , 2009, Anatomical record.

[31]  C. Farquharson,et al.  Increased bone mass , altered trabecular architecture and modified growth plate organization in the growing skeleton of SOCS 2 deficient mice , 2013 .

[32]  R. Maciewicz,et al.  Bone marrow lesions from osteoarthritis knees are characterized by sclerotic bone that is less well mineralized , 2009, Arthritis research & therapy.

[33]  R. Recker,et al.  Cancellous and cortical bone architecture and turnover at the iliac crest of postmenopausal osteoporotic women treated with parathyroid hormone 1-84. , 2009, Bone.

[34]  Steven K Boyd,et al.  Postpubertal Architectural Developmental Patterns Differ Between the L3 Vertebra and Proximal Tibia in Three Inbred Strains of Mice , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[35]  Deepak Vashishth,et al.  Microarchitecture Influences Microdamage Accumulation in Human Vertebral Trabecular Bone , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[36]  H. Genant,et al.  Histomorphometric and μCT Analysis of Bone Biopsies From Postmenopausal Osteoporotic Women Treated With Strontium Ranelate , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[37]  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.

[38]  C. Rubin,et al.  Evaluation of trabecular mechanical and microstructural properties in human calcaneal bone of advanced age using mechanical testing, microCT, and DXA. , 2008, Journal of biomechanics.

[39]  M Viceconti,et al.  Structural parameters and mechanical strength of cancellous bone in the femoral head in osteoarthritis do not depend on age. , 2007, Bone.

[40]  Mary L Bouxsein,et al.  Age‐Related Changes in Trabecular Architecture Differ in Female and Male C57BL/6J Mice , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[41]  Swee Hin Teoh,et al.  Correlation of cancellous bone microarchitectural parameters from microCT to CT number and bone mechanical properties , 2007 .

[42]  P. Papadopoulos,et al.  Influence of bone volume fraction and architecture on computed large-deformation failure mechanisms in human trabecular bone. , 2006, Bone.

[43]  Ralph Müller,et al.  Monitoring individual morphological changes over time in ovariectomized rats by in vivo micro-computed tomography. , 2006, Bone.

[44]  S. Vukicevic,et al.  Systemically Administered Bone Morphogenetic Protein-6 Restores Bone in Aged Ovariectomized Rats by Increasing Bone Formation and Suppressing Bone Resorption* , 2006, Journal of Biological Chemistry.

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

[46]  M. Ashby The properties of foams and lattices , 2006, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[47]  Daniel Chappard,et al.  Comparison Insight Bone Measurements by Histomorphometry and μCT , 2005 .

[48]  Yi-Xian Qin,et al.  Interrelationship of trabecular mechanical and microstructural properties in sheep trabecular bone. , 2005, Journal of biomechanics.

[49]  M. Uetani,et al.  Effects of risedronate on trabecular microstructure and biomechanical properties in ovariectomized rat tibia , 2005, Osteoporosis International.

[50]  R. Müller,et al.  Intermittent Ibandronate Preserves Bone Quality and Bone Strength in the Lumbar Spine After 16 Months of Treatment in the Ovariectomized Cynomolgus Monkey , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[51]  S. Movérare-Skrtic,et al.  Additive Protective Effects of Estrogen and Androgen Treatment on Trabecular Bone in Ovariectomized Rats , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[52]  T. Keaveny,et al.  Mechanisms of uniformity of yield strains for trabecular bone. , 2004, Journal of biomechanics.

[53]  Harrie Weinans,et al.  An Improved Segmentation Method for In Vivo μCT Imaging , 2004 .

[54]  A. Mócsai,et al.  The immunomodulatory adapter proteins DAP12 and Fc receptor γ-chain (FcRγ) regulate development of functional osteoclasts through the Syk tyrosine kinase , 2004 .

[55]  A. Chines,et al.  Risedronate preserves bone architecture in postmenopausal women with osteoporosis as measured by three-dimensional microcomputed tomography. , 2004, Bone.

[56]  Harrie Weinans,et al.  An improved segmentation method for in vivo microCT imaging. , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[57]  H. Genant,et al.  Recombinant Human Parathyroid Hormone (1–34) [Teriparatide] Improves Both Cortical and Cancellous Bone Structure , 2003, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[58]  Masako Ito,et al.  Long‐Term Treatment of Incadronate Disodium Accumulates Microdamage but Improves the Trabecular Bone Microarchitecture in Dog Vertebra , 2003, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[59]  Sharmila Majumdar,et al.  Changes in Bone Structure and Mass With Advancing Age in the Male C57BL/6J Mouse , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[60]  S. Majumdar,et al.  The Temporal Changes of Trabecular Architecture in Ovariectomized Rats Assessed by MicroCT , 2001, Osteoporosis International.

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

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

[63]  W. Lorensen,et al.  Marching cubes: a high resolution 3D surface construction algorithm , 1998 .

[64]  William E. Lorensen,et al.  Marching cubes: A high resolution 3D surface construction algorithm , 1987, SIGGRAPH.