Three-dimensional microcomputed tomography imaging of basic multicellular unit-related resorption spaces in human cortical bone.

This study employed microcomputed tomography (micro-CT) as a novel means for visualizing the morphology and quantifying the range (length) of basic multicellular unit (BMU)-related resorption spaces in human cortical bone. We tested the hypotheses that the density and range of spaces vary with age and sex. The sample included 82 human (18-92 years) anterior femoral midshaft samples. The morphology of the spaces (n = 99) was varied, including unidirectional, bidirectional, branched, and even highly clustered forms. The density of resorption spaces was negatively correlated with age for the combined sexes and females, with Spearman's rho values of -0.355 (P < 0.001) and -0.522 (P = 0.002), respectively. The density of spaces did not differ significantly between the sexes (P = 0.735). Mean range +/- SD for the combined sexes, females, and males was 2,706 +/- 1,177, 2,681 +/- 1,247, and 2,718 +/- 1,150 microm, respectively. Numerical simulation of the effect of the 7,000 microm scan field of view suggested that the actual mean range of the spaces for the pooled sample was actually on the order of 3,770 microm. Range did not correlate significantly with age for the combined sexes (P = 0.587) or females (P = 0.345) and males (P = 0.896) considered separately and was not significantly different (P = 0.883) between the sexes. These results suggest that the range of BMUs is not affected by age. The age-dependent decrease in resorption space density for the females and pooled sexes was most likely a consequence of cortical rarefaction, leading to difficulty detecting resorption spaces with micro-CT, rather than a decrease in overall remodeling activity.

[1]  A. Robling,et al.  Morphology of the Drifting Osteon , 1999, Cells Tissues Organs.

[2]  Theo H Smit,et al.  Strain-derived canalicular fluid flow regulates osteoclast activity in a remodelling osteon--a proposal. , 2003, Journal of biomechanics.

[3]  T. Smit,et al.  Is BMU‐Coupling a Strain‐Regulated Phenomenon? A Finite Element Analysis , 2000, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[4]  Three-dimensional reconstruction of Haversian systems in ovine compact bone. , 2002, European journal of morphology.

[5]  M. Hahn,et al.  High Spatial Resolution Imaging of Bone Mineral Using Computed Microtomography: Comparison with Microradiography and Undecalcified Histologic Sections , 1993, Investigative radiology.

[6]  L. Harsányi Differential Diagnosis of Human and Animal Bone , 1993 .

[7]  J. Currey Differences in the Blood-Supply of Bone of Different Histological Types , 1960 .

[8]  L. Claes,et al.  Prediction of strength of cortical bone in vitro by microcomputed tomography. , 2001, Clinical biomechanics.

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

[10]  Z. Jaworski,et al.  The rate of osteoclastic bone erosion in Haversian remodeling sites of adult dog's rib , 2005, Calcified Tissue Research.

[11]  Andrei L. Turinsky,et al.  Quantitative 3D analysis of the canal network in cortical bone by micro-computed tomography. , 2003, Anatomical record. Part B, New anatomist.

[12]  D. Simmons Options for bone aging with the microscope , 1985 .

[13]  R. Amprino A contribution to the functional meaning of the substitution of primary by secondary bone tissue. , 1948, Acta anatomica.

[14]  D. Enlow,et al.  A comparative histological study of fossil and recent bone tissues. Part III. , 1957 .

[15]  J. Jowsey Studies of Haversian systems in man and some animals. , 1966, Journal of anatomy.

[16]  R. Martin On the histologic measurement of osteonal BMU activation frequency. , 1994, Bone.

[17]  M. Boon,et al.  4D confocal microscopy for visualisation of bone remodelling. , 1996, Pathology, research and practice.

[18]  W. Enneking,et al.  Temporal and spatial activity in mirror segments of mature dog fibulae , 2005, Calcified Tissue Research.

[19]  Z. Jaworski,et al.  Observations on two types of resorption cavities in human lamellar cortical bone. , 1972, Clinical orthopaedics and related research.

[20]  J. Reeve,et al.  A novel mechanism for induction of increased cortical porosity in cases of intracapsular hip fracture. , 2000, Bone.

[21]  A. Beddoe Measurements of the microscopic structure of cortical bone. , 1977, Physics in medicine and biology.

[22]  D. Ubelaker,et al.  Differences in osteon banding between human and nonhuman bone. , 2001, Journal of forensic sciences.

[23]  E. A. Tonna,et al.  A comparative histological study of mammalian bone , 1974, Journal of morphology.

[24]  R. Martin,et al.  Is all cortical bone remodeling initiated by microdamage? , 2002, Bone.

[25]  S Pfeiffer,et al.  Variability in osteon size in recent human populations. , 1998, American journal of physical anthropology.

[26]  N. Tappen Three-dimensional studies on resorption spaces and developing osteons. , 1977, The American journal of anatomy.

[27]  Theo H Smit,et al.  A Case for Strain‐Induced Fluid Flow as a Regulator of BMU‐Coupling and Osteonal Alignment , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[28]  G. Marotti,et al.  Changes in the vascular network during the formation of Haversian systems. , 1980, Acta anatomica.

[29]  Microscopic metabolism of calcium in bone. I. Three-dimensional deposition of Ca45 in canine osteons. , 1959, Radiation research.

[30]  S. Teitelbaum,et al.  Bone resorption by osteoclasts. , 2000, Science.

[31]  J. Cohen,et al.  The three-dimensional anatomy of haversian systems. , 1958, The Journal of bone and joint surgery. American volume.

[32]  A. Ricqlès Some Remarks on Palaeohistology from a Comparative Evolutionary Point of View , 1993 .

[33]  N Loveridge,et al.  Super‐osteons (remodeling clusters) in the cortex of the femoral shaft: Influence of age and gender , 2001, The Anatomical record.

[34]  L. Claes,et al.  Prediction of cortical bone porosityIn Vitro by microcomputed tomography , 2007, Calcified Tissue International.

[35]  A. Parfitt Osteonal and hemi‐osteonal remodeling: The spatial and temporal framework for signal traffic in adult human bone , 1994, Journal of cellular biochemistry.

[36]  A. Mace Sample-Size Determination. , 1964 .

[37]  F. Vasciaveo,et al.  Vascular channels and resorption cavities in the long bone cortex. The bovine bone. , 1961, Acta anatomica.

[38]  B. Hallgrímsson,et al.  Comparison of Microcomputed Tomographic and Microradiographic Measurements of Cortical Bone Porosity , 2004, Calcified Tissue International.

[39]  Dietmar W Hutmacher,et al.  Analysis of 3D bone ingrowth into polymer scaffolds via micro-computed tomography imaging. , 2004, Biomaterials.

[40]  Françoise Peyrin,et al.  Cortical Bone in the Human Femoral Neck: Three‐Dimensional Appearance and Porosity Using Synchrotron Radiation , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[41]  H. Frost Tetracycline-based histological analysis of bone remodeling , 2005, Calcified Tissue Research.

[42]  N. Rushton,et al.  Osteoclastic cortical erosion as a determinant of subperiosteal osteoblastic bone formation in the femoral neck’s response to BMU imbalance. Effects of stance-related loading and hip fracture , 2005, Osteoporosis International.

[43]  Kentaro Uesugi,et al.  Monochromatic synchrotron radiation muCT reveals disuse-mediated canal network rarefaction in cortical bone of growing rat tibiae. , 2006, Journal of applied physiology.

[44]  W. T. Dempster,et al.  Patterns of vascular channels in the cortex of the human mandible , 1959, The Anatomical record.

[45]  H. Gruber,et al.  Vertebral Endplate Architecture and Vascularization: Application of Micro-Computerized Tomography, a Vascular Tracer, and Immunocytochemistry in Analyses of Disc Degeneration in the Aging Sand Rat , 2005, Spine.