Abstract
Three-dimensional (3D) characterization of cortical porosity, most of which is under 100 µm in diameter, is usually confined to measurements made in 3–4 mm diameter cylinders of bone. We used micro-computed tomography (micro-CT) scanning of entire transaxial cross sections of human proximal femoral shafts (30–35 mm diameter) to quantify regional variation in porosity within the same scan. Complete, up to 10-mm-thick, transaxial slices of femoral upper shafts from 8 female cadavers were studied (n = 3 aged 29–37 years, n = 5 aged 72–90 years). Scanning was performed using high-resolution micro-CT (8.65 µm/voxel). Micro-CT volumes (10 × 10 × 5 mm) were selected via software in the anterior, medial and lateral regions. Images were segmented with voids appearing as 3D-interconnected canals. The percent void-to-tissue volume (Vo.V/TV) and the corresponding void surface area/TV were 86–309 % higher in older than younger subjects in anterior (p = 0.034), medial (p = 0.077), and lateral aspects (p = 0.034). Although not significant, void separation was reciprocally lower by 19–39 %, and void diameter was 65 % larger in older than younger subjects; void number tended to be 24–25 % higher medially and laterally but not anteriorly. For all specimens combined, medially there was higher Vo.V/TV and void surface area/TV than anteriorly (+48 %, p = 0.018; +33 %, p = 0.018) and laterally (+56 %, p = 0.062; +36 %, p = 0.043). There is regional heterogeneity in the 3D microarchitecture of the intracortical canals of the femoral shaft. The higher void volume in advanced age appears to be due to larger, rather than more, pores. However, creation of new canals from existing canals may contribute, depending on the location. High-resolution micro-computed tomography scanning of entire bone segments enables quantification of the 3D microanatomy of the intracortical void network at multiple locations.
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Zebaze RM, Ghasem-Zadeh A, Bohte A, Iuliano-Burns S, Mirams M, Price RI, Mackie EJ, Seeman E (2010) Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet 375:1729–1736
Thomas CD, Feik SA, Clement JG (2006) Increase in pore area, and not pore density, is the main determinant in the development of porosity in human cortical bone. J Anat 209:219–230
Chappard C, Bensalah S, Olivier C, Gouttenoire PJ, Marchadier A, Benhamou C, Peyrin F (2013) 3D characterization of pores in the cortical bone of human femur in the elderly at different locations as determined by synchrotron micro-computed tomography images. Osteoporos Int 24:1023–1033
Whiting WC, Zernicke RF (2008) Biomechanics of musculoskeletal injury. 2nd ed, Publisher: Human Kinetics, Champaign: chapter 3 basic biomechanics, material mechanics 80–92
Bell KL, Loveridge N, Power J, Garrahan N, Meggitt BF, Reeve J (1999) Regional differences in cortical porosity in the fractured femoral neck. Bone 24:57–64
McCalden RW, McGeough JA, Barker MB, Court-Brown CM (1993) Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg Am 75:1193–1205
Bala Y, Chapurlat R, Cheung AM, Felsenberg D, LaRoche M, Morris E, Reeve J, Thomas T, Zanchetta J, Bock O, Ghasem-Zadeh A, Djoumessi RM, Seeman E, Rizzoli R (2014) Risedronate slows or partly reverses cortical and trabecular microarchitectural deterioration in postmenopausal women. J Bone Miner Res 29:380–388
Perilli E, Parkinson IH, Reynolds KJ (2012) Micro-CT examination of human bone: from biopsies towards the entire organ. Ann Ist Super Sanita 48:75–82
Briggs AM, Perilli E, Parkinson IH, Wrigley TV, Fazzalari NL, Kantor S, Wark JD (2010) Novel assessment of subregional bone mineral density using DXA and pQCT and subregional microarchitecture using micro-CT in whole human vertebrae: applications, methods, and correspondence between technologies. J Clin Densitom 13:161–174
Perilli E, Briggs AM, Kantor S, Codrington J, Wark JD, Parkinson IH, Fazzalari NL (2012) Failure strength of human vertebrae: prediction using bone mineral density measured by DXA and bone volume by micro-CT. Bone 50:1416–1425
Cooper DM, Matyas JR, Katzenberg MA, Hallgrimsson B (2004) Comparison of microcomputed tomographic and microradiographic measurements of cortical bone porosity. Calcif Tissue Int 74:437–447
Cooper DM, Thomas CD, Clement JG, Turinsky AL, Sensen CW, Hallgrimsson B (2007) Age-dependent change in the 3D structure of cortical porosity at the human femoral midshaft. Bone 40:957–965
Donaldson FE, Pankaj P, Cooper DM, Thomas CD, Clement JG, Simpson AH (2011) Relating age and micro-architecture with apparent-level elastic constants: a micro-finite element study of female cortical bone from the anterior femoral midshaft. Proc Inst Mech Eng H 225:585–596
Dempster DW, Compston JE, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR, Parfitt AM (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 28:2–17
Ulrich D, van Rietbergen B, Laib A, Rüegsegger P (1999) The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25:55–60
Hildebrand T, Rüegsegger P (1997) A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc 185:67–75
Perilli E, Baruffaldi F, Bisi MC, Cristofolini L, Cappello A (2006) A physical phantom for the calibration of three-dimensional X-ray microtomography examination. J Microsc 222:124–134
Lorensen WE, Cline HE (1987) Marching cubes: a high resolution 3D surface construction algorithm. Comput Graph 21:163–169
Jordan GR, Loveridge N, Bell KL, Power J, Rushton N, Reeve J (2000) Spatial clustering of remodeling osteons in the femoral neck cortex: a cause of weakness in hip fracture? Bone 26:305–313
Cadet ER, Gafni RI, McCarthy EF, McCray DR, Bacher JD, Barnes KM, Baron J (2003) Mechanisms responsible for longitudinal growth of the cortex: coalescence of trabecular bone into cortical bone. J Bone Joint Surg Am 85-A:1739–1748
Atkins GJ, Findlay DM (2012) Osteocyte regulation of bone mineral: a little give and take. Osteoporos Int 23:2067–2079
Teti A, Zallone A (2009) Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone 44:11–16
Qing H, Ardeshirpour L, Pajevic PD, Dusevich V, Jahn K, Kato S, Wysolmerski J, Bonewald LF (2012) Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J Bone Miner Res 27:1018–1029
Stein MS, Feik SA, Thomas CD, Clement JG, Wark JD (1999) An automated analysis of intracortical porosity in human femoral bone across age. J Bone Miner Res 14:624–632
Martin RB, Pickett JC, Zinaich S (1980) Studies of skeletal remodeling in aging men. Clin Orthop Relat Res 149:268–282
Biewener AA (1991) Musculoskeletal design in relation to body size. J Biomech 24(Suppl 1):19–29
Lanyon LE (1992) The success and failure of the adaptive response to functional load-bearing in averting bone fracture. Bone 13(Suppl 2):S17–S21
Thomas CD, Feik SA, Clement JG (2005) Regional variation of intracortical porosity in the midshaft of the human femur: age and sex differences. J Anat 206:115–125
Feik SA, Thomas CD, Bruns R, Clement JG (2000) Regional variations in cortical modeling in the femoral mid-shaft: sex and age differences. Am J Phys Anthropol 112:191–205
Ostertag A, Peyrin F, Fernandez S, Laredo JD, de Vernejoul MC, Chappard C (2014) Cortical measurements of the tibia from high resolution peripheral quantitative computed tomography images: a comparison with synchrotron radiation micro-computed tomography. Bone 63:7–14
Bousson V, Peyrin F, Bergot C, Hausard M, Sautet A, Laredo JD (2004) Cortical bone in the human femoral neck: three-dimensional appearance and porosity using synchrotron radiation. J Bone Miner Res 19:794–801
Lieber RL (1990) Statistical significance and statistical power in hypothesis testing. J Orthop Res 8:304–309
Bousson V, Meunier A, Bergot C, Vicaut E, Rocha MA, Morais MH, Laval-Jeantet AM, Laredo JD (2001) Distribution of intracortical porosity in human midfemoral cortex by age and gender. J Bone Miner Res 16:1308–1317
Jowsey J (1960) Age changes in human bone. Clin Orthop Relat Res 38:210–217
Atkinson PJ (1965) Changes in resorption spaces in femoral cortical bone with age. J Pathol Bacteriol 89:173–178
Acknowledgments
Funding for this study was provided by Osteoporosis Australia/Australia New Zealand Bone and Mineral Society, Amgen-GSK Grants Program 2012.
Conflict of Interest
Egon Perilli, Yohann Bala, Roger Zebaze, Karen J Reynolds, and Ego Seeman declare that they have no conflict of interest.
Human and Animal Rights and Informed Consent
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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Perilli, E., Bala, Y., Zebaze, R. et al. Regional Heterogeneity in the Configuration of the Intracortical Canals of the Femoral Shaft. Calcif Tissue Int 97, 327–335 (2015). https://doi.org/10.1007/s00223-015-0014-5
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DOI: https://doi.org/10.1007/s00223-015-0014-5