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Interindividual and intraspecimen variability of 3-D bone microarchitectural parameters in iliac crest biopsies imaged by conventional micro-computed tomography

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Abstract

Bone microarchitecture of the iliac bone is used to characterize the properties of bone tissue in osteoporosis, particularly in pharmacological studies. Trabecular bone is known to be heterogeneous media. For a few years, the analysis of three-dimensional (3-D) bone microarchitecture has been based on micro-computed tomography (micro-CT). To assess the interindividual variability (inter-indVar) and the intrasample variability (intra-sampVar) of iliac crest biopsies, we used a Bordier needle trephine in 35 postmenopausal female cadavers (mean age, 74.4 ± 10.4 years). Finally, we had at our disposal 32 individual iliac crests to assess the inter-indVar and 21 oriented specimens to assess the intra-sampVar. All the samples were chemically defatted, and the images were performed with a desktop micro-CT with a voxel size of 10.77 μm. We measured trabecular bone parameters: bone volume/tissue volume (BV/TV %), trabecular thickness and spacing (Tb. Th*, Tb.Sp* μm), bone surface/bone volume (BS/BV, 1/mm), the trabecular number (Tb.N, 1/mm), structure model index (SMI), trabecular pattern factor (Tb.Pf), and degree of anisotropy (DA). We also measured cortical bone parameters: cortical thickness (Cort.Th), porosity (PoV/TV), and pore diameter (Po.Dm). For the inter-indVar, we analyzed a fixed volume of interest corresponding to 119.8 mm3 centered on each iliac crest. To assess the intra-sampVar, we divided the whole trabecular volume into three equal height parts (external, middle, internal). BV/TV, Tb.N, and PoV/TV were negatively correlated with age and Tb.Sp* and SMI were positively correlated. The mean difference of absolute individual variations in percentage with the middle area used as a reference, comparatively to external and internal areas, ranged from 6.6% (Tb.Sp*) to 27.8% (BV/TV), except Tb.Pf, which showed large variability. There was no difference between external and internal areas, with a tendency for lower values of BV/TV, Tb.Th*, and Tb.N in the middle of the iliac crest and higher values of Tb.Sp* and BS/BV. The evaluation of bone microarchitecture of iliac crest samples on micro-CT images is reliable. The heterogeneity of bone inside the iliac crest is noticeable as leading to analyzing the largest possible quantity of bone, with standardized location, according to cortex but without any assumption of orientation.

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References

  1. NIH Consensus (2000) Osteoporosis prevention, diagnosis, and therapy. NIH Consensus Statement 17:1–45

    Google Scholar 

  2. Parfitt AM, Mathews CH, Villanueva AR, Kleerekoper M, Frame B, Rao DS (1983) 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. J Clin Invest 72:1396–1409

    Article  PubMed  CAS  Google Scholar 

  3. Aaron JE, Makins NB, Sagreiya K (1987) The microanatomy of trabecular bone loss in normal aging men and women. Clin Orthop Relat Res 215:260–271

    PubMed  Google Scholar 

  4. Podenphant J, Gotfredsen A, Nilas L, Norgaard H, Braendstrup O (1986) Iliac crest biopsy: representativity for the amount of mineralized bone. Bone (NY) 76:427–430

    Google Scholar 

  5. Mosekilde L, Viidik A, Mosekilde L (1985) Correlation between the compressive strength of iliac and vertebral trabecular bone in normal individuals. Bone (NY) 65:291–295

    Google Scholar 

  6. Oleksik A, Ott SM, Vedi S, Bravenboer N, Compston J, Lips P (2000) Bone structure in patients with low bone mineral density with or without vertebral fractures. J Bone Miner Res 15: 1368–1375

    Article  PubMed  CAS  Google Scholar 

  7. Dalle Carbonare L, Arlot ME, Chavassieux PM, Roux JP, Portero NR, Meunier PJ (2001) Comparison of trabecular bone microarchitecture and remodeling in glucocorticoid-induced and postmenopausal osteoporosis. J Bone Miner Res 16:97–103

    Article  CAS  Google Scholar 

  8. Chappard D, Legrand E, Basle MF, Fromont P, Racineux JL, Rebel A, Audran M (1996) Altered trabecular architecture induced by corticosteroids: a bone histomorphometric study. J Bone Miner Res 1:676–685

    Google Scholar 

  9. Parisien M, Cosman F, Mellish RW, Schnitzer M, Nieves J, Silverberg SJ, Shane E, Kimmel D, Recker RR, Bilezikian JP (1995) Bone structure in postmenopausal hyperparathyroid, osteoporotic, and normal women. J Bone Miner Res 10:1393–1399

    PubMed  CAS  Google Scholar 

  10. Eriksen EF, Melsen F, Sod E, Barton I, Chines A (2002) Effects of long-term risedronate on bone quality and bone turnover in women with postmenopausal osteoporosis. Bone (NY) 31:620–625

    CAS  Google Scholar 

  11. Dufresne TE, Chmielewski PA, Manhart MD, Johnson TD, Borah B (2003) Risedronate preserves bone architecture in early postmenopausal women in 1 year as measured by three-dimensional microcomputed tomography. Calcif Tissue Int 73:423–432

    Article  PubMed  CAS  Google Scholar 

  12. Borah B, Dufresne TE, Chmielewski PA, Johnson TD, Chines A, Manhart MD (2004) Risedronate preserves bone architecture in postmenopausal women with osteoporosis as measured by three-dimensional microcomputed tomography. Bone (NY) 34:736–746

    CAS  Google Scholar 

  13. Jiang Y, Zhao JJ, Mitlak BH, Wang O, Genant HK, Eriksen EF (2003) Recombinant human parathyroid hormone (1–34) [teriparatide] improves both cortical and cancellous bone structure. J Bone Miner Res 18:1932–1941

    Article  PubMed  CAS  Google Scholar 

  14. Muller R, Koller B, Hildebrand T, Laib A, Gionollini S, Rüegsegger P (1996) Resolution dependency of microstructural properties of cancellous bone based on three dimensional μ-tomography. Technol Health Care 4:113–119

    PubMed  CAS  Google Scholar 

  15. Peyrin F, Salome M, Cloetens P, Laval-Jeantet AM, Ritman E, Ruegsegger P (1998) MicroCT examinations of trabecular bone samples at different resolutions: 14, 7 and 2 micron level Technol Health Care 6:391–401

    PubMed  CAS  Google Scholar 

  16. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595–610

    Article  PubMed  CAS  Google Scholar 

  17. Serra J (1982) Image Analysis and Mathematical Morphology. Academic Press, New York, p 104

    Google Scholar 

  18. Muller R, Van Campenhout H, Van Damme B, Van Der Perre G, Dequeker J, Hildebrand T, Ruegsegger P (1998) Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and microcomputed tomography. Bone (NY) 23:59–66

    CAS  Google Scholar 

  19. Chappard D, Retailleau-Gaborit N, Legrand E, Basle MF, Audran M (2005) Comparison insight bone measurements by histomorphometry and microCT. J Bone Miner Res 20:1177–1184

    Article  PubMed  Google Scholar 

  20. Muller R (2003) Bone microarchitecture assessment: current and future trends. Osteoporos Int 14(suppl 5):89–99

    Article  Google Scholar 

  21. van Rietbergen B, Majumdar S, Pistoia W, Newitt DC, Kothari M, Laib A, Ruegsegger P (1998) Assessment of cancellous bone mechanical properties from micro-FE models based on micro-CT, pQCT and MR images. Technol Health Care 6:413–420

    PubMed  Google Scholar 

  22. Uchiyama T, Tanizawa T, Muramatsu H, Endo N, Takahashi HE, Hara T (1999) Three-dimensional microstructural analysis of human trabecular bone in relation to its mechanical properties. Bone (NY) 25:487–491

    CAS  Google Scholar 

  23. Recker R, Masarachia P, Santora A, Howard T, Chavassieux P, Arlot M, Rodan G, Wehren L, Kimmel D (2005) Trabecular bone microarchitecture after alendronate treatment of osteoporotic women. Curr Med Res Opin. 21:185–194. Erratum in: Curr Med Res Opin 21:324

    Article  PubMed  CAS  Google Scholar 

  24. Dempster DW, Cosman F, Kurland ES, Zhou H, Nieves J, Woelfert L, Shane E, Plavetic K, Muller R, Bilezikian J, Lindsay R (2001) Effects of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis: a paired biopsy study. J Bone Miner Res 16:1846–1853

    Article  PubMed  CAS  Google Scholar 

  25. Amling M, Herden S, Posl M, Hahn M, Ritzel H, Delling G (1996) Heterogeneity of the skeleton: comparison of the trabecular microarchitecture of the spine, the iliac crest, the femur, and the calcaneus. J Bone Miner Res 11:36–4

    PubMed  CAS  Google Scholar 

  26. Parisien MV, McMahon D, Pushparaj N, Dempster DW (1988) Trabecular architecture in iliac crest bone biopsies: infra-individual variability in structural parameters and changes with age. Bone (NY) 9:289–295

    CAS  Google Scholar 

  27. Podenphant J, Gotfredsen A, Nilas L, Norgard H, Braendstrup O, Christiansen C (1986) Iliac crest biopsy: an investigation on certain aspects of precision and accuracy. Bone Miner 1:279–287

    PubMed  CAS  Google Scholar 

  28. Chappard C, Basillais A, Benhamou L, Bonassie A, Brunet-Imbault B, Bonnet N, Peyrin F (2006) Comparison of synchrotron radiation and conventional x-ray microcomputed tomography for assessing trabecular bone microarchitecture of human femoral heads. Med Phys 33:3568–3577

    Article  PubMed  Google Scholar 

  29. Lorensen WE, Cline HE (1987) Marching cubes: a high resolution 3D surface construction algorithm. Computer Graphics 21(suppl 1):7–12

    Google Scholar 

  30. Ulrich D, Van Rietbergen B, Laib A, Ruegsegger P (1999) The ability of three dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone (NY) 25:55–60

    CAS  Google Scholar 

  31. Hildebrand T, Rüegsegger P (1997) A new method for the model independent assessment of thickness in three dimensional images. J Microsc 185:67–75

    Article  Google Scholar 

  32. Whitehouse WJ (1974) The quantitative morphology of anisotropic trabecular bone. J Microsc 101:153–156

    PubMed  CAS  Google Scholar 

  33. Hildebrand T, Rüegsegger P (1997) Quantification of bone microarchitecture with the structure model index. Comput Methods Biomech Biomed Eng 1:15–23

    Article  Google Scholar 

  34. Hahn M, Vogel M, Pompesius-Kempa M, Delling G (1992) Trabecular bone pattern factor: a new parameter for simple quantification of bone microarchitecture. Bone (NY) 13:327–330

    CAS  Google Scholar 

  35. Dufresne T (1998) Segmentation techniques for analysis of bone by three-dimensional computed tomographic imaging. Technol Health Care 6:351–359

    PubMed  CAS  Google Scholar 

  36. Basillais A, Bensamoun S, Chappard C, Brunet-Imbault B, Lemineur G III, Ilharreborde B, Ho Ba Tho MC, Benhamou CL (2007) Three dimensional characterization of cortical bone microstructure by micro-computed tomography: validation with ultrasound and microscopic measurements. J Orthop Sci 12:141–148

    Article  PubMed  Google Scholar 

  37. Gluer CC, Blake G, Lu Y, Blunt BA, Jergas M, Genant HK (1995) Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques. Osteoporos Int 5:262–270

    Article  PubMed  CAS  Google Scholar 

  38. Akhter MP, Lappe JM, Davies KM, Recker RR (2007) Transmenopausal changes in the trabecular bone structure. Bone (NY) 41:111–116

    CAS  Google Scholar 

  39. Kim DG, Christopherson GT, Dong XN, Fyhrie DP, Yeni YN (2004) The effect of microcomputed tomography scanning and reconstruction voxel size on the accuracy of stereological measurements in human cancellous bone. Bone (NY) 35:1375–1382

    Google Scholar 

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Authors and Affiliations

  1. U658, Inserm, CHRO 1 rue porte Madeleine, Orleans, 45000, France

    Christine Chappard, Arnaud Marchadier & Laurent Benhamou

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  1. Christine Chappard
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  2. Arnaud Marchadier
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  3. Laurent Benhamou
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Correspondence to Christine Chappard.

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Chappard, C., Marchadier, A. & Benhamou, L. Interindividual and intraspecimen variability of 3-D bone microarchitectural parameters in iliac crest biopsies imaged by conventional micro-computed tomography. J Bone Miner Metab 26, 506–513 (2008). https://doi.org/10.1007/s00774-008-0856-2

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  • DOI: https://doi.org/10.1007/s00774-008-0856-2

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