3D osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-CT images

Bone

Volumn 60, Issue , 2014, Pages 172-185

  Dong, Pei ^a,b   Haupert, Sylvain ^c   Hesse, Bernhard ^a,b,d   Langer, Max ^a,b   Gouttenoire, Pierre Jean ^a,b   Bousson, Valérie ^e   Peyrin, Françoise ^a,b  

^a UNIVERSITÉ DE LYON   (France)

^b EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

3D image analysis; Cortical bone; Lacunar descriptors; Osteocyte lacunae; Synchrotron radiation micro CT

Indexed keywords

AGED; ARTICLE; BONE DENSITY; CONTROLLED STUDY; CORTICAL BONE; FEMALE; FEMUR; HUMAN; HUMAN CELL; HUMAN TISSUE; IMAGE ANALYSIS; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; OSTEOCYTE; POROSITY; REPRODUCIBILITY; SYNCHROTRON RADIATION; THREE DIMENSIONAL IMAGING; VERY ELDERLY;

3D IMAGE ANALYSIS; CORTICAL BONE; LACUNAR DESCRIPTORS; OSTEOCYTE LACUNAE; SYNCHROTRON RADIATION MICRO-CT;

AGED; AGED, 80 AND OVER; BONE MATRIX; FEMALE; FEMUR; HUMANS; IMAGING, THREE-DIMENSIONAL; OSTEOCYTES; POROSITY; REGRESSION ANALYSIS; SYNCHROTRONS; X-RAY MICROTOMOGRAPHY;

EID: 84891366112     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.12.008     Document Type: Article

References (53)

1. Ciarelli M.J., Goldstein S.A., Kuhn J.L., Cody D.D., Brown M.B. Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography. J Orthop Res 1991, 9:674-682.
2. Seeman E., Delmas P.D. Bone quality-the material and structural basis of bone strength and fragility. N Engl J Med 2006, 354:2250-2261.
3. Bonewald L.F. The amazing osteocyte. J Bone Miner Res 2011, 26:229-238.
4. Bonucci E. The osteocyte: the underestimated conductor of the bone orchestra. Rend Lincei 2009, 20:237-254.
5. Bonewald L.F., Johnson M.L. Osteocytes, mechanosensing and Wnt signaling. Bone 2008, 42:606-615.
6. Bonewald L.F. Mechanosensation and transduction in osteocytes. Bonekey Osteovision 2006, 3:7-15.
7. Burger E.H., Klein-Nulend J. Mechanotransduction in bone-role of the lacuno-canalicular network. FASEB J 1999, (13 Suppl.):S101-S112.
8. Westbroek I., De Rooij K.E., Nijweide P.J. Osteocyte-specific monoclonal antibody MAb OB7.3 is directed against Phex protein. J Bone Miner Res 2002, 17:845-853.
9. Qing H., Ardeshirpour L., Pajevic P.D., Dusevich V., Jähn K., Kato S., et al. Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J Bone Miner Res 2012, 27:1018-1029.
10. Bacabac R.G., Mizuno D., Schmidt C.F., MacKintosh F.C., Van Loon J.J.W.A., Klein-Nulend J., et al. Round versus flat: bone cell morphology, elasticity, and mechanosensing. J Biomech 2008, 41:1590-1598.
11. Mullins L.P., McGarry J.P., Bruzzi M.S., McHugh P.E. Micromechanical modelling of cortical bone. Comput Methods Biomech Biomed Engin 2007, 10:159-169.
12. Currey J.D. The many adaptations of bone. J Biomech 2003, 36:1487-1495.
13. Schneider P., Meier M., Wepf R., Müller R. Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network. Bone 2010, 47:848-858.
14. Hirose S., Li M., Kojima T., de Freitas P.H.L., Ubaidus S., Oda K., et al. A histological assessment on the distribution of the osteocytic lacunar canalicular system using silver staining. J Bone Miner Metab 2007, 25:374-382.
15. Sugawara Y., Kamioka H., Honjo T., Tezuka K., Takano-Yamamoto T. Three-dimensional reconstruction of chick calvarial osteocytes and their cell processes using confocal microscopy. Bone 2005, 36:877-883.
16. Van Hove R.P., Nolte P.A., Vatsa A., Semeins C.M., Salmon P.L., Smit T.H., et al. Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density-is there a role for mechanosensing?. Bone 2009, 45:321-329.
17. Boyde A., Jones S.J. Scanning electron microscopy of bone: instrument, specimen, and issues. Microsc Res Tech 1996, 33:92-120.
18. Okada S., Yoshida S., Ashrafi S.H., Schraufnagel D.E. The canalicular structure of compact bone in the rat at different ages. Microsc Microanal 2002, 8:104-115.
19. You L.D., Weinbaum S., Cowin S.C., Schaffler M.B. Ultrastructure of the osteocyte process and its pericellular matrix. Anat Rec A Discov Mol Cell Evol Biol 2004, 278:505-513.
20. Rubin M.A., Rubin J., Jasiuk I. SEM and TEM study of the hierarchical structure of C57BL/6J and C3H/HeJ mice trabecular bone. Bone 2004, 35:11-20.
21. Schneider P., Meier M., Wepf R., Müller R. Serial FIB/SEM imaging for quantitative 3D assessment of the osteocyte lacuno-canalicular network. Bone 2011, 49:304-311.
22. Dierolf M., Menzel A., Thibault P., Schneider P., Kewish C.M., Wepf R., et al. Ptychographic X-ray computed tomography at the nanoscale. Nature 2010, 467:436-439.
23. Vatsa A., Breuls R.G., Semeins C.M., Salmon P.L., Smit T.H., Klein-Nulend J. Osteocyte morphology in fibula and calvaria-is there a role for mechanosensing?. Bone 2008, 43:452-458.
24. Salomé M., Peyrin F., Cloetens P., Odet C., Laval-Jeantet A.M., Baruchel J., et al. A synchrotron radiation microtomography system for the analysis of trabecular bone samples. Med Phys 1999, 26:2194-2204.
25. Peyrin F., Salome M., Cloetens P., Laval-Jeantet A.M., Ritman E., Rüegsegger P. Micro-CT examinations of trabecular bone samples at different resolutions: 14, 7 and 2 micron level. Technol Health Care 1998, 6:391-401.
26. Hengsberger S., Enstroem J., Peyrin F., Zysset P. How is the indentation modulus of bone tissue related to its macroscopic elastic response? A validation study. J Biomech 2003, 36:1503-1509.
27. Hannah K.M., Thomas C.D.L., Clement J.G., De Carlo F., Peele A.G. Bimodal distribution of osteocyte lacunar size in the human femoral cortex as revealed by micro-CT. Bone 2010, 47:866-871.
28. Carter Y., Thomas C.D.L., Clement J.G., Peele A.G., Hannah K., Cooper D.M.L. Variation in osteocyte lacunar morphology and density in the human femur-a synchrotron radiation micro-CT study. Bone 2012, 52:126-132.
29. Marotti G. Osteocyte orientation in human lamellar bone and its relevance to the morphometry of periosteocytic lacunae. Metab Bone Dis Relat Res 1979, 1:325-333.
30. Mullender M.G., van der Meer D.D., Huiskes R., Lips P. Osteocyte density changes in aging and osteoporosis. Bone 1996, 18:109-113.
31. Skedros J.G., Grunander T.R., Hamrick M.W. Spatial distribution of osteocyte lacunae in equine radii and third metacarpals: considerations for cellular communication, microdamage detection and metabolism. Cells Tissues Organs 2005, 180:215-236. (Print).
32. Beno T., Yoon Y.-J., Cowin S.C., Fritton S.P. Estimation of bone permeability using accurate microstructural measurements. J Biomech 2006, 39:2378-2387.
33. McCreadie B.R., Hollister S.J., Schaffler M.B., Goldstein S.a Osteocyte lacuna size and shape in women with and without osteoporotic fracture. J Biomech 2004, 37:563-572.
34. Granke M., Grimal Q., Saïed A., Nauleau P., Peyrin F., Laugier P. Change in porosity is the major determinant of the variation of cortical bone elasticity at the millimeter scale in aged women. Bone 2011, 49:1020-1026.
35. Canny J. A computational approach to edge detection. IEEE Trans Pattern Anal Mach Intell 1986, PAMI-8:679-698.
36. Hoshen J., Kopelman R. Percolation and cluster distribution I. Cluster multiple labeling technique and critical concentration algorithm. Phys Rev B 1976, 14:3438.
37. Kerschnitzki M., Kollmannsberger P., Burghammer M., Duda G.N., Weinkamer R., Wagermaier W., et al. Architecture of the osteocyte network correlates with bone material quality. J Bone Miner Res 2013, 28:1837-1845.
38. Hildebrand T., Rüegsegger P. Quantification of bone microarchitecture with the structure model index. Comput Methods Biomech Biomed Engin 1997, 1:15-23.
39. Ohser J., Schladitz K. 3D images of materials structures: processing and analysis 2009, Wiley.
40. Ohser J., Nagel W., Schladitz K. The Euler number of discretized sets-on the choice of adjacency in homogeneous lattices. Morphology of condensed matter 2002, 275-298. Springer, Berlin Heidelberg. K. Mecke, D. Stoyan (Eds.).
41. Ohser J., Nagel W., Schladitz K. Miles formulae for Boolean models observed on lattices. Image Anal Stereol 2009, 28:77-92.
42. Schladitz K., Ohser J., Nagel W. Measuring intrinsic volumes in digital 3D images. Discrete geometry for computer imagery 2006, 247-258. Springer, Berlin Heidelberg. A. Kuba, L.G. Nyúl, K. Palágyi (Eds.).
43. Dice L.R. Measures of the amount of ecologic association between species. Ecology 1945, 26:297.
44. Müller R. Hierarchical microimaging of bone structure and function. Nat Rev Rheumatol 2009, 5:373-381.
45. Jones C.W., Smolinski D., Keogh A., Kirk T.B., Zheng M.H. Confocal laser scanning microscopy in orthopaedic research. Prog Histochem Cytochem 2005, 40:1-71.
46. Pacureanu A., Langer M., Boller E., Tafforeau P., Peyrin F. Nanoscale imaging of the bone cell network with synchrotron X-ray tomography: optimization of acquisition setup. Med Phys 2012, 39:2229-2238.
47. Langer M., Pacureanu A., Suhonen H., Grimal Q., Cloetens P., Peyrin F. X-ray phase nanotomography resolves the 3D human bone ultrastructure. PLoS One 2012, 7:e35691.
48. Shahar R., Lukas C., Papo S., Dunlop J.W.C., Weinkamer R. Characterization of the spatial arrangement of secondary osteons in the diaphysis of equine and canine long bones. Anat Rec (Hoboken) 2011, 294:1093-1102.
49. Teti A., Zallone A. Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone 2009, 44:11-16.
50. Power J., Noble B.S., Loveridge N., Bell K.L., Rushton N., Reeve J. Osteocyte lacunar occupancy in the femoral neck cortex: an association with cortical remodeling in hip fracture cases and controls. Calcif Tissue Int 2001, 69:13-19.
51. Vashishth D., Gibson G., Kimura J., Schaffler M.B., Fyhrie D.P. Determination of bone volume by osteocyte population. Anat Rec 2002, 267:292-295.
52. Vashishth D., Verborgt O., Divine G., Schaffler M.B., Fyhrie D.P. Decline in osteocyte lacunar density in human cortical bone is associated with accumulation of microcracks with age. Bone 2000, 26:375-380.
53. Currey J.D., Shahar R. Cavities in the compact bone in tetrapods and fish and their effect on mechanical properties. J Struct Biol 2013, 183:107-122.