A quantitative framework for the 3D characterization of the osteocyte lacunar system

Bone

Volumn 57, Issue 1, 2013, Pages 142-154

  Mader, Kevin Scott ^a,b   Schneider, Philipp ^c   Müller, Ralph ^c   Stampanoni, Marco ^a,b  

^a PAUL SCHERRER INSTITUTE   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c ETH ZURICH   (Switzerland)

Author keywords

3D morphology; Cell alignment; Cell distribution; Cell shape; Cortical bone; Osteocyte lacunae

Indexed keywords

GROWTH HORMONE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE REMODELING; BONE STRUCTURE; BONE TISSUE; CELL SHAPE; COMPUTER ASSISTED TOMOGRAPHY; COMPUTER MODEL; CONFOCAL LASER MICROSCOPY; CORTICAL BONE; HORMONE ACTION; IMAGE QUALITY; MORPHOMETRICS; MOUSE; NONHUMAN; OSTEOCYTE; OSTEOCYTE LACUNAE; QUANTITATIVE ANALYSIS; STRAIN DIFFERENCE; STRUCTURE ACTIVITY RELATION; SYNCHROTRON RADIATION; THREE DIMENSIONAL IMAGING; TISSUE CHARACTERIZATION; VALIDATION PROCESS;

3D MORPHOLOGY; CELL ALIGNMENT; CELL DISTRIBUTION; CELL SHAPE; CORTICAL BONE; OSTEOCYTE LACUNAE;

ANIMALS; GROWTH HORMONE; MICE; MODELS, THEORETICAL; OSTEOCYTES;

EID: 84883013286     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.06.026     Document Type: Article

References (71)

1. Statistical analysis used in a quantitative framework for the 3D characterization of the osteocyte lacunar system 2013.
2. Ascenzi M.-G., Gill J., Lomovtsev A. Orientation of collagen at the osteocyte lacunae in human secondary osteons. J Biomech Dec. 2008, 41(16):3426-3435.
3. Asipauskas M., Aubouy M., Glazier J.A., Graner F., Jiang Y. A texture tensor to quantify deformations: the example of two-dimensional flowing foams. Granul Matter July 2003, 5(2):71-74.
4. Beno T., Yoon Y.-J., Cowin S.C., Fritton S.P. Estimation of bone permeability using accurate microstructural measurements. J Biomech Jan. 2006, 39(13):2378-2387.
5. Blatov V.A. Voronoi-dirichlet polyhedra in crystal chemistry: theory and applications. Crystallogr Rev 2004, 10(4):249-318.
6. Bouxsein M.L., Boyd S.K., Christiansen B.A., Guldberg R.E., Jepsen K.J., Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res June 2010, 25(7):1468-1486.
7. Britz H.M., Carter Y., Jokihaara J., Leppänen O.V., Järvinen T.L.N., Belev G., et al. Prolonged unloading in growing rats reduces cortical osteocyte lacunar density and volume in the distal tibia. Bone Dec. 2012, 51(5):913-919.
8. Brostow W., Chybicki M., Laskowski R., Rybicki J. Voronoi polyhedra and Delaunay simplexes in the structural analysis of molecular-dynamics-simulated materials. Phys Rev B June 1998, 57(21):13448-13458.
9. Canè V., Marotti G., Volpi G., Zaffe D., Palazzini S., Remaggi F., et al. Size and density of osteocyte lacunae in different regions of long bones. Calcif Tissue Int Dec. 1982, 34(1):558-563.
10. 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 Oct. 2012, 52(1):126-132.
11. Dale M., Fortin M.-J. From graphs to spatial graphs. Annu Rev Ecol Evol Syst Dec. 2010, 41(1):21-38.
12. Dinis L., Natal Jorge R., Belinha J. Analysis of plates and laminates using the natural neighbour radial point interpolation method. Eng Anal Bound Elem Mar. 2008, 32(3):267-279.
13. Dinis L., Nataljorge R., Belinha J. Analysis of 3D solids using the natural neighbour radial point interpolation method. Comput Methods Appl Mech Eng Mar. 2007, 196(13-16):2009-2028.
14. Donahue L.R., Guido V.E., Rosen C.J., Horton L.G., Ackert-Bicknell C.L., Bouxsein M.L., et al. GH/IGF-I independent genetic effects on BMD and skeletal morphology are both gender dependent and independent. J Bone Miner Res 2003, 18.
15. Doube M., Kłosowski M.M., Arganda-Carreras I., Cordelières F.P., Dougherty R.P., Jackson J.S., et al. BoneJ: free and extensible bone image analysis in ImageJ. Bone Sept. 2010, 47:1076-1079.
16. Dougherty W. Oriented spermatozoa in the spermatophore of the palaemonid shrimp, Macrobrachium rosenbergii. Tissue Cell 1987, 19(1):7.
17. Du Q., Faber V., Gunzburger M. Centroidal Voronoi tessellations: applications and algorithms. Soc Ind Appl Math Rev 1999, 41(4):637-676.
18. Duyckaerts C., Godefroy G. Voronoi tessellation to study the numerical density and the spatial distribution of neurones. J Chem Neuroanat Oct. 2000, 20(1):83-92.
19. Ghosh S. Quantitative characterization and modeling of composite microstructures by Voronoi cells. Acta Mater June 1997, 45(6):2215-2234.
20. Graner F., Dollet B., Raufaste C., Marmottant P. Discrete rearranging disordered patterns, part I: robust statistical tools in two or three dimensions. Eur Phys J E Soft Matter Apr. 2008, 25(4):349-369.
21. 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 Nov. 2010, 47(5):866-871.
22. Hirose S., Li M., Kojima T. A histological assessment on the distribution of the osteocytic lacunar canalicular system using silver staining. J Bone Miner Metab 2007, 25(6):374-382.
23. Ionova-Martin S.S., Wade J.M., Tang S., Shahnazari M., Ager J.W., Lane N.E., et al. Changes in cortical bone response to high-fat diet from adolescence to adulthood in mice. Osteoporos Int 2010, 22:2283-2293.
24. James D.A., Debroy S. RMySQL: R interface to the MySQL database 2012.
25. 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, 8:1837-1845.
26. Kerschnitzki M., Wagermaier W., Roschger P., Seto J., Shahar R., Duda G.N., et al. The organization of the osteocyte network mirrors the extracellular matrix orientation in bone. J Struct Biol Feb. 2011, 173(2):303-311.
27. Klein-Nulend J., Burger E.H., Semeins C.M., Raisz L.G., Pilbeam C.C. Pulsating fluid flow stimulates prostaglandin release and inducible prostaglandin G/H synthase mRNA expression in primary mouse bone cells. J Bone Miner Res Jan. 1997, 12(1):45-51.
28. Klein-Nulend J., Nijweide P.J., Burger E.H. Osteocyte and bone structure. Curr Osteoporos Rep June 2003, 1(1). [5-10-10].
29. Klein-Nulend J., Van Der Plas A., Semeins C., Ajubi N., Frangos J., Nijweide P., et al. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J 1995, 9(5):441-445.
30. Kneissel M. The rise of osteocyte biology continues Meeting Report from the 32nd Annual Meeting of the American Society for Bone and Mineral Research: October 15-19, 2010. Tech. rep 2011.
31. Knothe M.L., Adamson J.R., Tami A.E., Bauer T.W. The osteocyte. Cell 2004, 36:1-8.
32. Kubitscheck U., Wedekind P., Zeidler O., Grote M., Peters R. Single nuclear pores visualized by confocal microscopy and image processing. Biophys J May 1996, 70(5):2067-2077.
33. Langer M., Pacureanu A., Suhonen H., Grimal Q., Cloetens P., Peyrin F. X-ray phase nanotomography resolves the 3D human bone ultrastructure. PLoS One Jan. 2012, 7(8):e35691.
34. Lucarini V. Three-dimensional random Voronoi tessellations: from cubic crystal lattices to Poisson point processes. J Stat Phys Jan. 2009, 134(1):185-206.
35. Mader K., Marone F., Mikuljan G., Isenegger A., Stampanoni M. High-throughput, fully-automatic, synchrotron-based microscopy station at TOMCAT. J Synchrotron Radiat 2011, 18(2):117-124.
36. Marmottant P., Raufaste C., Graner F. Discrete rearranging disordered patterns, part II: 2D plasticity, elasticity and flow of a foam. Eur Phys J E Soft Matter Apr. 2008, 25(4):371-384.
37. Matthews B.J., Kim M.E., Flanagan J.J., Hattori D., Clemens J.C., Zipursky S.L., et al. Dendrite self-avoidance is controlled by Dscam. Cell May 2007, 129(3):593-604.
38. Mayhew T.M. Quantitative description of the spatial arrangement of organelles in a polarised secretory epithelial cell: the salivary gland acinar cell. J Anat Feb. 1999, 194(Pt 2):279-285.
39. Mccreadie B. Osteocyte lacuna size and shape in women with and without osteoporotic fracture. J Biomech Apr. 2004, 37(4):563-572.
40. Morin A., Urban J., Adams P.D., Foster I., Sali A., Baker D., et al. Research priorities. Shining light into black boxes. Science Apr. 2012, 336(6078):159-160.
41. Pacureanu A., Larrue A., Langer M., Olivier C., Muller C., Lafage-Proust M.-H., et al. Adaptive filtering for enhancement of the osteocyte cell network in 3D microtomography images. IRBM Feb. 2013, 34(1):48-52.
42. Palanza L., Jhaveri S., Donati S., Nuzzi R., Vercelli A. Quantitative spatial analysis of the distribution of NADPH-diaphorase-positive neurons in the developing and mature rat retina. Brain Res Bull Apr. 2005, 65(4):349-360.
43. Parfitt A.M., Drezner M.K., Glorieux F.H., Kanis J.A., Malluche H., Meunier P.J., et al. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res Dec. 1987, 2(6):595-610.
44. Peng R.D. Reproducible research in computational science. Science Dec. 2011, 334(6060):1226-1227.
45. Philippe T., De Geuser F., Duguay S., Lefebvre W., Cojocaru-Mirédin O., Da Costa G., et al. Clustering and nearest neighbour distances in atom-probe tomography. Ultramicroscopy Sept. 2009, 109(10):1304-1309.
46. Power J., Loveridge N., Rushton N., Parker M., Reeve J. Osteocyte density in aging subjects is enhanced in bone adjacent to remodeling haversian systems. Bone 2002, 30(6):859-865.
47. Qiu S., Rao D., Palnitkar S., Parfitt A. Age and distance from the surface but not menopause reduce osteocyte density in human cancellous bone. Bone 2002, 31(2):313-318.
48. Raufaste C., Marmottant P., Graner F. Discrete rearranging disordered patterns: prediction of elastic and plastic behavior, and application to two-dimensional foams. Phys Rev E Mar. 2010, 81(3).
49. Remaggi F., Canè V., Palumbo C., Ferretti M. Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. I. Woven-fibered and parallel-fibered bones. Ital J Anat Embryol 1998, 103(4):145-155.
50. Resasco D.C., Gao F., Morgan F., Novak I.L., Schaff J.C., Slepchenko B.M. Virtual Cell: computational tools for modeling in cell biology. Wiley Interdiscip Rev Syst Biol Med 2012, 4(2):129-140.
51. Handbook of computational geometry 1999, Elsevier. 1st ed. J. Sack, J. Urrutia (Eds.).
52. Schneider P., Meier M., Wepf R., Müller R. Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network. Bone Nov. 2010, 47(5):848-858.
53. Schneider P., Stauber M., Voide R., Stampanoni M., Donahue L.R., Müller R. Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and nano-CT. J Bone Miner Res 2007, 22(10):1557-1570.
54. Schneider P., Voide R., Stampanoni M., Donahue L., Müller R. The importance of the intracortical microstructure for bone mechanics. Bone Cond 2012, 53:120-128.
55. Schwarz H., Exner H.E. The characterization of the arrangement of feature centroids in planes and volumes. J Microsc Feb. 1983, 129(2):155-169.
56. Singth R.K., Tropsha A., Vaisman I.I. Delaunay tessellation of proteins: four body nearest-neighbor propensities of amino acid residues. J Comput Biol Jan. 1996, 3(2):213-221.
57. Smith-Spangler C.M. Transparency and reproducible research in modeling: why we need it and how to get there. Med Decis Making Jan. 2012, 32(5):663-666.
58. Steffen B., Seyfried A. Methods for measuring pedestrian density, flow, speed and direction with minimal scatter. Physica A Nov. 2009, 16.
59. Subirana I., Sanz H., Vila J. compareGroups: descriptives by groups 2012.
60. Sugawara Y., Kamioka H., Honjo T., Tezuka K.-i, Takano-Yamamoto T. Three-dimensional reconstruction of chick calvarial osteocytes and their cell processes using confocal microscopy. Bone May 2005, 36(5):877-883.
61. R Core Team a language and environment for statistical computing 2013, R Foundation for Statistical Computing, Vienna, Austria.
62. Teti A., Zallone A. Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone Jan. 2009, 44(1):11-16.
63. Truskett T., Torquato S., Debenedetti P. Towards a quantification of disorder in materials: distinguishing equilibrium and glassy sphere packings. Phys Rev E July 2000, 62(1):993-1001.
64. Turner C.H., Forwood M.R. What role does the osteocyte network play in bone adaptation?. Bone Mar. 1995, 16(3):283-285.
65. 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 Aug. 2009, 45(2):321-329.
66. Vasilić B., Rajapakse C.S., Wehrli F.W. Classification of trabeculae into three-dimensional rodlike and platelike structures via local inertial anisotropy. Med Phys July 2009, 36(7):3280-3291.
67. 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 Sept. 2008, 43(3):452-458.
68. Wickham H. ggplot2: elegant graphics for data analysis 2009, Springer, New York.
69. Wickham H. The split-apply-combine strategy for data analysis. J Stat Softw 2011, 40(1):1-29.
70. Yang R., Zou R., Yu A. Voronoi tessellation of the packing of fine uniform spheres. Phys Rev E Apr. 2002, 65(4).
71. Yang R.Y., Zou R.P., Yu A.B.., Choi S.K. Pore structure of the packing of fine particles. J Colloid Interface Sci July 2006, 299(2):719-725.