X-Ray Phase Nanotomography Resolves the 3D Human Bone Ultrastructure

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Langer, Max ^a,b   Pacureanu, Alexandra ^a,b,c   Suhonen, Heikki ^b   Grimal, Quentin ^d   Cloetens, Peter ^b   Peyrin, Françoise ^a,b  

^a UNIVERSITÉ DE LYON   (France)

^b EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^c UNIVERSITY POLITEHNICA OF BUCHAREST   (Romania)

^d SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN FIBER;

AGED; ARTICLE; BONE CELL; BONE RADIOGRAPHY; BONE STRUCTURE; FEMALE; HUMAN; HUMAN TISSUE; IMAGE ANALYSIS; IMAGE RECONSTRUCTION; INTERSTITIUM; NANOIMAGING; OPTICAL RESOLUTION; SENSITIVITY ANALYSIS; THREE DIMENSIONAL IMAGING; TOMOGRAPHY; X RAY PHASE NANOTOMOGRAPHY;

ABSORPTION; AGED; AGED, 80 AND OVER; ALGORITHMS; BONE AND BONES; COLLAGEN; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MODELS, STATISTICAL; NANOTECHNOLOGY; NORMAL DISTRIBUTION; OSTEOCYTES; TOMOGRAPHY, X-RAY COMPUTED; X-RAYS;

EID: 84865578322     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035691     Document Type: Article

References (37)

1. Huiskes R, Ruimerman R, van Lenthe GH, Janssen JD, (2000) Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 405: 704-706.
2. Taylor D, Hazenberg JG, Lee TC, (2007) Living with cracks: Damage and repair in human bone. Nat Mater 6: 263-268.
3. Schneider P, Meier M, Wepf R, Müller R, (2010) Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network. Bone 47: 848-858.
4. van Hove RP, Nolte PA, Vatsa A, Semeins CM, Salmon PL, et al. (2009) Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density- Is there a role for mechanosensing? Bone 45: 321-329.
5. Sugawara Y, Kamioka H, Honjo T, Tezuka K, Takano-Yamamoto T, (2005) Three-dimensional reconstruction of chick calvarial osteocytes and their cell processes using confocal microscopy. Bone 36: 877-83.
6. Schneider P, Meier M, Wepf R, Müller R, (2011) Serial FIB/SEM imaging for quantitative 3D assessment of the osteocyte lacuno-canalicular network. Bone 49: 304-311.
7. Andrews JC, Almeida E, van der Meulen MC, Alwood JS, Lee C, Liu Y, et al. (2010) Nanoscale X-ray microscopic imaging of mammalian mineralized tissue. Microsc Microanal 16: 327-336.
8. Dierolf M, Menzel A, Thibault P, Schneider P, Kewish CM, et al. (2010) Ptychographic X-ray computed tomography at the nanoscale. Nature 467: 436-439.
9. Muller R, (2009) Hierarchical microimaging of bone structure and function. Nat Rev Rheumatol 5: 373-381.
10. Lane NE, Yao W, Balooch M, Nalla RK, Balooch G, et al. (2005) Glucocorticoid-Treated Mice Have Localized Changes in Trabecular Bone Material Properties and Osteocyte Lacunar Size That Are Not Observed in Placebo-Treated or Estrogen-Deficient Mice. J Bone Miner Res 21: 466-476.
11. Nuzzo S, Lafage-Proust MH, Martin-Badosa E, Boivin G, Thomas T, et al. (2002) Synchrotron Radiation Microtomography Allows the Analysis of Three-Dimensional Microarchitecture and Degree of Mineralization of Human Iliac Crest Biopsy Specimens: Effects of Etidronate Treatment. J Bone Miner Res 17: 1372-1382.
12. Bousson V, Peyrin F, Bergot C, Hausard M, Sautet A, et al. (2004) Cortical Bone in the Human Femoral Neck: Three-Dimensional Appearance and Porosity Using Synchrotron Radiation. J Bone Miner Res 19: 794-801.
13. Kirkpatrick P, Baez AV, (1948) Formation of Optical Images by X-Rays. J Opt Soc Am 38: 766-773.
14. Hignette O, Cloetens P, Rostaing G, Bernard P, Morawe C, (2005) Efficient sub 100 nm focusing of hard×rays. Rev Sci Instrum 76: 063709.
15. Mokso R, Cloetens P, Maire E, Ludwig W, Buffière J-Y, (2007) Nanoscale zoom tomography with hard×rays using Kirkpatrick-Baez optics. Appl Phys Lett 90: 144104.
16. Bleuet P, Cloetens P, Gergaud P, Mariolle D, Chevalier N, et al. (2009) A hard x-ray nanoprobe for scanning and projection nanotomography. Rev Sci Instrum 80: 056101.
17. Cloetens P, Ludwig W, Baruchel J, Van Dyck D, Van Landuyt J, et al. (1999) Holotomography: Quantitative phase tomography with micrometer resolution using hard synchrotron radiation×rays. Appl Phys Lett 75: 2912-2914.
18. Kerschnitzki M, Wagermaier W, Roschger P, Seto J, Shahar R, et al. (2011) The organization of the osteocyte network mirrors the extracellular matrix orientation in bone. J Struct Biol 173: 303-311.
19. Giraud-Guille MM, (1988) Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif Tissue Int 42: 167-180.
20. Teti A, Zallone A, (2009) Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone 44: 11-16.
21. Marotti G, Ferretti M, Remaggi F, Palumbo C, (1995) Quantitative evaluation on osteocyte canalicular density in human secondary osteons. Bone 16: 125-128.
22. Burr DB, Schaffler MB, Frederickson RG, (1988) Composition of the cement line and its possible mechanical role as a local interface in human compact bone. J Biomech 21: 939-945.
23. O'Brien FJ, Taylor D, Lee TC, (2003) Microcrack accumulation at different intervals during fatigue testing of compact bone. J Biomech 36: 973-980.
24. Schaffler MB, Burr DB, Frederickson RG, (1987) Morphology of the osteonal cement line in human bone. Anat Rec 217: 223-228.
25. Davies JE, (2007) Bone bonding at natural and biomaterial surfaces. Biomaterials 28: 5058-5067.
26. Skedros JG, Holmes JL, Vajda EG, Bloebaum RD, (2005) Cement lines of secondary osteons in human bone are not mineral-deficient: New data in a historical perspective. Anat Rec A Discov Mol Cell Evol Biol 286: 781-803.
27. Pannarale L, Braidotti P, d'Alba L, Gaudio E, (1994) Scanning electron microscopy of collagen fiber orientation in the bone lamellar system in non-decalcified human samples. Acta Anat (Basel) 151: 36-42.
28. Kingsmill VJ, Boyde A, (1998) Mineralisation density of human mandibular bone: quantitative backscattered electron image analysis. Journal of Anatomy 192: 245-256.
29. Giraud-Guille MM, Besseau L, Martin R, (2003) Liquid crystalline assemblies of collagen in bone and in vitro systems. J Biomech 36: 1571-1579.
30. Hassenkam T, Fantner GE, Cutroni JA, Weaver JC, Morse DE, et al. (2004) High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35: 4-10.
31. Bromage TG, Goldman HM, McFarlin SC, Warshaw J, Boyde A, et al. (2003) Circularly polarized light standards for investigations of collagen fiber orientation in bone. Anat Rec B New Anat 274: 157-168.
32. Kazanci M, Roschger P, Paschalis EP, Klaushofer K, Fratzl P, (2006) Bone osteonal tissues by Raman spectral mapping: Orientation-composition. J Struct Biol 156: 489-496.
33. Barth HD, Zimmermann EA, Schaible E, Tang SY, Alliston T, et al. (2011) Characterization of the effects of X-ray irradiation on the hierarchical structure and mechanical properties of human cortical bone. Biomaterials 32: 8892-8904.
34. Martin T, Douissard PA, Couchaud M, Cecilia A, Baumbach T, et al. (2009) LSO-based single crystal film scintillator for synchrotron-based hard X-ray micro-imaging. IEEE Trans Nucl Sci 56: 1412-1418.
35. Guinier A (1994) X-ray diffraction in crystals, imperfect crystals, and amorphous bodies, (Dover, Minneola, NY).
36. Sato Y, Nakajima S, Shiraga N, Atsumi H, Yoshida S, et al. (1998) Three-dimensional multi-scale line filter for segmentation and visualization of curvilinear structures in medical images. Med Image Anal 2: 143-168.
37. Hoshen J, Kopelman R, (1976) Percolation and cluster distribution. I. Cluster multiple labeling technique and critical concentration algorithm. Phys Rev B 14: 3438-3445.