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2016 | OriginalPaper | Chapter

1. Synchrotron X-Ray Phase Nanotomography for Bone Tissue Characterization

Authors : Peter Varga, Loriane Weber, Bernhard Hesse, Max Langer

Published in: X-ray and Neutron Techniques for Nanomaterials Characterization

Publisher: Springer Berlin Heidelberg

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Abstract

X-ray phase nano-tomography allows the characterisation of bone ultrastructure: the lacuno-canalicular network, nanoscale mineralisation and the collagen orientation. In this chapter, we review the different X-ray imaging techniques capable of imaging the bone ultrastructure and then describe the work that has been done so far in nanoscale bone tissue characterisation using X-ray phase nano-tomography.
X-ray computed tomography at the micrometric scale is more and more considered as the reference technique in imaging of bone microstructure. The trend has been to push towards higher and higher resolution. Due to the difficulty of realising optics in the hard X-ray regime, the magnification has mainly been due to the use of visible light optics and indirect detection of the X-rays, which limits the attainable resolution with respect to the wavelength of the visible light used in detection. Recent developments in X-ray optics and instrumentation have allowed the implementation of several types of methods that achieve imaging limited in resolution by the X-ray wavelength, thus enabling computed tomography at the nanoscale. We review here the X-ray techniques with 3D imaging capability at the nanoscale: transmission X-ray microscopy, ptychography and in-line holography. Then, we present the experimental methodology for the in-line phase tomography, both at the instrumentation level and the physics behind this imaging technique. Further, we review the different ultrastructural features of bone that have so far been resolved and the applications that have been reported: imaging of the lacuno-canalicular network, direct analysis of collagen orientation, analysis of mineralisation on the nanoscale and the use of 3D images at the nanoscale as the basis of mechanical analyses. Finally, we discuss the issue of going beyond qualitative description to quantification of ultrastructural features.

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Literature
1.
go back to reference Röntgen WC (1896) On a new kind of rays. Nature 53:274–277 Röntgen WC (1896) On a new kind of rays. Nature 53:274–277
2.
go back to reference Cormack AM (1963) Representation of a function by its line integrals, with some radiological applications. J Appl Phys 34:2722CrossRef Cormack AM (1963) Representation of a function by its line integrals, with some radiological applications. J Appl Phys 34:2722CrossRef
3.
go back to reference Hounsfield GN (1972) A method and apparatus for examination of a body by radiation such as X-ray or gamma radiation. 1283915 Hounsfield GN (1972) A method and apparatus for examination of a body by radiation such as X-ray or gamma radiation. 1283915
4.
go back to reference Bonse U (2002) Developments in X-ray tomography II. In: Proceedings of the SPIE, vol. 4503 Bonse U (2002) Developments in X-ray tomography II. In: Proceedings of the SPIE, vol. 4503
5.
go back to reference Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25(7):1468–1486CrossRef Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25(7):1468–1486CrossRef
6.
go back to reference Engelke K, Karolczak M, Lutz A, Seibert U, Schaller S, Kalender W (1999) Micro-CT. Technology and application for assessing bone structure. Radiologe 39(3):203–212CrossRef Engelke K, Karolczak M, Lutz A, Seibert U, Schaller S, Kalender W (1999) Micro-CT. Technology and application for assessing bone structure. Radiologe 39(3):203–212CrossRef
7.
go back to reference Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P (1999) Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 14(7):1167–1174CrossRef Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P (1999) Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 14(7):1167–1174CrossRef
8.
go back to reference Salomé M, Peyrin F, Cloetens P, Odet C, Laval-Jeantet A-M, Baruchel J, Spanne P (1999) A synchrotron radiation microtomography system for the analysis of trabecular bone samples. Med Phys 26(10):2194CrossRef Salomé M, Peyrin F, Cloetens P, Odet C, Laval-Jeantet A-M, Baruchel J, Spanne P (1999) A synchrotron radiation microtomography system for the analysis of trabecular bone samples. Med Phys 26(10):2194CrossRef
9.
go back to reference Nuzzo S, Peyrin FF, Cloetens P, Baruchel JJ, Boivin G (2002) Quantification of the degree of mineralization of bone in three dimensions using synchrotron radiation microtomography. Med Phys 29(11):2672CrossRef Nuzzo S, Peyrin FF, Cloetens P, Baruchel JJ, Boivin G (2002) Quantification of the degree of mineralization of bone in three dimensions using synchrotron radiation microtomography. Med Phys 29(11):2672CrossRef
10.
go back to reference Peyrin F, Salomé M, Nuzzo S, Cloetens P, Laval-Jeantet AM, Baruchel J (2000) Perspectives in three-dimensional analysis of bone samples using synchrotron radiation microtomography. Cell Mol Biol 46(6):1089–1102 Peyrin F, Salomé M, Nuzzo S, Cloetens P, Laval-Jeantet AM, Baruchel J (2000) Perspectives in three-dimensional analysis of bone samples using synchrotron radiation microtomography. Cell Mol Biol 46(6):1089–1102
11.
go back to reference Schneider P, Meier M, Wepf R, Müller R (2010) Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network. Bone 47(5):848–858CrossRef Schneider P, Meier M, Wepf R, Müller R (2010) Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network. Bone 47(5):848–858CrossRef
12.
go back to reference van Hove RP, Nolte PA, Vatsa A, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2009) Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density – is there a role for mechanosensing? Bone 45(2):321–329CrossRef van Hove RP, Nolte PA, Vatsa A, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2009) Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density – is there a role for mechanosensing? Bone 45(2):321–329CrossRef
13.
go back to reference Labiche J-C, Mathon O, Pascarelli S, Newton MA, Ferre GG, Curfs C, Vaughan G, Homs A, Carreiras DF (2007) Invited article: the fast readout low noise camera as a versatile x-ray detector for time resolved dispersive extended x-ray absorption fine structure and diffraction studies of dynamic problems in materials science, chemistry, and catalysis. Rev Sci Instrum 78(9):091301CrossRef Labiche J-C, Mathon O, Pascarelli S, Newton MA, Ferre GG, Curfs C, Vaughan G, Homs A, Carreiras DF (2007) Invited article: the fast readout low noise camera as a versatile x-ray detector for time resolved dispersive extended x-ray absorption fine structure and diffraction studies of dynamic problems in materials science, chemistry, and catalysis. Rev Sci Instrum 78(9):091301CrossRef
14.
go back to reference Paschalis EP, Mendelsohn R, Boskey AL (2011) Infrared assessment of bone quality: a review. Clin Orthop Relat Res 469(8):2170–2178CrossRef Paschalis EP, Mendelsohn R, Boskey AL (2011) Infrared assessment of bone quality: a review. Clin Orthop Relat Res 469(8):2170–2178CrossRef
15.
go back to reference Seeman E, Delmas PD (2006) Bone quality – the material and structural basis of bone strength and fragility. N Engl J Med 354(21):2250–2261CrossRef Seeman E, Delmas PD (2006) Bone quality – the material and structural basis of bone strength and fragility. N Engl J Med 354(21):2250–2261CrossRef
16.
go back to reference Bonewald LF (2006) Mechanosensation and transduction in osteocytes. Bonekey Osteovision 3(10):7–15CrossRef Bonewald LF (2006) Mechanosensation and transduction in osteocytes. Bonekey Osteovision 3(10):7–15CrossRef
17.
go back to reference Klein-Nulend J, Bacabac RG, Mullender MG (2005) Mechanobiology of bone tissue. Pathol Biol 53(10):576–580CrossRef Klein-Nulend J, Bacabac RG, Mullender MG (2005) Mechanobiology of bone tissue. Pathol Biol 53(10):576–580CrossRef
18.
go back to reference Knothe Tate ML, Adamson JR, Tami AE, Bauer TW, Nijweide PJ, Burger EH, Nulend JK (2004) The osteocyte. Int J Biochem Cell Biol 36(1):1–8CrossRef Knothe Tate ML, Adamson JR, Tami AE, Bauer TW, Nijweide PJ, Burger EH, Nulend JK (2004) The osteocyte. Int J Biochem Cell Biol 36(1):1–8CrossRef
19.
go back to reference Nijweide PJ, Burger EH, Nulend JK (2002) The osteocyte, pp 93–108 Nijweide PJ, Burger EH, Nulend JK (2002) The osteocyte, pp 93–108
20.
go back to reference Burger EH, Klein-Nulend J (1999) Mechanotransduction in bone – role of the lacuno-canalicular network. FASEB J 13(Suppl):S101–S112 Burger EH, Klein-Nulend J (1999) Mechanotransduction in bone – role of the lacuno-canalicular network. FASEB J 13(Suppl):S101–S112
21.
go back to reference Nicolella D, Feng J (2008) Effects of nanomechanical bone tissue properties on bone tissue strain: implications for osteocyte mechanotransduction. J Musculoskelet 8(4):330–331 Nicolella D, Feng J (2008) Effects of nanomechanical bone tissue properties on bone tissue strain: implications for osteocyte mechanotransduction. J Musculoskelet 8(4):330–331
22.
go back to reference Verbruggen SW, Vaughan TJ, McNamara LM (2012) Strain amplification in bone mechanobiology: a computational investigation of the in vivo mechanics of osteocytes. J R Soc Interface 9(75):2735–2744CrossRef Verbruggen SW, Vaughan TJ, McNamara LM (2012) Strain amplification in bone mechanobiology: a computational investigation of the in vivo mechanics of osteocytes. J R Soc Interface 9(75):2735–2744CrossRef
23.
go back to reference Verbruggen SW, Vaughan TJ, McNamara LM (2013) Fluid flow in the osteocyte mechanical environment: a fluid–structure interaction approach. Biomech Model Mechanobiol, epub, Apr 2013 Verbruggen SW, Vaughan TJ, McNamara LM (2013) Fluid flow in the osteocyte mechanical environment: a fluid–structure interaction approach. Biomech Model Mechanobiol, epub, Apr 2013
24.
go back to reference Hazenberg JG, Freeley M, Foran E, Lee TC, Taylor D (2006) Microdamage: a cell transducing mechanism based on ruptured osteocyte processes. J Biomech 39(11):2096–2103CrossRef Hazenberg JG, Freeley M, Foran E, Lee TC, Taylor D (2006) Microdamage: a cell transducing mechanism based on ruptured osteocyte processes. J Biomech 39(11):2096–2103CrossRef
25.
go back to reference Taylor D, Hazenberg JG, Lee TC (2007) Living with cracks: damage and repair in human bone. Nat Mater 6(4):263–268CrossRef Taylor D, Hazenberg JG, Lee TC (2007) Living with cracks: damage and repair in human bone. Nat Mater 6(4):263–268CrossRef
26.
go back to reference Qiu S, Rao DS, Fyhrie DP, Palnitkar S, Parfitt AM (2005) The morphological association between microcracks and osteocyte lacunae in human cortical bone. Bone 37(1):10–15CrossRef Qiu S, Rao DS, Fyhrie DP, Palnitkar S, Parfitt AM (2005) The morphological association between microcracks and osteocyte lacunae in human cortical bone. Bone 37(1):10–15CrossRef
27.
go back to reference Dooley C, Tisbo P, Lee TC, Taylor D (2012) Rupture of osteocyte processes across microcracks: the effect of crack length and stress. Biomech Model Mechanobiol 11(6):759–766CrossRef Dooley C, Tisbo P, Lee TC, Taylor D (2012) Rupture of osteocyte processes across microcracks: the effect of crack length and stress. Biomech Model Mechanobiol 11(6):759–766CrossRef
28.
go back to reference Bonewald LF, Kneissel M, Johnson M (2013) Preface: the osteocyte. Bone 54(2):181CrossRef Bonewald LF, Kneissel M, Johnson M (2013) Preface: the osteocyte. Bone 54(2):181CrossRef
29.
30.
go back to reference Kalajzic I, Matthews BG, Torreggiani E, Harris MA, Divieti Pajevic P, Harris SE (2013) In vitro and in vivo approaches to study osteocyte biology. Bone 54(2):296–306CrossRef Kalajzic I, Matthews BG, Torreggiani E, Harris MA, Divieti Pajevic P, Harris SE (2013) In vitro and in vivo approaches to study osteocyte biology. Bone 54(2):296–306CrossRef
31.
go back to reference Klein-Nulend J, Bakker AD, Bacabac RG, Vatsa A, Weinbaum S (2013) Mechanosensation and transduction in osteocytes. Bone 54(2):182 (in press)CrossRef Klein-Nulend J, Bakker AD, Bacabac RG, Vatsa A, Weinbaum S (2013) Mechanosensation and transduction in osteocytes. Bone 54(2):182 (in press)CrossRef
32.
go back to reference Rochefort GY, Pallu S, Benhamou CL (2010) Osteocyte : the unrecognized side of bone tissue. Osteoporos Int 21(9):1457–1469CrossRef Rochefort GY, Pallu S, Benhamou CL (2010) Osteocyte : the unrecognized side of bone tissue. Osteoporos Int 21(9):1457–1469CrossRef
33.
go back to reference Seeman E (2006) Osteocytes – martyrs for integrity of bone strength. Osteoporos Int 17(10):1443–1448CrossRef Seeman E (2006) Osteocytes – martyrs for integrity of bone strength. Osteoporos Int 17(10):1443–1448CrossRef
34.
go back to reference Atkins A, Dean MN, Habegger ML, Motta PJ, Ofer L, Repp F, Shipov A, Weiner S, Currey JD, Shahar R (2014) Remodeling in bone without osteocytes: billfish challenge bone structure-function paradigms. Proc Natl Acad Sci U S A 111(45):16047–16052CrossRef Atkins A, Dean MN, Habegger ML, Motta PJ, Ofer L, Repp F, Shipov A, Weiner S, Currey JD, Shahar R (2014) Remodeling in bone without osteocytes: billfish challenge bone structure-function paradigms. Proc Natl Acad Sci U S A 111(45):16047–16052CrossRef
35.
go back to reference 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(11):939–945CrossRef 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(11):939–945CrossRef
36.
go back to reference Schaffler MB, Burr DB, Frederickson RG (1987) Morphology of the osteonal cement line in human bone. Anat Rec 217(3):223–228CrossRef Schaffler MB, Burr DB, Frederickson RG (1987) Morphology of the osteonal cement line in human bone. Anat Rec 217(3):223–228CrossRef
37.
go back to reference Davies JE (2007) Bone bonding at natural and biomaterial surfaces. Biomaterials 28(34):5058–5067CrossRef Davies JE (2007) Bone bonding at natural and biomaterial surfaces. Biomaterials 28(34):5058–5067CrossRef
38.
go back to reference 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(1):781–803CrossRef 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(1):781–803CrossRef
39.
go back to reference Milovanovic P, Zimmermann EAE, Hahn M, Djonic D, Püschel K, Djuric M, Amling M, Busse B (2013) Osteocytic canalicular networks: morphological implications for altered mechanosensitivity. ACS 7(9):7542–7551 Milovanovic P, Zimmermann EAE, Hahn M, Djonic D, Püschel K, Djuric M, Amling M, Busse B (2013) Osteocytic canalicular networks: morphological implications for altered mechanosensitivity. ACS 7(9):7542–7551
40.
go back to reference Kingsmill VJ, Boyde A (1998) Mineralisation density of human mandibular bone: quantitative backscattered electron image analysis. J Anat 192(Pt 2):245–256CrossRef Kingsmill VJ, Boyde A (1998) Mineralisation density of human mandibular bone: quantitative backscattered electron image analysis. J Anat 192(Pt 2):245–256CrossRef
41.
go back to reference 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(1):36–42CrossRef 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(1):36–42CrossRef
42.
go back to reference Reznikov N, Almany-Magal R, Shahar R, Weiner S (2013) Three-dimensional imaging of collagen fibril organization in rat circumferential lamellar bone using a dual beam electron microscope reveals ordered and disordered. Bone 52(2):676–683CrossRef Reznikov N, Almany-Magal R, Shahar R, Weiner S (2013) Three-dimensional imaging of collagen fibril organization in rat circumferential lamellar bone using a dual beam electron microscope reveals ordered and disordered. Bone 52(2):676–683CrossRef
43.
go back to reference Reznikov N, Shahar R, Weiner S (2014) Three-dimensional structure of human lamellar bone: the presence of two different materials and new insights into the hierarchical organization. Bone 59(2012):93–104CrossRef Reznikov N, Shahar R, Weiner S (2014) Three-dimensional structure of human lamellar bone: the presence of two different materials and new insights into the hierarchical organization. Bone 59(2012):93–104CrossRef
44.
go back to reference Giraud-Guille M-M, Besseau L, Martin R (2003) Liquid crystalline assemblies of collagen in bone and in vitro systems. J Biomech 36(10):1571–1579CrossRef Giraud-Guille M-M, Besseau L, Martin R (2003) Liquid crystalline assemblies of collagen in bone and in vitro systems. J Biomech 36(10):1571–1579CrossRef
45.
go back to reference Hassenkam T, Fantner GE, Cutroni JA, Weaver JC, Morse DE, Hansma PK (2004) High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35(1):4–10CrossRef Hassenkam T, Fantner GE, Cutroni JA, Weaver JC, Morse DE, Hansma PK (2004) High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35(1):4–10CrossRef
46.
go back to reference Bromage TG, Goldman HM, McFarlin SC, Warshaw J, Boyde A, Riggs CM (2003) Circularly polarized light standards for investigations of collagen fiber orientation in bone. Anat Rec B New Anat 274(1):157–168CrossRef Bromage TG, Goldman HM, McFarlin SC, Warshaw J, Boyde A, Riggs CM (2003) Circularly polarized light standards for investigations of collagen fiber orientation in bone. Anat Rec B New Anat 274(1):157–168CrossRef
47.
go back to reference Kazanci M, Roschger P, Paschalis EP, Klaushofer K, Fratzl P (2006) Bone osteonal tissues by Raman spectral mapping: orientation-composition. J Struct Biol 156(3):489–496CrossRef Kazanci M, Roschger P, Paschalis EP, Klaushofer K, Fratzl P (2006) Bone osteonal tissues by Raman spectral mapping: orientation-composition. J Struct Biol 156(3):489–496CrossRef
48.
go back to reference Schrof S, Varga P, Galvis L, Raum K, Masic A (2014) 3D Raman mapping of the collagen fibril orientation in human osteonal lamellae. J Struct Biol 187(3):266–275CrossRef Schrof S, Varga P, Galvis L, Raum K, Masic A (2014) 3D Raman mapping of the collagen fibril orientation in human osteonal lamellae. J Struct Biol 187(3):266–275CrossRef
49.
go back to reference Carter Y, Thomas CDL, Clement JG, Peele AG, Hannah K, Cooper DMLL (2013) Variation in osteocyte lacunar morphology and density in the human femur – a synchrotron radiation micro-CT study. Bone 52(1):126–132CrossRef Carter Y, Thomas CDL, Clement JG, Peele AG, Hannah K, Cooper DMLL (2013) Variation in osteocyte lacunar morphology and density in the human femur – a synchrotron radiation micro-CT study. Bone 52(1):126–132CrossRef
50.
go back to reference Carter Y, Thomas CDL, Clement JG, Cooper DML (2013) Femoral osteocyte lacunar density, volume and morphology in women across the lifespan. J Struct Biol 183(3):519–526CrossRef Carter Y, Thomas CDL, Clement JG, Cooper DML (2013) Femoral osteocyte lacunar density, volume and morphology in women across the lifespan. J Struct Biol 183(3):519–526CrossRef
51.
go back to reference Dong P, Haupert S, Hesse B, Langer M, Gouttenoire P-J, Bousson V, Peyrin F (2014) 3D osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-CT images. Bone 60:172–185CrossRef Dong P, Haupert S, Hesse B, Langer M, Gouttenoire P-J, Bousson V, Peyrin F (2014) 3D osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-CT images. Bone 60:172–185CrossRef
52.
go back to reference Hesse B, Varga P, Langer M, Pacureanu A, Schrof S, Männicke N, Suhonen H, Maurer P, Cloetens P, Peyrin F, Raum K (2014) Canalicular network morphology is the major determinant of the spatial distribution of mass density in human bone tissue – evidence by means of synchrotron radiation phase-contrast nano-CT. J Bone Miner Res 30(2):346–356CrossRef Hesse B, Varga P, Langer M, Pacureanu A, Schrof S, Männicke N, Suhonen H, Maurer P, Cloetens P, Peyrin F, Raum K (2014) Canalicular network morphology is the major determinant of the spatial distribution of mass density in human bone tissue – evidence by means of synchrotron radiation phase-contrast nano-CT. J Bone Miner Res 30(2):346–356CrossRef
53.
go back to reference Hesse B, Langer M, Varga P, Pacureanu A, Dong P, Schrof S, Männicke N, Suhonen H, Olivier C, Maurer P, Kazakia GJ, Raum K, Peyrin F (2014) Alterations of mass density and 3D osteocyte lacunar properties in bisphosphonate-related osteonecrotic human jaw Bone, a synchrotron μCT study. PLoS One 9(2), e88481CrossRef Hesse B, Langer M, Varga P, Pacureanu A, Dong P, Schrof S, Männicke N, Suhonen H, Olivier C, Maurer P, Kazakia GJ, Raum K, Peyrin F (2014) Alterations of mass density and 3D osteocyte lacunar properties in bisphosphonate-related osteonecrotic human jaw Bone, a synchrotron μCT study. PLoS One 9(2), e88481CrossRef
54.
go back to reference Pacureanu A, Langer M, Boller E, Tafforeau P, Peyrin FF (2012) Nanoscale imaging of the bone cell network with synchrotron x-ray tomography: optimization of acquisition setup. Med Phys 39(4):2229–2238CrossRef Pacureanu A, Langer M, Boller E, Tafforeau P, Peyrin FF (2012) Nanoscale imaging of the bone cell network with synchrotron x-ray tomography: optimization of acquisition setup. Med Phys 39(4):2229–2238CrossRef
55.
go back to reference Pacureanu A, Larrue A, Langer M, Olivier C, Muller C, Lafage-Proust M-H, Peyrin F (2013) Adaptive filtering for enhancement of the osteocyte cell network in 3D microtomography images. IRBM 34(1):48–52CrossRef Pacureanu A, Larrue A, Langer M, Olivier C, Muller C, Lafage-Proust M-H, Peyrin F (2013) Adaptive filtering for enhancement of the osteocyte cell network in 3D microtomography images. IRBM 34(1):48–52CrossRef
56.
go back to reference 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(5):877–883CrossRef 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(5):877–883CrossRef
57.
go back to reference Gourion-Arsiquaud S, Marcott C, Hu Q, Boskey AL (2014) Studying variations in bone composition at nano-scale resolution: a preliminary report. Calcif Tissue Int 95(5):413–418CrossRef Gourion-Arsiquaud S, Marcott C, Hu Q, Boskey AL (2014) Studying variations in bone composition at nano-scale resolution: a preliminary report. Calcif Tissue Int 95(5):413–418CrossRef
58.
go back to reference Geith T, Amarie S, Milz S, Bamberg F, Keilmann F (2014) Visualisation of methacrylate-embedded human bone sections by infrared nanoscopy. J Biophotonics 7(6):418–424CrossRef Geith T, Amarie S, Milz S, Bamberg F, Keilmann F (2014) Visualisation of methacrylate-embedded human bone sections by infrared nanoscopy. J Biophotonics 7(6):418–424CrossRef
59.
go back to reference 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(2):304–311CrossRef 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(2):304–311CrossRef
60.
go back to reference Magal RA, Reznikov N (2014) Three-dimensional structure of minipig fibrolamellar bone: adaptation to axial loading. J Struct 186(2):253–264 Magal RA, Reznikov N (2014) Three-dimensional structure of minipig fibrolamellar bone: adaptation to axial loading. J Struct 186(2):253–264
61.
go back to reference Kamioka H, Murshid SA, Ishihara Y, Kajimura N, Hasegawa T, Ando R, Sugawara Y, Yamashiro T, Takaoka A, Takano-Yamamoto T (2009) A method for observing silver-stained osteocytes in situ in 3-microm sections using ultra-high voltage electron microscopy tomography. Microsc Microanal 15(5):377–383CrossRef Kamioka H, Murshid SA, Ishihara Y, Kajimura N, Hasegawa T, Ando R, Sugawara Y, Yamashiro T, Takaoka A, Takano-Yamamoto T (2009) A method for observing silver-stained osteocytes in situ in 3-microm sections using ultra-high voltage electron microscopy tomography. Microsc Microanal 15(5):377–383CrossRef
62.
go back to reference Martínez-Criado G, Tucoulou R, Cloetens P, Bleuet P, Bohic S, Cauzid J, Kieffer I, Kosior E, Labouré S, Petitgirard S, Rack A, Sans JA, Segura-Ruiz J, Suhonen H, Susini J, Villanova J (2012) Status of the hard x-ray microprobe beamline ID22 of the European Synchrotron Radiation Facility. J Synchrotron Radiat 19(Pt 1):10–18CrossRef Martínez-Criado G, Tucoulou R, Cloetens P, Bleuet P, Bohic S, Cauzid J, Kieffer I, Kosior E, Labouré S, Petitgirard S, Rack A, Sans JA, Segura-Ruiz J, Suhonen H, Susini J, Villanova J (2012) Status of the hard x-ray microprobe beamline ID22 of the European Synchrotron Radiation Facility. J Synchrotron Radiat 19(Pt 1):10–18CrossRef
63.
go back to reference Morawe C, Hignette O, Cloetens P, Ludwig W, Borel C, Bernard P, Rommeveaux A (2006) Graded multilayers for focusing hard x-rays below 50 nm. In: SPIE optics + photonics, pp 63170F–63170F-11 Morawe C, Hignette O, Cloetens P, Ludwig W, Borel C, Bernard P, Rommeveaux A (2006) Graded multilayers for focusing hard x-rays below 50 nm. In: SPIE optics + photonics, pp 63170F–63170F-11
64.
go back to reference Barrett R, Baker R, Cloetens P, Dabin Y, Morawe C, Suhonen H, Tucoulou R, Vivo A, Zhang L (2011) Dynamically-figured mirror system for high-energy nanofocusing at the ESRF. In: SPIE optical engineering + applications. pp 813904–813904-12 Barrett R, Baker R, Cloetens P, Dabin Y, Morawe C, Suhonen H, Tucoulou R, Vivo A, Zhang L (2011) Dynamically-figured mirror system for high-energy nanofocusing at the ESRF. In: SPIE optical engineering + applications. pp 813904–813904-12
65.
go back to reference Hignette O, Cloetens P, Morawe C, Borel C, Ludwig W, Bernard P, Rommeveaux A, Bohic S (2007) Nanofocusing at ESRF using graded multilayer mirrors. AIP Conf Proc 879(1):792–795CrossRef Hignette O, Cloetens P, Morawe C, Borel C, Ludwig W, Bernard P, Rommeveaux A, Bohic S (2007) Nanofocusing at ESRF using graded multilayer mirrors. AIP Conf Proc 879(1):792–795CrossRef
66.
go back to reference Zhang L, Baker R, Barrett R, Cloetens P, Dabin Y, Garrett R, Gentle I, Nugent K, Wilkins S (2010) Mirror profile optimization for nano-focusing KB mirror. In: SRI 2009, 10th international conference on radiation instrumentation, vol 1234(1), pp 801–804 Zhang L, Baker R, Barrett R, Cloetens P, Dabin Y, Garrett R, Gentle I, Nugent K, Wilkins S (2010) Mirror profile optimization for nano-focusing KB mirror. In: SRI 2009, 10th international conference on radiation instrumentation, vol 1234(1), pp 801–804
67.
go back to reference Cloetens P, Suhonen H, Bay A, Bohic S, Fleck C, Langer M, Pacureanu A, Peyrin F, Rack A, Vigneron JP, Zaslansky P (2012) Non-destructive and multi-modal 3D imaging of biological materials. In: 2012 MRS spring meeting and exhibit Cloetens P, Suhonen H, Bay A, Bohic S, Fleck C, Langer M, Pacureanu A, Peyrin F, Rack A, Vigneron JP, Zaslansky P (2012) Non-destructive and multi-modal 3D imaging of biological materials. In: 2012 MRS spring meeting and exhibit
68.
go back to reference Tucoulou R, Martinez-Criado G, Bleuet P, Kieffer I, Cloetens P, Labouré S, Martin T, Guilloud C, Susini J (2008) High-resolution angular beam stability monitoring at a nanofocusing beamline. J Synchrotron Radiat 15(Pt 4):392–398CrossRef Tucoulou R, Martinez-Criado G, Bleuet P, Kieffer I, Cloetens P, Labouré S, Martin T, Guilloud C, Susini J (2008) High-resolution angular beam stability monitoring at a nanofocusing beamline. J Synchrotron Radiat 15(Pt 4):392–398CrossRef
69.
go back to reference Jackson JD (1975) Classical electrodynamics Jackson JD (1975) Classical electrodynamics
70.
go back to reference Snigirev A, Snigireva I, Kohn V, Kuznetsov S, Schelokov I (1995) On the possibilities of x-ray phase contrast microimaging by coherent high-energy synchrotron radiation. Rev Sci Instrum 66(12):5486CrossRef Snigirev A, Snigireva I, Kohn V, Kuznetsov S, Schelokov I (1995) On the possibilities of x-ray phase contrast microimaging by coherent high-energy synchrotron radiation. Rev Sci Instrum 66(12):5486CrossRef
71.
go back to reference Goodman JW (2005) Introduction to fourier optics Goodman JW (2005) Introduction to fourier optics
72.
go back to reference Langer M, Pacureanu A, Suhonen H, Grimal Q, Cloetens P, Peyrin F (2012) X-ray phase nanotomography resolves the 3D human bone ultrastructure. PLoS One 7(8), e35691CrossRef Langer M, Pacureanu A, Suhonen H, Grimal Q, Cloetens P, Peyrin F (2012) X-ray phase nanotomography resolves the 3D human bone ultrastructure. PLoS One 7(8), e35691CrossRef
73.
go back to reference Cloetens P, Ludwig W, Baruchel J, Van Dyck D, Van Landuyt J, Guigay JP, Schlenker M (1999) Holotomography: quantitative phase tomography with micrometer resolution using hard synchrotron radiation x rays. Appl Phys Lett 75(19):2912CrossRef Cloetens P, Ludwig W, Baruchel J, Van Dyck D, Van Landuyt J, Guigay JP, Schlenker M (1999) Holotomography: quantitative phase tomography with micrometer resolution using hard synchrotron radiation x rays. Appl Phys Lett 75(19):2912CrossRef
74.
go back to reference Langer M, Cloetens P, Guigay J-P, Peyrin F (2008) Quantitative comparison of direct phase retrieval algorithms in in-line phase tomography. Med Phys 35(10):4556–4566CrossRef Langer M, Cloetens P, Guigay J-P, Peyrin F (2008) Quantitative comparison of direct phase retrieval algorithms in in-line phase tomography. Med Phys 35(10):4556–4566CrossRef
75.
go back to reference Elser V (2003) Solution of the crystallographic phase problem by iterated projections. Acta Crystallogr Sect A: Found Crystallogr 59(3):201–209CrossRef Elser V (2003) Solution of the crystallographic phase problem by iterated projections. Acta Crystallogr Sect A: Found Crystallogr 59(3):201–209CrossRef
76.
go back to reference Fienup JR (1982) Phase retrieval algorithms: a comparison. Appl Opt 21(15):2758–2769CrossRef Fienup JR (1982) Phase retrieval algorithms: a comparison. Appl Opt 21(15):2758–2769CrossRef
77.
go back to reference Gerchberg RW, Saxton WO (1972) A practical algorithm for the determination of phase from image and diffraction plane pictures. Optik (Stuttg) 35:237–246 Gerchberg RW, Saxton WO (1972) A practical algorithm for the determination of phase from image and diffraction plane pictures. Optik (Stuttg) 35:237–246
78.
go back to reference Bauschke HH, Combettes PL, Luke DR (2002) Phase retrieval, error reduction algorithm, and Fienup variants: a view from convex optimization. J Opt Soc Am A 19(7):1334CrossRef Bauschke HH, Combettes PL, Luke DR (2002) Phase retrieval, error reduction algorithm, and Fienup variants: a view from convex optimization. J Opt Soc Am A 19(7):1334CrossRef
79.
go back to reference Thibault P, Elser V (2010) X-ray diffraction microscopy. Annu Rev Condens Matter Phys 1(1):237–255CrossRef Thibault P, Elser V (2010) X-ray diffraction microscopy. Annu Rev Condens Matter Phys 1(1):237–255CrossRef
80.
go back to reference Elser V, Rankenburg I, Thibault P (2007) Searching with iterated maps. Proc Natl Acad Sci U S A 104(2):418–423CrossRef Elser V, Rankenburg I, Thibault P (2007) Searching with iterated maps. Proc Natl Acad Sci U S A 104(2):418–423CrossRef
81.
go back to reference Dierolf M, Menzel A, Thibault P, Schneider P, Kewish CM, Wepf R, Bunk O, Pfeiffer F (2010) Ptychographic x-ray computed tomography at the nanoscale. Nature 467(7314):436–439CrossRef Dierolf M, Menzel A, Thibault P, Schneider P, Kewish CM, Wepf R, Bunk O, Pfeiffer F (2010) Ptychographic x-ray computed tomography at the nanoscale. Nature 467(7314):436–439CrossRef
82.
go back to reference Schroer C, Boye P, Feldkamp J, Patommel J, Schropp A, Schwab A, Stephan S, Burghammer M, Schöder S, Riekel C (2008) Coherent X-ray diffraction imaging with nanofocused illumination. Phys Rev Lett 101(9):090801CrossRef Schroer C, Boye P, Feldkamp J, Patommel J, Schropp A, Schwab A, Stephan S, Burghammer M, Schöder S, Riekel C (2008) Coherent X-ray diffraction imaging with nanofocused illumination. Phys Rev Lett 101(9):090801CrossRef
83.
go back to reference Huang X, Nelson J, Kirz J, Lima E, Marchesini S, Miao H, Neiman A, Shapiro D, Steinbrener J, Stewart A, Turner J, Jacobsen C (2009) Soft X-ray diffraction microscopy of a frozen hydrated yeast cell. Phys Rev Lett 103(19):198101CrossRef Huang X, Nelson J, Kirz J, Lima E, Marchesini S, Miao H, Neiman A, Shapiro D, Steinbrener J, Stewart A, Turner J, Jacobsen C (2009) Soft X-ray diffraction microscopy of a frozen hydrated yeast cell. Phys Rev Lett 103(19):198101CrossRef
84.
go back to reference Maiden AM, Rodenburg JM (2009) An improved ptychographical phase retrieval algorithm for diffractive imaging. Ultramicroscopy 109(10):1256–1262CrossRef Maiden AM, Rodenburg JM (2009) An improved ptychographical phase retrieval algorithm for diffractive imaging. Ultramicroscopy 109(10):1256–1262CrossRef
85.
go back to reference Thibault P, Dierolf M, Menzel A, Bunk O, David C, Pfeiffer F (2008) High-resolution scanning x-ray diffraction microscopy. Science 321(5887):379–382CrossRef Thibault P, Dierolf M, Menzel A, Bunk O, David C, Pfeiffer F (2008) High-resolution scanning x-ray diffraction microscopy. Science 321(5887):379–382CrossRef
86.
go back to reference Thibault P, Dierolf M, Bunk O, Menzel A, Pfeiffer F (2009) Probe retrieval in ptychographic coherent diffractive imaging. Ultramicroscopy 109(4):338–343CrossRef Thibault P, Dierolf M, Bunk O, Menzel A, Pfeiffer F (2009) Probe retrieval in ptychographic coherent diffractive imaging. Ultramicroscopy 109(4):338–343CrossRef
87.
go back to reference Hoppe W (1969) Beugung im inhomogenen Primärstrahlwellenfeld. I. Prinzip einer Phasenmessung von Elektronenbeungungsinterferenzen. Acta Crystallogr Sect A 25(4):495–501CrossRef Hoppe W (1969) Beugung im inhomogenen Primärstrahlwellenfeld. I. Prinzip einer Phasenmessung von Elektronenbeungungsinterferenzen. Acta Crystallogr Sect A 25(4):495–501CrossRef
88.
go back to reference Guinier A (1994) X-ray diffraction in crystals, imperfect crystals, and amorphous bodies. Courier Dover Publications Guinier A (1994) X-ray diffraction in crystals, imperfect crystals, and amorphous bodies. Courier Dover Publications
89.
go back to reference Langer M, Cloetens P, Peyrin F (2010) Regularization of phase retrieval with phase-attenuation duality prior for 3-D holotomography. IEEE Trans Image Process 19(9):2428–2436CrossRef Langer M, Cloetens P, Peyrin F (2010) Regularization of phase retrieval with phase-attenuation duality prior for 3-D holotomography. IEEE Trans Image Process 19(9):2428–2436CrossRef
90.
go back to reference Paganin D, Mayo SC, Gureyev TE, Miller PR, Wilkins SW (2002) Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J Microsc 206(1):33–40CrossRef Paganin D, Mayo SC, Gureyev TE, Miller PR, Wilkins SW (2002) Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J Microsc 206(1):33–40CrossRef
91.
go back to reference Wilkins SW, Gureyev TE, Gao D, Pogany A, Stevenson AW (1996) Phase-contrast imaging using polychromatic hard x-rays. Nature 384(6607):335–338CrossRef Wilkins SW, Gureyev TE, Gao D, Pogany A, Stevenson AW (1996) Phase-contrast imaging using polychromatic hard x-rays. Nature 384(6607):335–338CrossRef
92.
go back to reference Holler M, Diaz A, Guizar-Sicairos M, Karvinen P, Färm E, Härkönen E, Ritala M, Menzel A, Raabe J, Bunk O (2014) X-ray ptychographic computed tomography at 16 nm isotropic 3D resolution. Sci Rep 4:3857CrossRef Holler M, Diaz A, Guizar-Sicairos M, Karvinen P, Färm E, Härkönen E, Ritala M, Menzel A, Raabe J, Bunk O (2014) X-ray ptychographic computed tomography at 16 nm isotropic 3D resolution. Sci Rep 4:3857CrossRef
93.
go back to reference Dennis MDP, Ghiglia C (1998) Two-dimensional phase unwrapping: theory, algorithms, and software. Wiley, New York Dennis MDP, Ghiglia C (1998) Two-dimensional phase unwrapping: theory, algorithms, and software. Wiley, New York
94.
go back to reference Andrews JC, Almeida E, van der Meulen MCH, Alwood JS, Lee C, Liu Y, Chen J, Meirer F, Feser M, Gelb J, Rudati J, Tkachuk A, Yun W, Pianetta P (2010) Nanoscale x-ray microscopic imaging of mammalian mineralized tissue. Microsc Microanal 16(3):327–336CrossRef Andrews JC, Almeida E, van der Meulen MCH, Alwood JS, Lee C, Liu Y, Chen J, Meirer F, Feser M, Gelb J, Rudati J, Tkachuk A, Yun W, Pianetta P (2010) Nanoscale x-ray microscopic imaging of mammalian mineralized tissue. Microsc Microanal 16(3):327–336CrossRef
95.
go back to reference Mokso R, Cloetens P, Maire E, Ludwig W, Buffière J-Y (2007) Nanoscale zoom tomography with hard x rays using Kirkpatrick-Baez optics. Appl Phys Lett 90(14):144104CrossRef Mokso R, Cloetens P, Maire E, Ludwig W, Buffière J-Y (2007) Nanoscale zoom tomography with hard x rays using Kirkpatrick-Baez optics. Appl Phys Lett 90(14):144104CrossRef
96.
go back to reference Guigay JP, Langer M, Boistel R, Cloetens P (2007) Mixed contrast transfer and transport of intensity approach for phase retrieval in the Fresnel region. Opt Lett 32:1617–1619CrossRef Guigay JP, Langer M, Boistel R, Cloetens P (2007) Mixed contrast transfer and transport of intensity approach for phase retrieval in the Fresnel region. Opt Lett 32:1617–1619CrossRef
97.
go back to reference Langer M, Hesse B, Pacureanu A, Suhonen H, Cloetens P, Raum K, Peyrin F (2013) Priors for x-ray in-line phase tomography of heterogeneous objects. Phil Trans R Soc A 372:20130129CrossRef Langer M, Hesse B, Pacureanu A, Suhonen H, Cloetens P, Raum K, Peyrin F (2013) Priors for x-ray in-line phase tomography of heterogeneous objects. Phil Trans R Soc A 372:20130129CrossRef
98.
go back to reference Langer M, Cloetens P, Hesse B, Pacureanu A, Raum K, Lafage-Proust M-H, Peyrin F (2012) X-ray in-line phase micro-CT for simultaneous bone and soft tissue visualisation. In: Nouvelles m{é}thodologies en imagerie du vivant, p 9581 Langer M, Cloetens P, Hesse B, Pacureanu A, Raum K, Lafage-Proust M-H, Peyrin F (2012) X-ray in-line phase micro-CT for simultaneous bone and soft tissue visualisation. In: Nouvelles m{é}thodologies en imagerie du vivant, p 9581
99.
go back to reference Langer M, Cloetens P, Peyrin F (2009) Fourier-wavelet regularization of phase retrieval in x-ray in-line phase tomography. J Opt Soc Am A Opt Image Sci Vis 26(8):1876–1881CrossRef Langer M, Cloetens P, Peyrin F (2009) Fourier-wavelet regularization of phase retrieval in x-ray in-line phase tomography. J Opt Soc Am A Opt Image Sci Vis 26(8):1876–1881CrossRef
100.
go back to reference Davidoiu V, Sixou B, Langer M, Peyrin F (2011) Non-linear iterative phase retrieval based on Frechet derivative and projection operators. Opt Express 19(23):106–109CrossRef Davidoiu V, Sixou B, Langer M, Peyrin F (2011) Non-linear iterative phase retrieval based on Frechet derivative and projection operators. Opt Express 19(23):106–109CrossRef
101.
go back to reference Davidoiu V, Sixou B, Langer M, Peyrin F (2013) Nonlinear approaches for the single-distance phase retrieval problem involving regularizations with sparsity constraints. Appl Opt 52(17):3977–3986CrossRef Davidoiu V, Sixou B, Langer M, Peyrin F (2013) Nonlinear approaches for the single-distance phase retrieval problem involving regularizations with sparsity constraints. Appl Opt 52(17):3977–3986CrossRef
102.
go back to reference Davidoiu V, Sixou B, Langer M, Peyrin F (2013) In-line phase tomography using nonlinear phase retrieval. Ann Univ Bucharest Math Ser 4(LXII):115–122 Davidoiu V, Sixou B, Langer M, Peyrin F (2013) In-line phase tomography using nonlinear phase retrieval. Ann Univ Bucharest Math Ser 4(LXII):115–122
103.
go back to reference Moosmann J, Hofmann R, Baumbach T (2011) Single-distance phase retrieval at large phase shifts. Opt Express 19:12066–12073CrossRef Moosmann J, Hofmann R, Baumbach T (2011) Single-distance phase retrieval at large phase shifts. Opt Express 19:12066–12073CrossRef
104.
go back to reference Moosmann J, Hofmann R, Bronnikov A, Baumbach T (2010) Nonlinear phase retrieval from single-distance radiograph. Opt Express 18:25771–25785CrossRef Moosmann J, Hofmann R, Bronnikov A, Baumbach T (2010) Nonlinear phase retrieval from single-distance radiograph. Opt Express 18:25771–25785CrossRef
105.
go back to reference Gebhardt W (1906) Ueber funktionell wichtige Anordnungsweisen der groberen und feineren Bauelemente des Wirbeltierknochens. Arch Entw Mech 20:187–322 Gebhardt W (1906) Ueber funktionell wichtige Anordnungsweisen der groberen und feineren Bauelemente des Wirbeltierknochens. Arch Entw Mech 20:187–322
106.
go back to reference Wang Y, Azaïs T, Robin M, Vallée A, Catania C, Legriel P, Pehau-Arnaudet G, Babonneau F, Giraud-Guille M-M, Nassif N (2012) The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite. Nat Mater 11(8):724–733CrossRef Wang Y, Azaïs T, Robin M, Vallée A, Catania C, Legriel P, Pehau-Arnaudet G, Babonneau F, Giraud-Guille M-M, Nassif N (2012) The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite. Nat Mater 11(8):724–733CrossRef
107.
go back to reference Fratzl P, Weinkamer R (2007) Nature’s hierarchical materials. Prog Mater Sci 52(8):1263–1334CrossRef Fratzl P, Weinkamer R (2007) Nature’s hierarchical materials. Prog Mater Sci 52(8):1263–1334CrossRef
108.
go back to reference Ascenzi A, Bonucci E (1967) The tensile properties of single osteons. Anat Rec 158(4):375–386CrossRef Ascenzi A, Bonucci E (1967) The tensile properties of single osteons. Anat Rec 158(4):375–386CrossRef
109.
go back to reference Ascenzi A, Bonucci E (1968) The compressive properties of single osteons. Anat Rec 161(3):377–391CrossRef Ascenzi A, Bonucci E (1968) The compressive properties of single osteons. Anat Rec 161(3):377–391CrossRef
110.
go back to reference Ascenzi A, Bonucci E (1972) The shearing properties of single osteons. Anat Rec 172(3):499–510CrossRef Ascenzi A, Bonucci E (1972) The shearing properties of single osteons. Anat Rec 172(3):499–510CrossRef
111.
go back to reference Ascenzi A, Benvenuti A, Bonucci E (1982) The tensile properties of single osteonic lamellae: technical problems and preliminary results. J Biomech 15(1):29–37CrossRef Ascenzi A, Benvenuti A, Bonucci E (1982) The tensile properties of single osteonic lamellae: technical problems and preliminary results. J Biomech 15(1):29–37CrossRef
112.
go back to reference Giraud-Guille MM (1988) Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif Tissue Int 42(3):167–180CrossRef Giraud-Guille MM (1988) Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif Tissue Int 42(3):167–180CrossRef
113.
go back to reference Marotti G, Muglia MA, Palumbo C (1994) Structure and function of lamellar bone. Clin Rheumatol 13(Suppl 1):63–68 Marotti G, Muglia MA, Palumbo C (1994) Structure and function of lamellar bone. Clin Rheumatol 13(Suppl 1):63–68
114.
go back to reference Weiner S, Arad T, Sabanay I, Traub W (1997) Rotated plywood structure of primary lamellar bone in the rat: orientations of the collagen fibril arrays. Bone 20(6):509–514CrossRef Weiner S, Arad T, Sabanay I, Traub W (1997) Rotated plywood structure of primary lamellar bone in the rat: orientations of the collagen fibril arrays. Bone 20(6):509–514CrossRef
115.
go back to reference Ascenzi MG, Ascenzi A, Benvenuti A, Burghammer M, Panzavolta S, Bigi A (2003) Structural differences between ‘dark’ and ‘bright’ isolated human osteonic lamellae. J Struct Biol 141(1):22–33CrossRef Ascenzi MG, Ascenzi A, Benvenuti A, Burghammer M, Panzavolta S, Bigi A (2003) Structural differences between ‘dark’ and ‘bright’ isolated human osteonic lamellae. J Struct Biol 141(1):22–33CrossRef
116.
go back to reference Ascenzi M-G, Lomovtsev A (2006) Collagen orientation patterns in human secondary osteons, quantified in the radial direction by confocal microscopy. J Struct Biol 153(1):14–30CrossRef Ascenzi M-G, Lomovtsev A (2006) Collagen orientation patterns in human secondary osteons, quantified in the radial direction by confocal microscopy. J Struct Biol 153(1):14–30CrossRef
117.
go back to reference Hofmann T, Heyroth F, Meinhard H, Fränzel W, Raum K (2006) Assessment of composition and anisotropic elastic properties of secondary osteon lamellae. J Biomech 39(12):2282–2294CrossRef Hofmann T, Heyroth F, Meinhard H, Fränzel W, Raum K (2006) Assessment of composition and anisotropic elastic properties of secondary osteon lamellae. J Biomech 39(12):2282–2294CrossRef
118.
go back to reference Kazanci M, Wagner HD, Manjubala NI, Gupta HS, Paschalis E, Roschger P, Fratzl P (2007) Raman imaging of two orthogonal planes within cortical bone. Bone 41(3):456–461CrossRef Kazanci M, Wagner HD, Manjubala NI, Gupta HS, Paschalis E, Roschger P, Fratzl P (2007) Raman imaging of two orthogonal planes within cortical bone. Bone 41(3):456–461CrossRef
119.
go back to reference Spiesz EM, Kaminsky W, Zysset PK (2011) A quantitative collagen fibers orientation assessment using birefringence measurements: calibration and application to human osteons. J Struct Biol 176(3):302–306CrossRef Spiesz EM, Kaminsky W, Zysset PK (2011) A quantitative collagen fibers orientation assessment using birefringence measurements: calibration and application to human osteons. J Struct Biol 176(3):302–306CrossRef
120.
go back to reference Gourrier A, Wagermaier W, Burghammer M, Lammie D, Gupta HS, Fratzl P, Riekel C, Wess TJ, Paris O (2007) Scanning x-ray imaging with small-angle scattering contrast. J Appl Crystallogr 40(s1):s78–s82CrossRef Gourrier A, Wagermaier W, Burghammer M, Lammie D, Gupta HS, Fratzl P, Riekel C, Wess TJ, Paris O (2007) Scanning x-ray imaging with small-angle scattering contrast. J Appl Crystallogr 40(s1):s78–s82CrossRef
121.
go back to reference Seidel R, Gourrier A, Kerschnitzki M, Burghammer M, Fratzl P, Gupta HS, Wagermaier W (2011) Synchrotron 3D SAXS analysis of bone nanostructure. Bioinspired Biomim Nanobiomaterials 1:123–131CrossRef Seidel R, Gourrier A, Kerschnitzki M, Burghammer M, Fratzl P, Gupta HS, Wagermaier W (2011) Synchrotron 3D SAXS analysis of bone nanostructure. Bioinspired Biomim Nanobiomaterials 1:123–131CrossRef
122.
go back to reference Granke M, Gourrier A, Rupin F, Raum K, Peyrin F, Burghammer M, Saïed A, Laugier P (2013) Microfibril orientation dominates the microelastic properties of human bone tissue at the lamellar length scale. PLoS One 8(3), e58043CrossRef Granke M, Gourrier A, Rupin F, Raum K, Peyrin F, Burghammer M, Saïed A, Laugier P (2013) Microfibril orientation dominates the microelastic properties of human bone tissue at the lamellar length scale. PLoS One 8(3), e58043CrossRef
123.
go back to reference Wagermaier W, Gupta HS, Gourrier A, Paris O, Roschger P, Burghammer M, Riekel C, Fratzl P (2007) Scanning texture analysis of lamellar bone using microbeam synchrotron x-ray radiation. J Appl Crystallogr 40(1):115–120CrossRef Wagermaier W, Gupta HS, Gourrier A, Paris O, Roschger P, Burghammer M, Riekel C, Fratzl P (2007) Scanning texture analysis of lamellar bone using microbeam synchrotron x-ray radiation. J Appl Crystallogr 40(1):115–120CrossRef
124.
go back to reference Wagermaier W, Gupta HS, Gourrier A, Burghammer M, Roschger P, Fratzl P (2006) Spiral twisting of fiber orientation inside bone lamellae. Biointerphases 1(1):1CrossRef Wagermaier W, Gupta HS, Gourrier A, Burghammer M, Roschger P, Fratzl P (2006) Spiral twisting of fiber orientation inside bone lamellae. Biointerphases 1(1):1CrossRef
125.
go back to reference Marotti G (1993) A new theory of bone lamellation. Calcif Tissue Int 53(Suppl 1):S47–S55; discussion S56CrossRef Marotti G (1993) A new theory of bone lamellation. Calcif Tissue Int 53(Suppl 1):S47–S55; discussion S56CrossRef
126.
go back to reference Marotti G, Ferretti M, Palumbo C (2013) The problem of bone lamellation: an attempt to explain different proposed models. J Morphol 274(5):543–550CrossRef Marotti G, Ferretti M, Palumbo C (2013) The problem of bone lamellation: an attempt to explain different proposed models. J Morphol 274(5):543–550CrossRef
127.
go back to reference Varga P, Pacureanu A, Langer M, Suhonen H, Hesse B, Grimal Q, Cloetens P, Raum K, Peyrin F (2013) Investigation of the 3D orientation of mineralized collagen fibrils in human lamellar bone using synchrotron x-ray phase nano-tomography. Acta Biomater 9:8118–8127CrossRef Varga P, Pacureanu A, Langer M, Suhonen H, Hesse B, Grimal Q, Cloetens P, Raum K, Peyrin F (2013) Investigation of the 3D orientation of mineralized collagen fibrils in human lamellar bone using synchrotron x-ray phase nano-tomography. Acta Biomater 9:8118–8127CrossRef
128.
go back to reference Rho JY, Kuhn-Spearing L, Zioupos P (1998) Mechanical properties and the hierarchical structure of bone. Med Eng Phys 20(2):92–102CrossRef Rho JY, Kuhn-Spearing L, Zioupos P (1998) Mechanical properties and the hierarchical structure of bone. Med Eng Phys 20(2):92–102CrossRef
129.
go back to reference Ritchie RO (2011) The conflicts between strength and toughness. Nat Mater 10(11):817–822CrossRef Ritchie RO (2011) The conflicts between strength and toughness. Nat Mater 10(11):817–822CrossRef
130.
go back to reference Marotti G (1993) Calcified tissue a new theory of bone lamellation, vol 53 Marotti G (1993) Calcified tissue a new theory of bone lamellation, vol 53
131.
go back to reference Gupta HS, Stachewicz U, Wagermaier W, Roschger P, Wagner HD, Fratzl P (2006) Mechanical modulation at the lamellar level in osteonal bone. J Mater Res 21:1913–1921CrossRef Gupta HS, Stachewicz U, Wagermaier W, Roschger P, Wagner HD, Fratzl P (2006) Mechanical modulation at the lamellar level in osteonal bone. J Mater Res 21:1913–1921CrossRef
132.
go back to reference Reisinger AG, Pahr DH, Zysset PK (2011) Elastic anisotropy of bone lamellae as a function of fibril orientation pattern. Biomech Model Mechanobiol 10(1):67–77CrossRef Reisinger AG, Pahr DH, Zysset PK (2011) Elastic anisotropy of bone lamellae as a function of fibril orientation pattern. Biomech Model Mechanobiol 10(1):67–77CrossRef
133.
go back to reference Carnelli D, Vena P, Dao M, Ortiz C, Contro R (2013) Orientation and size-dependent mechanical modulation within individual secondary osteons in cortical bone tissue. J R Soc Interface 10(81):20120953CrossRef Carnelli D, Vena P, Dao M, Ortiz C, Contro R (2013) Orientation and size-dependent mechanical modulation within individual secondary osteons in cortical bone tissue. J R Soc Interface 10(81):20120953CrossRef
134.
go back to reference Faingold A, Cohen SR, Reznikov N, Wagner HD (2013) Osteonal lamellae elementary units: lamellar microstructure, curvature and mechanical properties. Acta Biomater 9(4):5956–5962CrossRef Faingold A, Cohen SR, Reznikov N, Wagner HD (2013) Osteonal lamellae elementary units: lamellar microstructure, curvature and mechanical properties. Acta Biomater 9(4):5956–5962CrossRef
135.
go back to reference Chen X, Nadiarynkh O, Plotnikov S, Campagnola PJ (2012) Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat Protoc 7(4):654–669CrossRef Chen X, Nadiarynkh O, Plotnikov S, Campagnola PJ (2012) Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat Protoc 7(4):654–669CrossRef
136.
go back to reference Williams RM, Zipfel WR, Webb WW (2005) Interpreting second-harmonic generation images of collagen I fibrils. Biophys J 88(2):1377–1386CrossRef Williams RM, Zipfel WR, Webb WW (2005) Interpreting second-harmonic generation images of collagen I fibrils. Biophys J 88(2):1377–1386CrossRef
137.
go back to reference Currey JD, Shahar R (2013) Cavities in the compact bone in tetrapods and fish and their effect on mechanical properties. J Struct Biol 183(2):107–122CrossRef Currey JD, Shahar R (2013) Cavities in the compact bone in tetrapods and fish and their effect on mechanical properties. J Struct Biol 183(2):107–122CrossRef
138.
go back to reference Qing H, Ardeshirpour L, Pajevic PD, Dusevich V, Jähn K, Kato S, Wysolmerski J, Bonewald LF (2012) Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J Bone Miner Res 27(5):1018–1029CrossRef Qing H, Ardeshirpour L, Pajevic PD, Dusevich V, Jähn K, Kato S, Wysolmerski J, Bonewald LF (2012) Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J Bone Miner Res 27(5):1018–1029CrossRef
139.
go back to reference Webster DJ, Schneider P, Dallas SL, Müller R (2013) Studying osteocytes within their environment. Bone (in press) Webster DJ, Schneider P, Dallas SL, Müller R (2013) Studying osteocytes within their environment. Bone (in press)
140.
go back to reference Vatsa A, Breuls RG, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2008) Osteocyte morphology in fibula and calvaria – is there a role for mechanosensing? Bone 43(3):452–458CrossRef Vatsa A, Breuls RG, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2008) Osteocyte morphology in fibula and calvaria – is there a role for mechanosensing? Bone 43(3):452–458CrossRef
141.
go back to reference Hannah KM, Thomas CDL, Clement JG, De Carlo F, Peele AG (2010) Bimodal distribution of osteocyte lacunar size in the human femoral cortex as revealed by micro-CT. Bone 47(5):866–871CrossRef Hannah KM, Thomas CDL, Clement JG, De Carlo F, Peele AG (2010) Bimodal distribution of osteocyte lacunar size in the human femoral cortex as revealed by micro-CT. Bone 47(5):866–871CrossRef
142.
go back to reference Hesse B, Männicke N, Pacureanu A, Varga P, Langer M, Maurer P, Peyrin F, Raum K (2014) Accessing osteocyte lacunar geometrical properties in human jaw bone on the submicron length scale using synchrotron radiation μCT. J Microsc 255(3):158–168CrossRef Hesse B, Männicke N, Pacureanu A, Varga P, Langer M, Maurer P, Peyrin F, Raum K (2014) Accessing osteocyte lacunar geometrical properties in human jaw bone on the submicron length scale using synchrotron radiation μCT. J Microsc 255(3):158–168CrossRef
143.
go back to reference Dong P, Pacureanu A, Zuluaga MA, Olivier C, Grimal Q, Peyrin F (2014) Quantification of the 3D morphology of the bone cell network from synchrotron micro-ct images. Image Anal Stereol 33(2):157CrossRef Dong P, Pacureanu A, Zuluaga MA, Olivier C, Grimal Q, Peyrin F (2014) Quantification of the 3D morphology of the bone cell network from synchrotron micro-ct images. Image Anal Stereol 33(2):157CrossRef
144.
go back to reference Mullender MG, Tan SD, Vico L, Alexandre C, Klein-Nulend J (2005) Differences in osteocyte density and bone histomorphometry between men and women and between healthy and osteoporotic subjects. Calcif Tissue Int 77(5):291–296CrossRef Mullender MG, Tan SD, Vico L, Alexandre C, Klein-Nulend J (2005) Differences in osteocyte density and bone histomorphometry between men and women and between healthy and osteoporotic subjects. Calcif Tissue Int 77(5):291–296CrossRef
145.
go back to reference Knothe Tate ML, Tami A, Bauer TW, Knothe U (2002) Micropathoanatomy of osteoporosis – indications for a cellular basis of bone disease. Adv Osteoporotic Fract Manag 2(1):9–14 Knothe Tate ML, Tami A, Bauer TW, Knothe U (2002) Micropathoanatomy of osteoporosis – indications for a cellular basis of bone disease. Adv Osteoporotic Fract Manag 2(1):9–14
146.
go back to reference Loiselle AE, Jiang JX, Donahue HJ (2013) Gap junction and hemichannel functions in osteocytes. Bone 54(2):205–212CrossRef Loiselle AE, Jiang JX, Donahue HJ (2013) Gap junction and hemichannel functions in osteocytes. Bone 54(2):205–212CrossRef
147.
go back to reference Price C, Zhou X, Li W, Wang L (2011) Real-time measurement of solute transport within the lacunar-canalicular system of mechanically loaded bone: direct evidence for load-induced fluid flow. J Bone Miner Res 26(2):277–285CrossRef Price C, Zhou X, Li W, Wang L (2011) Real-time measurement of solute transport within the lacunar-canalicular system of mechanically loaded bone: direct evidence for load-induced fluid flow. J Bone Miner Res 26(2):277–285CrossRef
148.
go back to reference You L-D, Weinbaum S, Cowin SC, Schaffler MB (2004) Ultrastructure of the osteocyte process and its pericellular matrix. Anat Rec A: Discov Mol Cell Evol Biol 278(2):505–513CrossRef You L-D, Weinbaum S, Cowin SC, Schaffler MB (2004) Ultrastructure of the osteocyte process and its pericellular matrix. Anat Rec A: Discov Mol Cell Evol Biol 278(2):505–513CrossRef
149.
go back to reference Wang Y, McNamara LM, Schaffler MB, Weinbaum S (2007) A model for the role of integrins in flow induced mechanotransduction in osteocytes. Proc Natl Acad Sci U S A 104(40):15941–15946CrossRef Wang Y, McNamara LM, Schaffler MB, Weinbaum S (2007) A model for the role of integrins in flow induced mechanotransduction in osteocytes. Proc Natl Acad Sci U S A 104(40):15941–15946CrossRef
150.
go back to reference Nguyen AM, Jacobs CR (2013) Emerging role of primary cilia as mechanosensors in osteocytes. Bone 54(2):196–204CrossRef Nguyen AM, Jacobs CR (2013) Emerging role of primary cilia as mechanosensors in osteocytes. Bone 54(2):196–204CrossRef
151.
go back to reference Stern AR, Nicolella DP (2013) Measurement and estimation of osteocyte mechanical strain. Bone 54(2):191–195CrossRef Stern AR, Nicolella DP (2013) Measurement and estimation of osteocyte mechanical strain. Bone 54(2):191–195CrossRef
152.
go back to reference Group M, Hero S, Burr DB (1996) In vivo measurement of human tibial strains during vigorous activity 18(5) Group M, Hero S, Burr DB (1996) In vivo measurement of human tibial strains during vigorous activity 18(5)
153.
go back to reference You L, Cowin SC, Schaffler MB, Weinbaum S (2001) A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech 34(11):1375–1386CrossRef You L, Cowin SC, Schaffler MB, Weinbaum S (2001) A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech 34(11):1375–1386CrossRef
154.
go back to reference Nicolella DP, Moravits DE, Gale AM, Bonewald LF, Lankford J (2006) Osteocyte lacunae tissue strain in cortical bone. J Biomech 39(9):1735–1743CrossRef Nicolella DP, Moravits DE, Gale AM, Bonewald LF, Lankford J (2006) Osteocyte lacunae tissue strain in cortical bone. J Biomech 39(9):1735–1743CrossRef
155.
go back to reference Weinbaum S, Cowin SC, Zeng Y (1994) A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 27(3):339–360CrossRef Weinbaum S, Cowin SC, Zeng Y (1994) A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 27(3):339–360CrossRef
156.
go back to reference Han Y, Cowin SC, Schaffler MB, Weinbaum S (2004) Mechanotransduction and strain amplification in osteocyte cell processes. Proc Natl Acad Sci U S A 101(47):16689–16694CrossRef Han Y, Cowin SC, Schaffler MB, Weinbaum S (2004) Mechanotransduction and strain amplification in osteocyte cell processes. Proc Natl Acad Sci U S A 101(47):16689–16694CrossRef
157.
go back to reference McCreadie BR, Hollister SJ, Schaffler MB, Goldstein SA (2004) Osteocyte lacuna size and shape in women with and without osteoporotic fracture. J Biomech 37(4):563–572CrossRef McCreadie BR, Hollister SJ, Schaffler MB, Goldstein SA (2004) Osteocyte lacuna size and shape in women with and without osteoporotic fracture. J Biomech 37(4):563–572CrossRef
158.
go back to reference Bonivtch AR, Bonewald LF, Nicolella DP (2007) Tissue strain amplification at the osteocyte lacuna: a microstructural finite element analysis. J Biomech 40(10):2199–2206CrossRef Bonivtch AR, Bonewald LF, Nicolella DP (2007) Tissue strain amplification at the osteocyte lacuna: a microstructural finite element analysis. J Biomech 40(10):2199–2206CrossRef
159.
go back to reference Deligianni DD, Apostolopoulos CA (2008) Multilevel finite element modeling for the prediction of local cellular deformation in bone. Biomech Model Mechanobiol 7(2):151–159CrossRef Deligianni DD, Apostolopoulos CA (2008) Multilevel finite element modeling for the prediction of local cellular deformation in bone. Biomech Model Mechanobiol 7(2):151–159CrossRef
160.
go back to reference Anderson EJ, Knothe Tate ML (2008) Idealization of pericellular fluid space geometry and dimension results in a profound underprediction of nano-microscale stresses imparted by fluid drag on osteocytes. J Biomech 41(8):1736–1746CrossRef Anderson EJ, Knothe Tate ML (2008) Idealization of pericellular fluid space geometry and dimension results in a profound underprediction of nano-microscale stresses imparted by fluid drag on osteocytes. J Biomech 41(8):1736–1746CrossRef
161.
go back to reference Rath AL, Bonewald LF, Ling J, Jiang JX, Van Dyke ME, Nicolella DP (2010) Correlation of cell strain in single osteocytes with intracellular calcium, but not intracellular nitric oxide, in response to fluid flow. J Biomech 43(8):1560–1564CrossRef Rath AL, Bonewald LF, Ling J, Jiang JX, Van Dyke ME, Nicolella DP (2010) Correlation of cell strain in single osteocytes with intracellular calcium, but not intracellular nitric oxide, in response to fluid flow. J Biomech 43(8):1560–1564CrossRef
162.
go back to reference Schneider P, Ruffoni D, Larsson D, Chiapparini I, Müller R (2012) Image-based finite element models for the investigation of osteocyte mechanotransduction. J Biomech 45(1):S436CrossRef Schneider P, Ruffoni D, Larsson D, Chiapparini I, Müller R (2012) Image-based finite element models for the investigation of osteocyte mechanotransduction. J Biomech 45(1):S436CrossRef
163.
go back to reference Cardoso L, Fritton SP, Gailani G, Benalla M, Cowin SC (2013) Advances in assessment of bone porosity, permeability and interstitial fluid flow. J Biomech 46(2):253–265CrossRef Cardoso L, Fritton SP, Gailani G, Benalla M, Cowin SC (2013) Advances in assessment of bone porosity, permeability and interstitial fluid flow. J Biomech 46(2):253–265CrossRef
164.
go back to reference Marotti G (1990) The original contributions of the scanning electron microscope to the knowledge of bone structure. In: Bonucci E, Motta PM (eds) Ultrastructure of skeletal tissues SE – 2, vol 7. Springer, pp 19–39 Marotti G (1990) The original contributions of the scanning electron microscope to the knowledge of bone structure. In: Bonucci E, Motta PM (eds) Ultrastructure of skeletal tissues SE – 2, vol 7. Springer, pp 19–39
165.
go back to reference Kerschnitzki M, Wagermaier W, Liu Y, Roschger P, Duda GN, Fratzl P (2011) Poorly ordered bone as an endogenous scaffold for the deposition of highly oriented lamellar tissue in rapidly growing ovine bone. Cells Tissues Organs 194(2–4):119–123CrossRef Kerschnitzki M, Wagermaier W, Liu Y, Roschger P, Duda GN, Fratzl P (2011) Poorly ordered bone as an endogenous scaffold for the deposition of highly oriented lamellar tissue in rapidly growing ovine bone. Cells Tissues Organs 194(2–4):119–123CrossRef
166.
go back to reference Sharma D, Ciani C, Marin PAR, Levy JD, Doty SB, Fritton SP (2012) Alterations in the osteocyte lacunar-canalicular microenvironment due to estrogen deficiency. Bone 51(3):488–497CrossRef Sharma D, Ciani C, Marin PAR, Levy JD, Doty SB, Fritton SP (2012) Alterations in the osteocyte lacunar-canalicular microenvironment due to estrogen deficiency. Bone 51(3):488–497CrossRef
167.
go back to reference Kerschnitzki M, Kollmannsberger P, Burghammer M, Duda GN, Weinkamer R, Wagermaier W, Fratzl P (2013) Architecture of the osteocyte network correlates with bone material quality. J Bone Miner Res 28(8):1837–1845CrossRef Kerschnitzki M, Kollmannsberger P, Burghammer M, Duda GN, Weinkamer R, Wagermaier W, Fratzl P (2013) Architecture of the osteocyte network correlates with bone material quality. J Bone Miner Res 28(8):1837–1845CrossRef
168.
go back to reference Varga P, Hesse B, Langer M, Schrof S, Männicke N, Suhonen H, Pacureanu A, Pahr D, Peyrin F, Raum K (2015) Synchrotron x-ray phase nano-tomography-based analysis of the lacunar-canalicular network morphology and its relation to the strains experienced by osteocytes in situ as predicted by case-specific finite element analysis. Biomech Model Mechanobiol 14(2):267–282CrossRef Varga P, Hesse B, Langer M, Schrof S, Männicke N, Suhonen H, Pacureanu A, Pahr D, Peyrin F, Raum K (2015) Synchrotron x-ray phase nano-tomography-based analysis of the lacunar-canalicular network morphology and its relation to the strains experienced by osteocytes in situ as predicted by case-specific finite element analysis. Biomech Model Mechanobiol 14(2):267–282CrossRef
169.
go back to reference McNamara LM, Majeska RJ, Weinbaum S, Friedrich V, Schaffler MB (2009) Attachment of osteocyte cell processes to the bone matrix. Anat Rec 292(3):355–363CrossRef McNamara LM, Majeska RJ, Weinbaum S, Friedrich V, Schaffler MB (2009) Attachment of osteocyte cell processes to the bone matrix. Anat Rec 292(3):355–363CrossRef
170.
go back to reference Wu D, Ganatos P, Spray DC, Weinbaum S (2011) On the electrophysiological response of bone cells using a Stokesian fluid stimulus probe for delivery of quantifiable localized picoNewton level forces. J Biomech 44(9):1702–1708CrossRef Wu D, Ganatos P, Spray DC, Weinbaum S (2011) On the electrophysiological response of bone cells using a Stokesian fluid stimulus probe for delivery of quantifiable localized picoNewton level forces. J Biomech 44(9):1702–1708CrossRef
171.
go back to reference Weiner S, Traub W (1992) Bone structure: from angstroms to microns. FASEB J 6(3):879–885 Weiner S, Traub W (1992) Bone structure: from angstroms to microns. FASEB J 6(3):879–885
172.
go back to reference Parfitt AM (2003) Misconceptions (3): calcium leaves bone only by resorption and enters only by formation. Bone 33(3):259–263CrossRef Parfitt AM (2003) Misconceptions (3): calcium leaves bone only by resorption and enters only by formation. Bone 33(3):259–263CrossRef
173.
go back to reference Marenzana M, Shipley AM, Squitiero P, Kunkel JG, Rubinacci A (2005) Bone as an ion exchange organ: evidence for instantaneous cell-dependent calcium efflux from bone not due to resorption. Bone 37(4):545–554CrossRef Marenzana M, Shipley AM, Squitiero P, Kunkel JG, Rubinacci A (2005) Bone as an ion exchange organ: evidence for instantaneous cell-dependent calcium efflux from bone not due to resorption. Bone 37(4):545–554CrossRef
174.
go back to reference Pirklbauer M, Mayer G (2011) The exchangeable calcium pool: physiology and pathophysiology in chronic kidney disease. Nephrol Dial Transplant 26(8):2438–2444CrossRef Pirklbauer M, Mayer G (2011) The exchangeable calcium pool: physiology and pathophysiology in chronic kidney disease. Nephrol Dial Transplant 26(8):2438–2444CrossRef
175.
go back to reference Talmage RV, Mobley HT (2008) Calcium homeostasis: reassessment of the actions of parathyroid hormone. Gen Comp Endocrinol 156(1):1–8CrossRef Talmage RV, Mobley HT (2008) Calcium homeostasis: reassessment of the actions of parathyroid hormone. Gen Comp Endocrinol 156(1):1–8CrossRef
176.
go back to reference Atkins GJ, Findlay DM (2012) Osteocyte regulation of bone mineral: a little give and take. Osteoporos Int 23(8):2067–2079CrossRef Atkins GJ, Findlay DM (2012) Osteocyte regulation of bone mineral: a little give and take. Osteoporos Int 23(8):2067–2079CrossRef
177.
go back to reference Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldberg HA (1996) Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins. Biochem J 317(Pt 1):59–64CrossRef Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldberg HA (1996) Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins. Biochem J 317(Pt 1):59–64CrossRef
178.
go back to reference Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-Hora M, Feng JQ, Bonewald LF, Kodama T, Wutz A, Wagner EF, Penninger JM, Takayanagi H (2011) Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med 17(10):1231–1234CrossRef Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-Hora M, Feng JQ, Bonewald LF, Kodama T, Wutz A, Wagner EF, Penninger JM, Takayanagi H (2011) Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med 17(10):1231–1234CrossRef
179.
go back to reference Feng JQ, Clinkenbeard EL, Yuan B, White KE, Drezner MK (2013) Osteocyte regulation of phosphate homeostasis and bone mineralization underlies the pathophysiology of the heritable disorders of rickets and osteomalacia. Bone 54(2):213–221CrossRef Feng JQ, Clinkenbeard EL, Yuan B, White KE, Drezner MK (2013) Osteocyte regulation of phosphate homeostasis and bone mineralization underlies the pathophysiology of the heritable disorders of rickets and osteomalacia. Bone 54(2):213–221CrossRef
180.
go back to reference Bélanger LF, Bélanger C, Semba T (1967) Technical approaches leading to the concept of osteocytic osteolysis. Clin Orthop Relat Res 54:187–196 Bélanger LF, Bélanger C, Semba T (1967) Technical approaches leading to the concept of osteocytic osteolysis. Clin Orthop Relat Res 54:187–196
181.
go back to reference Blaber EA, Dvorochkin N, Lee C, Alwood JS, Yousuf R, Pianetta P, Globus RK, Burns BP, Almeida EAC (2013) Microgravity induces pelvic bone loss through osteoclastic activity, osteocytic osteolysis, and osteoblastic cell cycle inhibition by CDKN1a/p21. PLoS One 8(4), e61372CrossRef Blaber EA, Dvorochkin N, Lee C, Alwood JS, Yousuf R, Pianetta P, Globus RK, Burns BP, Almeida EAC (2013) Microgravity induces pelvic bone loss through osteoclastic activity, osteocytic osteolysis, and osteoblastic cell cycle inhibition by CDKN1a/p21. PLoS One 8(4), e61372CrossRef
182.
go back to reference Lane NE, Yao W, Balooch M, Nalla RK, Balooch G, Habelitz S, Kinney JH, Bonewald LF (2006) 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(3):466–476CrossRef Lane NE, Yao W, Balooch M, Nalla RK, Balooch G, Habelitz S, Kinney JH, Bonewald LF (2006) 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(3):466–476CrossRef
183.
go back to reference Tommasini SM, Trinward A, Acerbo AS, De Carlo F, Miller LM, Judex S (2012) Changes in intracortical microporosities induced by pharmaceutical treatment of osteoporosis as detected by high resolution micro-CT. Bone 50(3):596–604CrossRef Tommasini SM, Trinward A, Acerbo AS, De Carlo F, Miller LM, Judex S (2012) Changes in intracortical microporosities induced by pharmaceutical treatment of osteoporosis as detected by high resolution micro-CT. Bone 50(3):596–604CrossRef
184.
go back to reference Qing H, Bonewald LF (2009) Osteocyte remodeling of the perilacunar and pericanalicular matrix. Int J Oral Sci 1(2):59–65CrossRef Qing H, Bonewald LF (2009) Osteocyte remodeling of the perilacunar and pericanalicular matrix. Int J Oral Sci 1(2):59–65CrossRef
185.
go back to reference Rubin MA, Rubin J, Jasiuk I (2004) SEM and TEM study of the hierarchical structure of C57BL/6J and C3H/HeJ mice trabecular bone. Bone 35(1):11–20CrossRef Rubin MA, Rubin J, Jasiuk I (2004) SEM and TEM study of the hierarchical structure of C57BL/6J and C3H/HeJ mice trabecular bone. Bone 35(1):11–20CrossRef
Metadata
Title
Synchrotron X-Ray Phase Nanotomography for Bone Tissue Characterization
Authors
Peter Varga
Loriane Weber
Bernhard Hesse
Max Langer
Copyright Year
2016
Publisher
Springer Berlin Heidelberg
DOI
https://doi.org/10.1007/978-3-662-48606-1_1

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