Abstract

The three-dimensional network of lacunae and canaliculi that regulates metabolism in bone contains osteocytes and their dendritic processes. We constructed a synchrotron radiation X-ray microscope for sequential tomography of mouse tibia first by using a Talbot interferometer to detect the degree of bone mineralization and then by using absorption contrast under a slightly defocused setting to enhance outline contrast thereby visualizing structures of the osteocyte lacuno-canalicular network. The resultant pair of tomograms was precisely aligned with each other, allowing evaluation of mineral density in the vicinity of each osteocyte lacuna and canaliculus over the entire thickness of the cortical bone. Thus, multiscan microscopic X-ray tomography is a powerful tool for analyzing bone mineralization in relation to the lacuno-canalicular network at the submicron resolution level.

© 2013 OSA

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  1. K. Matsuo and N. Irie, “Osteoclast-osteoblast communication,” Arch. Biochem. Biophys.473(2), 201–209 (2008).
    [CrossRef] [PubMed]
  2. L. F. Bonewald, “The amazing osteocyte,” J. Bone Miner. Res.26(2), 229–238 (2011).
    [CrossRef] [PubMed]
  3. L. D. You, S. Weinbaum, S. C. Cowin, and M. B. Schaffler, “Ultrastructure of the osteocyte process and its pericellular matrix,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol.278A(2), 505–513 (2004).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  6. H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  8. C. Ciani, S. B. Doty, and S. P. Fritton, “An effective histological staining process to visualize bone interstitial fluid space using confocal microscopy,” Bone44(5), 1015–1017 (2009).
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  11. A. Pacureanu, M. Langer, E. Boller, P. Tafforeau, and F. Peyrin, “Nanoscale imaging of the bone cell network with synchrotron X-ray tomography: optimization of acquisition setup,” Med. Phys.39(4), 2229–2238 (2012).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef]
  16. A. Momose, T. Takeda, Y. Itai, and K. Hirano, “Phase-contrast X-ray computed tomography for observing biological soft tissues,” Nat. Med.2(4), 473–475 (1996).
    [CrossRef] [PubMed]
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    [CrossRef]
  18. Y. Takeda, W. Yashiro, T. Hattori, A. Takeuchi, Y. Suzuki, and A. Momose, “Differential phase X-ray imaging microscopy with X-ray Talbot interferometer,” Appl. Phys. Express1, 117002 (2008).
    [CrossRef]
  19. A. Snigirev, I. Snigireva, V. Kohn, S. Kuznetsov, and I. Schelokov, “On the possibilities of X-ray phase contrast microimaging by coherent high‐energy synchrotron radiation,” Rev. Sci. Instrum.66(12), 5486–5492 (1995).
    [CrossRef]
  20. S. W. Wilkins, T. E. Gureyev, D. Gao, A. Pogany, and A. W. Stevenson, “Phase-contrast imaging using polychromatic hard X-rays,” Nature384(6607), 335–338 (1996).
    [CrossRef]
  21. S. Mayo, T. Davis, T. Gureyev, P. Miller, D. Paganin, A. Pogany, A. Stevenson, and S. Wilkins, “X-ray phase-contrast microscopy and microtomography,” Opt. Express11(19), 2289–2302 (2003).
    [CrossRef] [PubMed]

2013 (1)

J. J. Wysolmerski, “Osteocytes remove and replace perilacunar mineral during reproductive cycles,” Bone54(2), 230–236 (2013).
[CrossRef] [PubMed]

2012 (4)

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

A. Pacureanu, M. Langer, E. Boller, P. Tafforeau, and F. Peyrin, “Nanoscale imaging of the bone cell network with synchrotron X-ray tomography: optimization of acquisition setup,” Med. Phys.39(4), 2229–2238 (2012).
[CrossRef] [PubMed]

M. Langer, A. Pacureanu, H. Suhonen, Q. Grimal, P. Cloetens, and F. Peyrin, “X-ray phase nanotomography resolves the 3D human bone ultrastructure,” PLoS ONE7(8), e35691 (2012).
[CrossRef] [PubMed]

H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
[CrossRef] [PubMed]

2011 (1)

L. F. Bonewald, “The amazing osteocyte,” J. Bone Miner. Res.26(2), 229–238 (2011).
[CrossRef] [PubMed]

2010 (3)

P. Schneider, M. Meier, R. Wepf, and R. Müller, “Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network,” Bone47(5), 848–858 (2010).
[CrossRef] [PubMed]

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

M. Dierolf, A. Menzel, P. Thibault, P. Schneider, C. M. Kewish, R. Wepf, O. Bunk, and F. Pfeiffer, “Ptychographic X-ray computed tomography at the nanoscale,” Nature467(7314), 436–439 (2010).
[CrossRef] [PubMed]

2009 (2)

C. Ciani, S. B. Doty, and S. P. Fritton, “An effective histological staining process to visualize bone interstitial fluid space using confocal microscopy,” Bone44(5), 1015–1017 (2009).
[CrossRef] [PubMed]

A. Teti and A. Zallone, “Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited,” Bone44(1), 11–16 (2009).
[CrossRef] [PubMed]

2008 (2)

K. Matsuo and N. Irie, “Osteoclast-osteoblast communication,” Arch. Biochem. Biophys.473(2), 201–209 (2008).
[CrossRef] [PubMed]

Y. Takeda, W. Yashiro, T. Hattori, A. Takeuchi, Y. Suzuki, and A. Momose, “Differential phase X-ray imaging microscopy with X-ray Talbot interferometer,” Appl. Phys. Express1, 117002 (2008).
[CrossRef]

2006 (1)

A. Momose, W. Yashiro, Y. Takeda, Y. Suzuki, and T. Hattori, “Phase tomography by X-ray Talbot interferometry for biological Imaging,” Jpn. J. Appl. Phys.45(6A), 5254–5262 (2006).
[CrossRef]

2004 (1)

L. D. You, S. Weinbaum, S. C. Cowin, and M. B. Schaffler, “Ultrastructure of the osteocyte process and its pericellular matrix,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol.278A(2), 505–513 (2004).
[CrossRef] [PubMed]

2003 (2)

A. Momose, S. Kawamoto, I. Koyama, Y. Hamaishi, K. Takai, and Y. Suzuki, “Demonstration of X-ray Talbot interferometry,” Jpn. J. Appl. Phys.42(Part 2, No. 7B), L866–L868 (2003).
[CrossRef]

S. Mayo, T. Davis, T. Gureyev, P. Miller, D. Paganin, A. Pogany, A. Stevenson, and S. Wilkins, “X-ray phase-contrast microscopy and microtomography,” Opt. Express11(19), 2289–2302 (2003).
[CrossRef] [PubMed]

1996 (2)

S. W. Wilkins, T. E. Gureyev, D. Gao, A. Pogany, and A. W. Stevenson, “Phase-contrast imaging using polychromatic hard X-rays,” Nature384(6607), 335–338 (1996).
[CrossRef]

A. Momose, T. Takeda, Y. Itai, and K. Hirano, “Phase-contrast X-ray computed tomography for observing biological soft tissues,” Nat. Med.2(4), 473–475 (1996).
[CrossRef] [PubMed]

1995 (1)

A. Snigirev, I. Snigireva, V. Kohn, S. Kuznetsov, and I. Schelokov, “On the possibilities of X-ray phase contrast microimaging by coherent high‐energy synchrotron radiation,” Rev. Sci. Instrum.66(12), 5486–5492 (1995).
[CrossRef]

1969 (1)

L. F. Bélanger, “Osteocytic osteolysis,” Calcif. Tissue Res.4(1), 1–12 (1969).
[CrossRef] [PubMed]

Adachi, T.

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

Almeida, E.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Alwood, J. S.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Andrews, J. C.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Ardeshirpour, L.

H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
[CrossRef] [PubMed]

Bacabac, R. G.

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

Bakker, A. D.

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

Bélanger, L. F.

L. F. Bélanger, “Osteocytic osteolysis,” Calcif. Tissue Res.4(1), 1–12 (1969).
[CrossRef] [PubMed]

Boller, E.

A. Pacureanu, M. Langer, E. Boller, P. Tafforeau, and F. Peyrin, “Nanoscale imaging of the bone cell network with synchrotron X-ray tomography: optimization of acquisition setup,” Med. Phys.39(4), 2229–2238 (2012).
[CrossRef] [PubMed]

Bonewald, L. F.

H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
[CrossRef] [PubMed]

L. F. Bonewald, “The amazing osteocyte,” J. Bone Miner. Res.26(2), 229–238 (2011).
[CrossRef] [PubMed]

Bunk, O.

M. Dierolf, A. Menzel, P. Thibault, P. Schneider, C. M. Kewish, R. Wepf, O. Bunk, and F. Pfeiffer, “Ptychographic X-ray computed tomography at the nanoscale,” Nature467(7314), 436–439 (2010).
[CrossRef] [PubMed]

Chen, J.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Ciani, C.

C. Ciani, S. B. Doty, and S. P. Fritton, “An effective histological staining process to visualize bone interstitial fluid space using confocal microscopy,” Bone44(5), 1015–1017 (2009).
[CrossRef] [PubMed]

Cloetens, P.

M. Langer, A. Pacureanu, H. Suhonen, Q. Grimal, P. Cloetens, and F. Peyrin, “X-ray phase nanotomography resolves the 3D human bone ultrastructure,” PLoS ONE7(8), e35691 (2012).
[CrossRef] [PubMed]

Cowin, S. C.

L. D. You, S. Weinbaum, S. C. Cowin, and M. B. Schaffler, “Ultrastructure of the osteocyte process and its pericellular matrix,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol.278A(2), 505–513 (2004).
[CrossRef] [PubMed]

Davis, T.

Dierolf, M.

M. Dierolf, A. Menzel, P. Thibault, P. Schneider, C. M. Kewish, R. Wepf, O. Bunk, and F. Pfeiffer, “Ptychographic X-ray computed tomography at the nanoscale,” Nature467(7314), 436–439 (2010).
[CrossRef] [PubMed]

Divieti Pajevic, P.

H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
[CrossRef] [PubMed]

Doty, S. B.

C. Ciani, S. B. Doty, and S. P. Fritton, “An effective histological staining process to visualize bone interstitial fluid space using confocal microscopy,” Bone44(5), 1015–1017 (2009).
[CrossRef] [PubMed]

Dusevich, V.

H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
[CrossRef] [PubMed]

Feser, M.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Fritton, S. P.

C. Ciani, S. B. Doty, and S. P. Fritton, “An effective histological staining process to visualize bone interstitial fluid space using confocal microscopy,” Bone44(5), 1015–1017 (2009).
[CrossRef] [PubMed]

Gao, D.

S. W. Wilkins, T. E. Gureyev, D. Gao, A. Pogany, and A. W. Stevenson, “Phase-contrast imaging using polychromatic hard X-rays,” Nature384(6607), 335–338 (1996).
[CrossRef]

Gelb, J.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Grimal, Q.

M. Langer, A. Pacureanu, H. Suhonen, Q. Grimal, P. Cloetens, and F. Peyrin, “X-ray phase nanotomography resolves the 3D human bone ultrastructure,” PLoS ONE7(8), e35691 (2012).
[CrossRef] [PubMed]

Gureyev, T.

Gureyev, T. E.

S. W. Wilkins, T. E. Gureyev, D. Gao, A. Pogany, and A. W. Stevenson, “Phase-contrast imaging using polychromatic hard X-rays,” Nature384(6607), 335–338 (1996).
[CrossRef]

Hamaishi, Y.

A. Momose, S. Kawamoto, I. Koyama, Y. Hamaishi, K. Takai, and Y. Suzuki, “Demonstration of X-ray Talbot interferometry,” Jpn. J. Appl. Phys.42(Part 2, No. 7B), L866–L868 (2003).
[CrossRef]

Hattori, T.

Y. Takeda, W. Yashiro, T. Hattori, A. Takeuchi, Y. Suzuki, and A. Momose, “Differential phase X-ray imaging microscopy with X-ray Talbot interferometer,” Appl. Phys. Express1, 117002 (2008).
[CrossRef]

A. Momose, W. Yashiro, Y. Takeda, Y. Suzuki, and T. Hattori, “Phase tomography by X-ray Talbot interferometry for biological Imaging,” Jpn. J. Appl. Phys.45(6A), 5254–5262 (2006).
[CrossRef]

Hirano, K.

A. Momose, T. Takeda, Y. Itai, and K. Hirano, “Phase-contrast X-ray computed tomography for observing biological soft tissues,” Nat. Med.2(4), 473–475 (1996).
[CrossRef] [PubMed]

Imai, Y.

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

Irie, N.

K. Matsuo and N. Irie, “Osteoclast-osteoblast communication,” Arch. Biochem. Biophys.473(2), 201–209 (2008).
[CrossRef] [PubMed]

Itai, Y.

A. Momose, T. Takeda, Y. Itai, and K. Hirano, “Phase-contrast X-ray computed tomography for observing biological soft tissues,” Nat. Med.2(4), 473–475 (1996).
[CrossRef] [PubMed]

Jähn, K.

H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
[CrossRef] [PubMed]

Kameo, Y.

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

Kamioka, H.

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

Kato, S.

H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
[CrossRef] [PubMed]

Kawamoto, S.

A. Momose, S. Kawamoto, I. Koyama, Y. Hamaishi, K. Takai, and Y. Suzuki, “Demonstration of X-ray Talbot interferometry,” Jpn. J. Appl. Phys.42(Part 2, No. 7B), L866–L868 (2003).
[CrossRef]

Kewish, C. M.

M. Dierolf, A. Menzel, P. Thibault, P. Schneider, C. M. Kewish, R. Wepf, O. Bunk, and F. Pfeiffer, “Ptychographic X-ray computed tomography at the nanoscale,” Nature467(7314), 436–439 (2010).
[CrossRef] [PubMed]

Klein-Nulend, J.

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

Kohn, V.

A. Snigirev, I. Snigireva, V. Kohn, S. Kuznetsov, and I. Schelokov, “On the possibilities of X-ray phase contrast microimaging by coherent high‐energy synchrotron radiation,” Rev. Sci. Instrum.66(12), 5486–5492 (1995).
[CrossRef]

Koyama, I.

A. Momose, S. Kawamoto, I. Koyama, Y. Hamaishi, K. Takai, and Y. Suzuki, “Demonstration of X-ray Talbot interferometry,” Jpn. J. Appl. Phys.42(Part 2, No. 7B), L866–L868 (2003).
[CrossRef]

Kuznetsov, S.

A. Snigirev, I. Snigireva, V. Kohn, S. Kuznetsov, and I. Schelokov, “On the possibilities of X-ray phase contrast microimaging by coherent high‐energy synchrotron radiation,” Rev. Sci. Instrum.66(12), 5486–5492 (1995).
[CrossRef]

Langer, M.

A. Pacureanu, M. Langer, E. Boller, P. Tafforeau, and F. Peyrin, “Nanoscale imaging of the bone cell network with synchrotron X-ray tomography: optimization of acquisition setup,” Med. Phys.39(4), 2229–2238 (2012).
[CrossRef] [PubMed]

M. Langer, A. Pacureanu, H. Suhonen, Q. Grimal, P. Cloetens, and F. Peyrin, “X-ray phase nanotomography resolves the 3D human bone ultrastructure,” PLoS ONE7(8), e35691 (2012).
[CrossRef] [PubMed]

Lee, C.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Liu, Y.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Matsuo, K.

K. Matsuo and N. Irie, “Osteoclast-osteoblast communication,” Arch. Biochem. Biophys.473(2), 201–209 (2008).
[CrossRef] [PubMed]

Mayo, S.

Meier, M.

P. Schneider, M. Meier, R. Wepf, and R. Müller, “Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network,” Bone47(5), 848–858 (2010).
[CrossRef] [PubMed]

Meirer, F.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Menzel, A.

M. Dierolf, A. Menzel, P. Thibault, P. Schneider, C. M. Kewish, R. Wepf, O. Bunk, and F. Pfeiffer, “Ptychographic X-ray computed tomography at the nanoscale,” Nature467(7314), 436–439 (2010).
[CrossRef] [PubMed]

Miller, P.

Momose, A.

Y. Takeda, W. Yashiro, T. Hattori, A. Takeuchi, Y. Suzuki, and A. Momose, “Differential phase X-ray imaging microscopy with X-ray Talbot interferometer,” Appl. Phys. Express1, 117002 (2008).
[CrossRef]

A. Momose, W. Yashiro, Y. Takeda, Y. Suzuki, and T. Hattori, “Phase tomography by X-ray Talbot interferometry for biological Imaging,” Jpn. J. Appl. Phys.45(6A), 5254–5262 (2006).
[CrossRef]

A. Momose, S. Kawamoto, I. Koyama, Y. Hamaishi, K. Takai, and Y. Suzuki, “Demonstration of X-ray Talbot interferometry,” Jpn. J. Appl. Phys.42(Part 2, No. 7B), L866–L868 (2003).
[CrossRef]

A. Momose, T. Takeda, Y. Itai, and K. Hirano, “Phase-contrast X-ray computed tomography for observing biological soft tissues,” Nat. Med.2(4), 473–475 (1996).
[CrossRef] [PubMed]

Müller, R.

P. Schneider, M. Meier, R. Wepf, and R. Müller, “Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network,” Bone47(5), 848–858 (2010).
[CrossRef] [PubMed]

Pacureanu, A.

M. Langer, A. Pacureanu, H. Suhonen, Q. Grimal, P. Cloetens, and F. Peyrin, “X-ray phase nanotomography resolves the 3D human bone ultrastructure,” PLoS ONE7(8), e35691 (2012).
[CrossRef] [PubMed]

A. Pacureanu, M. Langer, E. Boller, P. Tafforeau, and F. Peyrin, “Nanoscale imaging of the bone cell network with synchrotron X-ray tomography: optimization of acquisition setup,” Med. Phys.39(4), 2229–2238 (2012).
[CrossRef] [PubMed]

Paganin, D.

Peyrin, F.

A. Pacureanu, M. Langer, E. Boller, P. Tafforeau, and F. Peyrin, “Nanoscale imaging of the bone cell network with synchrotron X-ray tomography: optimization of acquisition setup,” Med. Phys.39(4), 2229–2238 (2012).
[CrossRef] [PubMed]

M. Langer, A. Pacureanu, H. Suhonen, Q. Grimal, P. Cloetens, and F. Peyrin, “X-ray phase nanotomography resolves the 3D human bone ultrastructure,” PLoS ONE7(8), e35691 (2012).
[CrossRef] [PubMed]

Pfeiffer, F.

M. Dierolf, A. Menzel, P. Thibault, P. Schneider, C. M. Kewish, R. Wepf, O. Bunk, and F. Pfeiffer, “Ptychographic X-ray computed tomography at the nanoscale,” Nature467(7314), 436–439 (2010).
[CrossRef] [PubMed]

Pianetta, P.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Pogany, A.

S. Mayo, T. Davis, T. Gureyev, P. Miller, D. Paganin, A. Pogany, A. Stevenson, and S. Wilkins, “X-ray phase-contrast microscopy and microtomography,” Opt. Express11(19), 2289–2302 (2003).
[CrossRef] [PubMed]

S. W. Wilkins, T. E. Gureyev, D. Gao, A. Pogany, and A. W. Stevenson, “Phase-contrast imaging using polychromatic hard X-rays,” Nature384(6607), 335–338 (1996).
[CrossRef]

Qing, H.

H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
[CrossRef] [PubMed]

Rudati, J.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Schaffler, M. B.

L. D. You, S. Weinbaum, S. C. Cowin, and M. B. Schaffler, “Ultrastructure of the osteocyte process and its pericellular matrix,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol.278A(2), 505–513 (2004).
[CrossRef] [PubMed]

Schelokov, I.

A. Snigirev, I. Snigireva, V. Kohn, S. Kuznetsov, and I. Schelokov, “On the possibilities of X-ray phase contrast microimaging by coherent high‐energy synchrotron radiation,” Rev. Sci. Instrum.66(12), 5486–5492 (1995).
[CrossRef]

Schneider, P.

M. Dierolf, A. Menzel, P. Thibault, P. Schneider, C. M. Kewish, R. Wepf, O. Bunk, and F. Pfeiffer, “Ptychographic X-ray computed tomography at the nanoscale,” Nature467(7314), 436–439 (2010).
[CrossRef] [PubMed]

P. Schneider, M. Meier, R. Wepf, and R. Müller, “Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network,” Bone47(5), 848–858 (2010).
[CrossRef] [PubMed]

Snigirev, A.

A. Snigirev, I. Snigireva, V. Kohn, S. Kuznetsov, and I. Schelokov, “On the possibilities of X-ray phase contrast microimaging by coherent high‐energy synchrotron radiation,” Rev. Sci. Instrum.66(12), 5486–5492 (1995).
[CrossRef]

Snigireva, I.

A. Snigirev, I. Snigireva, V. Kohn, S. Kuznetsov, and I. Schelokov, “On the possibilities of X-ray phase contrast microimaging by coherent high‐energy synchrotron radiation,” Rev. Sci. Instrum.66(12), 5486–5492 (1995).
[CrossRef]

Stevenson, A.

Stevenson, A. W.

S. W. Wilkins, T. E. Gureyev, D. Gao, A. Pogany, and A. W. Stevenson, “Phase-contrast imaging using polychromatic hard X-rays,” Nature384(6607), 335–338 (1996).
[CrossRef]

Suhonen, H.

M. Langer, A. Pacureanu, H. Suhonen, Q. Grimal, P. Cloetens, and F. Peyrin, “X-ray phase nanotomography resolves the 3D human bone ultrastructure,” PLoS ONE7(8), e35691 (2012).
[CrossRef] [PubMed]

Suzuki, Y.

Y. Takeda, W. Yashiro, T. Hattori, A. Takeuchi, Y. Suzuki, and A. Momose, “Differential phase X-ray imaging microscopy with X-ray Talbot interferometer,” Appl. Phys. Express1, 117002 (2008).
[CrossRef]

A. Momose, W. Yashiro, Y. Takeda, Y. Suzuki, and T. Hattori, “Phase tomography by X-ray Talbot interferometry for biological Imaging,” Jpn. J. Appl. Phys.45(6A), 5254–5262 (2006).
[CrossRef]

A. Momose, S. Kawamoto, I. Koyama, Y. Hamaishi, K. Takai, and Y. Suzuki, “Demonstration of X-ray Talbot interferometry,” Jpn. J. Appl. Phys.42(Part 2, No. 7B), L866–L868 (2003).
[CrossRef]

Tafforeau, P.

A. Pacureanu, M. Langer, E. Boller, P. Tafforeau, and F. Peyrin, “Nanoscale imaging of the bone cell network with synchrotron X-ray tomography: optimization of acquisition setup,” Med. Phys.39(4), 2229–2238 (2012).
[CrossRef] [PubMed]

Takai, K.

A. Momose, S. Kawamoto, I. Koyama, Y. Hamaishi, K. Takai, and Y. Suzuki, “Demonstration of X-ray Talbot interferometry,” Jpn. J. Appl. Phys.42(Part 2, No. 7B), L866–L868 (2003).
[CrossRef]

Takaoka, A.

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

Takeda, T.

A. Momose, T. Takeda, Y. Itai, and K. Hirano, “Phase-contrast X-ray computed tomography for observing biological soft tissues,” Nat. Med.2(4), 473–475 (1996).
[CrossRef] [PubMed]

Takeda, Y.

Y. Takeda, W. Yashiro, T. Hattori, A. Takeuchi, Y. Suzuki, and A. Momose, “Differential phase X-ray imaging microscopy with X-ray Talbot interferometer,” Appl. Phys. Express1, 117002 (2008).
[CrossRef]

A. Momose, W. Yashiro, Y. Takeda, Y. Suzuki, and T. Hattori, “Phase tomography by X-ray Talbot interferometry for biological Imaging,” Jpn. J. Appl. Phys.45(6A), 5254–5262 (2006).
[CrossRef]

Takeuchi, A.

Y. Takeda, W. Yashiro, T. Hattori, A. Takeuchi, Y. Suzuki, and A. Momose, “Differential phase X-ray imaging microscopy with X-ray Talbot interferometer,” Appl. Phys. Express1, 117002 (2008).
[CrossRef]

Teti, A.

A. Teti and A. Zallone, “Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited,” Bone44(1), 11–16 (2009).
[CrossRef] [PubMed]

Thibault, P.

M. Dierolf, A. Menzel, P. Thibault, P. Schneider, C. M. Kewish, R. Wepf, O. Bunk, and F. Pfeiffer, “Ptychographic X-ray computed tomography at the nanoscale,” Nature467(7314), 436–439 (2010).
[CrossRef] [PubMed]

Tkachuk, A.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

van der Meulen, M. C. H.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Weinbaum, S.

L. D. You, S. Weinbaum, S. C. Cowin, and M. B. Schaffler, “Ultrastructure of the osteocyte process and its pericellular matrix,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol.278A(2), 505–513 (2004).
[CrossRef] [PubMed]

Wepf, R.

P. Schneider, M. Meier, R. Wepf, and R. Müller, “Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network,” Bone47(5), 848–858 (2010).
[CrossRef] [PubMed]

M. Dierolf, A. Menzel, P. Thibault, P. Schneider, C. M. Kewish, R. Wepf, O. Bunk, and F. Pfeiffer, “Ptychographic X-ray computed tomography at the nanoscale,” Nature467(7314), 436–439 (2010).
[CrossRef] [PubMed]

Wilkins, S.

Wilkins, S. W.

S. W. Wilkins, T. E. Gureyev, D. Gao, A. Pogany, and A. W. Stevenson, “Phase-contrast imaging using polychromatic hard X-rays,” Nature384(6607), 335–338 (1996).
[CrossRef]

Wysolmerski, J.

H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
[CrossRef] [PubMed]

Wysolmerski, J. J.

J. J. Wysolmerski, “Osteocytes remove and replace perilacunar mineral during reproductive cycles,” Bone54(2), 230–236 (2013).
[CrossRef] [PubMed]

Yamada, N.

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

Yamashiro, T.

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

Yashiro, W.

Y. Takeda, W. Yashiro, T. Hattori, A. Takeuchi, Y. Suzuki, and A. Momose, “Differential phase X-ray imaging microscopy with X-ray Talbot interferometer,” Appl. Phys. Express1, 117002 (2008).
[CrossRef]

A. Momose, W. Yashiro, Y. Takeda, Y. Suzuki, and T. Hattori, “Phase tomography by X-ray Talbot interferometry for biological Imaging,” Jpn. J. Appl. Phys.45(6A), 5254–5262 (2006).
[CrossRef]

You, L. D.

L. D. You, S. Weinbaum, S. C. Cowin, and M. B. Schaffler, “Ultrastructure of the osteocyte process and its pericellular matrix,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol.278A(2), 505–513 (2004).
[CrossRef] [PubMed]

Yun, W.

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Zallone, A.

A. Teti and A. Zallone, “Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited,” Bone44(1), 11–16 (2009).
[CrossRef] [PubMed]

Anat. Rec. A Discov. Mol. Cell. Evol. Biol. (1)

L. D. You, S. Weinbaum, S. C. Cowin, and M. B. Schaffler, “Ultrastructure of the osteocyte process and its pericellular matrix,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol.278A(2), 505–513 (2004).
[CrossRef] [PubMed]

Appl. Phys. Express (1)

Y. Takeda, W. Yashiro, T. Hattori, A. Takeuchi, Y. Suzuki, and A. Momose, “Differential phase X-ray imaging microscopy with X-ray Talbot interferometer,” Appl. Phys. Express1, 117002 (2008).
[CrossRef]

Arch. Biochem. Biophys. (1)

K. Matsuo and N. Irie, “Osteoclast-osteoblast communication,” Arch. Biochem. Biophys.473(2), 201–209 (2008).
[CrossRef] [PubMed]

Bone (4)

A. Teti and A. Zallone, “Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited,” Bone44(1), 11–16 (2009).
[CrossRef] [PubMed]

J. J. Wysolmerski, “Osteocytes remove and replace perilacunar mineral during reproductive cycles,” Bone54(2), 230–236 (2013).
[CrossRef] [PubMed]

C. Ciani, S. B. Doty, and S. P. Fritton, “An effective histological staining process to visualize bone interstitial fluid space using confocal microscopy,” Bone44(5), 1015–1017 (2009).
[CrossRef] [PubMed]

P. Schneider, M. Meier, R. Wepf, and R. Müller, “Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network,” Bone47(5), 848–858 (2010).
[CrossRef] [PubMed]

Calcif. Tissue Res. (1)

L. F. Bélanger, “Osteocytic osteolysis,” Calcif. Tissue Res.4(1), 1–12 (1969).
[CrossRef] [PubMed]

Integr. Biol. (1)

H. Kamioka, Y. Kameo, Y. Imai, A. D. Bakker, R. G. Bacabac, N. Yamada, A. Takaoka, T. Yamashiro, T. Adachi, and J. Klein-Nulend, “Microscale fluid flow analysis in a human osteocyte canaliculus using a realistic high-resolution image-based three-dimensional model,” Integr. Biol.4(10), 1198–1206 (2012).
[CrossRef] [PubMed]

J. Bone Miner. Res. (2)

H. Qing, L. Ardeshirpour, P. Divieti Pajevic, V. Dusevich, K. Jähn, S. Kato, J. Wysolmerski, and L. F. Bonewald, “Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation,” J. Bone Miner. Res.27(5), 1018–1029 (2012).
[CrossRef] [PubMed]

L. F. Bonewald, “The amazing osteocyte,” J. Bone Miner. Res.26(2), 229–238 (2011).
[CrossRef] [PubMed]

Jpn. J. Appl. Phys. (2)

A. Momose, W. Yashiro, Y. Takeda, Y. Suzuki, and T. Hattori, “Phase tomography by X-ray Talbot interferometry for biological Imaging,” Jpn. J. Appl. Phys.45(6A), 5254–5262 (2006).
[CrossRef]

A. Momose, S. Kawamoto, I. Koyama, Y. Hamaishi, K. Takai, and Y. Suzuki, “Demonstration of X-ray Talbot interferometry,” Jpn. J. Appl. Phys.42(Part 2, No. 7B), L866–L868 (2003).
[CrossRef]

Med. Phys. (1)

A. Pacureanu, M. Langer, E. Boller, P. Tafforeau, and F. Peyrin, “Nanoscale imaging of the bone cell network with synchrotron X-ray tomography: optimization of acquisition setup,” Med. Phys.39(4), 2229–2238 (2012).
[CrossRef] [PubMed]

Microsc. Microanal. (1)

J. C. Andrews, E. Almeida, M. C. H. van der Meulen, J. S. Alwood, C. Lee, Y. Liu, J. Chen, F. Meirer, M. Feser, J. Gelb, J. Rudati, A. Tkachuk, W. Yun, and P. Pianetta, “Nanoscale X-ray microscopic imaging of mammalian mineralized tissue,” Microsc. Microanal.16(03), 327–336 (2010).
[CrossRef] [PubMed]

Nat. Med. (1)

A. Momose, T. Takeda, Y. Itai, and K. Hirano, “Phase-contrast X-ray computed tomography for observing biological soft tissues,” Nat. Med.2(4), 473–475 (1996).
[CrossRef] [PubMed]

Nature (2)

M. Dierolf, A. Menzel, P. Thibault, P. Schneider, C. M. Kewish, R. Wepf, O. Bunk, and F. Pfeiffer, “Ptychographic X-ray computed tomography at the nanoscale,” Nature467(7314), 436–439 (2010).
[CrossRef] [PubMed]

S. W. Wilkins, T. E. Gureyev, D. Gao, A. Pogany, and A. W. Stevenson, “Phase-contrast imaging using polychromatic hard X-rays,” Nature384(6607), 335–338 (1996).
[CrossRef]

Opt. Express (1)

PLoS ONE (1)

M. Langer, A. Pacureanu, H. Suhonen, Q. Grimal, P. Cloetens, and F. Peyrin, “X-ray phase nanotomography resolves the 3D human bone ultrastructure,” PLoS ONE7(8), e35691 (2012).
[CrossRef] [PubMed]

Rev. Sci. Instrum. (1)

A. Snigirev, I. Snigireva, V. Kohn, S. Kuznetsov, and I. Schelokov, “On the possibilities of X-ray phase contrast microimaging by coherent high‐energy synchrotron radiation,” Rev. Sci. Instrum.66(12), 5486–5492 (1995).
[CrossRef]

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Figures (3)

Fig. 1
Fig. 1

Setup of multiscan X-ray microscope. (a) Differential phase-contrast mode in combination with a Talbot interferometer consisting of a phase grating and an amplitude grating. (b) Defocus absorption-contrast mode achieved by moving the Fresnel zone plate (thick arrow). (c) Block diagram of control system. FS, fringe scanning; GR, grating remove; DA, defocus arrangement; CR, CT scan rotation.

Fig. 2
Fig. 2

Preparation of mouse bone sample. (a) Schematic presentation of tibia. The cortical bone sample used for imaging is represented in green. (b) The sample (green arrow) attached to the holder using double-sided adhesive tape (arrowhead). Scale bar, 1 mm.

Fig. 3
Fig. 3

Reconstructed tomograms. (a) Phase tomogram, in which gray scale indicates the refractive index decrement δ ranging 0 (corresponding to low (L) mineral density) to 7 x 10−6 (corresponding to high (H) mineral density). Arrows, osteocyte canaliculi; Arrowheads, osteocyte lacunae; Double arrowhead, cement line. (b) Tomogram with defocus edge enhancement. The outer edges of the lacunae and canaliculi are enhanced. Note that black and white are reversed. (c) Combined image of (a) and (b). The defocus image is pseudocolored red. Scale bars, 25 μm. The dotted rectangle in (a-c) is magnified in the left image.

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