Abstract

The gold standard method for visualizing the pathologies underlying human sensorineural hearing loss has remained post-mortem histology for over 125 years, despite awareness that histological preparation induces severe artifacts in biological tissue. Historically, the transition from post-mortem assessment to non-invasive clinical biomedical imaging in living humans has revolutionized diagnosis and treatment of disease; however, innovation in non-invasive techniques for cellular-level intracochlear imaging in humans has been difficult due to the cochlea’s small size, complex 3D configuration, fragility, and deep encasement within bone. Here we investigate the ability of synchrotron radiation-facilitated X-ray absorption and phase contrast imaging to enable visualization of sensory cells and nerve fibers in the cochlea’s sensory epithelium in situ in 3D intact, non-decalcified, unstained human temporal bones. Our findings show that this imaging technique resolves the bone-encased sensory epithelium’s cytoarchitecture with unprecedented levels of cellular detail for an intact, unstained specimen, and is capable of distinguishing between healthy and damaged epithelium. All analyses were performed using commercially available software that quickly reconstructs and facilitates 3D manipulation of massive data sets. Results suggest that synchrotron radiation phase contrast imaging has the future potential to replace histology as a gold standard for evaluating intracochlear structural integrity in human specimens, and motivate further optimization for translation to the clinic.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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  25. D. D. Greenwood, “Audtory masking and the critical band,” J. Acoust. Soc. Am. 33(4), 484–502 (1961).
    [Crossref]
  26. D. D. Greenwood, “Critical bandwidth and the frequency coordinates of the basilar membrane,” J. Acoust. Soc. Am. 33(10), 1344–1356 (1961).
    [Crossref]
  27. R. A. Chole and M. J. McKenna, “A silent and imminent threat,” The Registry 20(2), 1–2 (2012).

2018 (2)

S. Agrawal, N. Schart-Morén, W. Liu, H. M. Ladak, H. Rask-Andersen, and H. Li, “The secondary spiral lamina and its relevance in cochlear implant surgery,” Ups. J. Med. Sci. 123(1), 9–18 (2018).
[Crossref] [PubMed]

C. P. Richter, H. Young, S. V. Richter, V. Smith-Bronstein, S. R. Stock, X. Xiao, C. Soriano, and D. S. Whitlon, “Fluvastatin protects cochleae from damage by high-level noise,” Sci. Rep. 8(1), 3033 (2018).
[Crossref] [PubMed]

2017 (2)

M. Elfarnawany, S. R. Alam, S. A. Rohani, N. Zhu, S. K. Agrawal, and H. M. Ladak, “Micro-CT versus synchrotron radiation phase contrast imaging of human cochlea,” J. Microsc. 265(3), 349–357 (2017).
[Crossref] [PubMed]

R. W. Koch, M. Elfarnawany, N. Zhu, H. M. Ladak, and S. K. Agrawal, “Evaluation of cochlear duct length computations using synchrotron radiation phase-contrast imaging,” Otol. Neurotol. 38(6), e92–e99 (2017).
[Crossref] [PubMed]

2015 (1)

T. W. Wysokinski, D. Chapman, G. Adams, M. Renier, R. Suortti, and W. Thomlinson, “Beamlines of the biomedical imaging and therapy facility at the Canadian light source – part 3,” Nucl. Instrum. Methods Phys. Res. A 775, 1–4 (2015).
[Crossref]

2014 (3)

M. S. Pearl, A. Roy, and C. J. Limb, “High-resolution secondary reconstructions with the use of flat panel CT in the clinical assessment of patients with cochlear implants,” AJNR Am. J. Neuroradiol. 35(6), 1202–1208 (2014).
[Crossref] [PubMed]

S. L. van Egmond, F. Visser, F. A. Pameijer, and W. Grolman, “Ex vivo and in vivo imaging of the inner ear at 7 Tesla MRI,” Otol. Neurotol. 35(4), 725–729 (2014).
[Crossref] [PubMed]

S. Chatterjee, “Artefacts in histopathology,” J. Oral Maxillofac. Pathol. 18(4), S111–S116 (2014).
[Crossref] [PubMed]

2013 (1)

T. S. Rau, W. Würfel, T. Lenarz, and O. Majdani, “Three-dimensional histological specimen preparation for accurate imaging and spatial reconstruction of the middle and inner ear,” Int. J. CARS 8(4), 481–509 (2013).
[Crossref] [PubMed]

2012 (4)

C. Rau, M. Hwang, W. K. Lee, and C. P. Richter, “Quantitative X-ray tomography of the mouse cochlea,” PLoS One 7(4), e33568 (2012).
[Crossref] [PubMed]

R. A. Chole and M. J. McKenna, “A silent and imminent threat,” The Registry 20(2), 1–2 (2012).

C. Liu, X. Bu, F. Wu, and G. Xing, “Unilateral auditory neuropathy caused by cochlear nerve deficiency,” Int. J. Otolaryngol. 2012, 1 (2012).
[Crossref] [PubMed]

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

2011 (1)

R. S. Z. Yiin, P. H. Tang, and T. Y. Tan, “Review of congenital inner ear abnormalities on CT temporal bone,” Br. J. Radiol. 84(1005), 859–863 (2011).
[Crossref] [PubMed]

2009 (1)

A. Lareida, F. Beckmann, A. Schrott-Fischer, R. Glueckert, W. Freysinger, and B. Müller, “High-resolution X-ray tomography of the human inner ear: synchrotron radiation-based study of nerve fibre bundles, membranes and ganglion cells,” J. Microsc. 234(1), 95–102 (2009).
[Crossref] [PubMed]

2006 (1)

S. F. Li, T. Y. Zhang, and Z. M. Wang, “An approach for precise three-dimensional modeling of the human inner ear,” ORL J. Otorhinolaryngol. Relat. Spec. 68(5), 302–310 (2006).
[Crossref] [PubMed]

2002 (1)

M. A. Brown, R. B. Reed, and R. W. Henry, “Effects of dehydration mediums and temperature on total dehydration time and tissue shrinkage,” J. Int. Soc. Plastination. 33, 28–33 (2002).

1999 (1)

U. Vogel, “New approach for 3D imaging and geometry modeling of the human inner ear,” ORL J. Otorhinolaryngol. Relat. Spec. 61(5), 259–267 (1999).
[Crossref] [PubMed]

1997 (1)

A. S. Brunschwig and A. N. Salt, “Fixation-induced shrinkage of Reissner’s membrane and its potential influence on the assessment of endolymph volume,” Hear. Res. 114(1-2), 62–68 (1997).
[Crossref] [PubMed]

1961 (2)

D. D. Greenwood, “Audtory masking and the critical band,” J. Acoust. Soc. Am. 33(4), 484–502 (1961).
[Crossref]

D. D. Greenwood, “Critical bandwidth and the frequency coordinates of the basilar membrane,” J. Acoust. Soc. Am. 33(10), 1344–1356 (1961).
[Crossref]

Adams, G.

T. W. Wysokinski, D. Chapman, G. Adams, M. Renier, R. Suortti, and W. Thomlinson, “Beamlines of the biomedical imaging and therapy facility at the Canadian light source – part 3,” Nucl. Instrum. Methods Phys. Res. A 775, 1–4 (2015).
[Crossref]

Agrawal, S.

S. Agrawal, N. Schart-Morén, W. Liu, H. M. Ladak, H. Rask-Andersen, and H. Li, “The secondary spiral lamina and its relevance in cochlear implant surgery,” Ups. J. Med. Sci. 123(1), 9–18 (2018).
[Crossref] [PubMed]

Agrawal, S. K.

R. W. Koch, M. Elfarnawany, N. Zhu, H. M. Ladak, and S. K. Agrawal, “Evaluation of cochlear duct length computations using synchrotron radiation phase-contrast imaging,” Otol. Neurotol. 38(6), e92–e99 (2017).
[Crossref] [PubMed]

M. Elfarnawany, S. R. Alam, S. A. Rohani, N. Zhu, S. K. Agrawal, and H. M. Ladak, “Micro-CT versus synchrotron radiation phase contrast imaging of human cochlea,” J. Microsc. 265(3), 349–357 (2017).
[Crossref] [PubMed]

Alam, S. R.

M. Elfarnawany, S. R. Alam, S. A. Rohani, N. Zhu, S. K. Agrawal, and H. M. Ladak, “Micro-CT versus synchrotron radiation phase contrast imaging of human cochlea,” J. Microsc. 265(3), 349–357 (2017).
[Crossref] [PubMed]

Arganda-Carreras, I.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Beckmann, F.

A. Lareida, F. Beckmann, A. Schrott-Fischer, R. Glueckert, W. Freysinger, and B. Müller, “High-resolution X-ray tomography of the human inner ear: synchrotron radiation-based study of nerve fibre bundles, membranes and ganglion cells,” J. Microsc. 234(1), 95–102 (2009).
[Crossref] [PubMed]

Brown, M. A.

M. A. Brown, R. B. Reed, and R. W. Henry, “Effects of dehydration mediums and temperature on total dehydration time and tissue shrinkage,” J. Int. Soc. Plastination. 33, 28–33 (2002).

Brunschwig, A. S.

A. S. Brunschwig and A. N. Salt, “Fixation-induced shrinkage of Reissner’s membrane and its potential influence on the assessment of endolymph volume,” Hear. Res. 114(1-2), 62–68 (1997).
[Crossref] [PubMed]

Bu, X.

C. Liu, X. Bu, F. Wu, and G. Xing, “Unilateral auditory neuropathy caused by cochlear nerve deficiency,” Int. J. Otolaryngol. 2012, 1 (2012).
[Crossref] [PubMed]

Cardona, A.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Chapman, D.

T. W. Wysokinski, D. Chapman, G. Adams, M. Renier, R. Suortti, and W. Thomlinson, “Beamlines of the biomedical imaging and therapy facility at the Canadian light source – part 3,” Nucl. Instrum. Methods Phys. Res. A 775, 1–4 (2015).
[Crossref]

Chatterjee, S.

S. Chatterjee, “Artefacts in histopathology,” J. Oral Maxillofac. Pathol. 18(4), S111–S116 (2014).
[Crossref] [PubMed]

Chole, R. A.

R. A. Chole and M. J. McKenna, “A silent and imminent threat,” The Registry 20(2), 1–2 (2012).

Elfarnawany, M.

M. Elfarnawany, S. R. Alam, S. A. Rohani, N. Zhu, S. K. Agrawal, and H. M. Ladak, “Micro-CT versus synchrotron radiation phase contrast imaging of human cochlea,” J. Microsc. 265(3), 349–357 (2017).
[Crossref] [PubMed]

R. W. Koch, M. Elfarnawany, N. Zhu, H. M. Ladak, and S. K. Agrawal, “Evaluation of cochlear duct length computations using synchrotron radiation phase-contrast imaging,” Otol. Neurotol. 38(6), e92–e99 (2017).
[Crossref] [PubMed]

Eliceiri, K.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Freysinger, W.

A. Lareida, F. Beckmann, A. Schrott-Fischer, R. Glueckert, W. Freysinger, and B. Müller, “High-resolution X-ray tomography of the human inner ear: synchrotron radiation-based study of nerve fibre bundles, membranes and ganglion cells,” J. Microsc. 234(1), 95–102 (2009).
[Crossref] [PubMed]

Frise, E.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Glueckert, R.

A. Lareida, F. Beckmann, A. Schrott-Fischer, R. Glueckert, W. Freysinger, and B. Müller, “High-resolution X-ray tomography of the human inner ear: synchrotron radiation-based study of nerve fibre bundles, membranes and ganglion cells,” J. Microsc. 234(1), 95–102 (2009).
[Crossref] [PubMed]

Greenwood, D. D.

D. D. Greenwood, “Audtory masking and the critical band,” J. Acoust. Soc. Am. 33(4), 484–502 (1961).
[Crossref]

D. D. Greenwood, “Critical bandwidth and the frequency coordinates of the basilar membrane,” J. Acoust. Soc. Am. 33(10), 1344–1356 (1961).
[Crossref]

Grolman, W.

S. L. van Egmond, F. Visser, F. A. Pameijer, and W. Grolman, “Ex vivo and in vivo imaging of the inner ear at 7 Tesla MRI,” Otol. Neurotol. 35(4), 725–729 (2014).
[Crossref] [PubMed]

Hartenstein, V.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Henry, R. W.

M. A. Brown, R. B. Reed, and R. W. Henry, “Effects of dehydration mediums and temperature on total dehydration time and tissue shrinkage,” J. Int. Soc. Plastination. 33, 28–33 (2002).

Hwang, M.

C. Rau, M. Hwang, W. K. Lee, and C. P. Richter, “Quantitative X-ray tomography of the mouse cochlea,” PLoS One 7(4), e33568 (2012).
[Crossref] [PubMed]

Kaynig, V.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Koch, R. W.

R. W. Koch, M. Elfarnawany, N. Zhu, H. M. Ladak, and S. K. Agrawal, “Evaluation of cochlear duct length computations using synchrotron radiation phase-contrast imaging,” Otol. Neurotol. 38(6), e92–e99 (2017).
[Crossref] [PubMed]

Ladak, H. M.

S. Agrawal, N. Schart-Morén, W. Liu, H. M. Ladak, H. Rask-Andersen, and H. Li, “The secondary spiral lamina and its relevance in cochlear implant surgery,” Ups. J. Med. Sci. 123(1), 9–18 (2018).
[Crossref] [PubMed]

R. W. Koch, M. Elfarnawany, N. Zhu, H. M. Ladak, and S. K. Agrawal, “Evaluation of cochlear duct length computations using synchrotron radiation phase-contrast imaging,” Otol. Neurotol. 38(6), e92–e99 (2017).
[Crossref] [PubMed]

M. Elfarnawany, S. R. Alam, S. A. Rohani, N. Zhu, S. K. Agrawal, and H. M. Ladak, “Micro-CT versus synchrotron radiation phase contrast imaging of human cochlea,” J. Microsc. 265(3), 349–357 (2017).
[Crossref] [PubMed]

Lareida, A.

A. Lareida, F. Beckmann, A. Schrott-Fischer, R. Glueckert, W. Freysinger, and B. Müller, “High-resolution X-ray tomography of the human inner ear: synchrotron radiation-based study of nerve fibre bundles, membranes and ganglion cells,” J. Microsc. 234(1), 95–102 (2009).
[Crossref] [PubMed]

Lee, W. K.

C. Rau, M. Hwang, W. K. Lee, and C. P. Richter, “Quantitative X-ray tomography of the mouse cochlea,” PLoS One 7(4), e33568 (2012).
[Crossref] [PubMed]

Lenarz, T.

T. S. Rau, W. Würfel, T. Lenarz, and O. Majdani, “Three-dimensional histological specimen preparation for accurate imaging and spatial reconstruction of the middle and inner ear,” Int. J. CARS 8(4), 481–509 (2013).
[Crossref] [PubMed]

Li, H.

S. Agrawal, N. Schart-Morén, W. Liu, H. M. Ladak, H. Rask-Andersen, and H. Li, “The secondary spiral lamina and its relevance in cochlear implant surgery,” Ups. J. Med. Sci. 123(1), 9–18 (2018).
[Crossref] [PubMed]

Li, S. F.

S. F. Li, T. Y. Zhang, and Z. M. Wang, “An approach for precise three-dimensional modeling of the human inner ear,” ORL J. Otorhinolaryngol. Relat. Spec. 68(5), 302–310 (2006).
[Crossref] [PubMed]

Limb, C. J.

M. S. Pearl, A. Roy, and C. J. Limb, “High-resolution secondary reconstructions with the use of flat panel CT in the clinical assessment of patients with cochlear implants,” AJNR Am. J. Neuroradiol. 35(6), 1202–1208 (2014).
[Crossref] [PubMed]

Liu, C.

C. Liu, X. Bu, F. Wu, and G. Xing, “Unilateral auditory neuropathy caused by cochlear nerve deficiency,” Int. J. Otolaryngol. 2012, 1 (2012).
[Crossref] [PubMed]

Liu, W.

S. Agrawal, N. Schart-Morén, W. Liu, H. M. Ladak, H. Rask-Andersen, and H. Li, “The secondary spiral lamina and its relevance in cochlear implant surgery,” Ups. J. Med. Sci. 123(1), 9–18 (2018).
[Crossref] [PubMed]

Longair, M.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Majdani, O.

T. S. Rau, W. Würfel, T. Lenarz, and O. Majdani, “Three-dimensional histological specimen preparation for accurate imaging and spatial reconstruction of the middle and inner ear,” Int. J. CARS 8(4), 481–509 (2013).
[Crossref] [PubMed]

McKenna, M. J.

R. A. Chole and M. J. McKenna, “A silent and imminent threat,” The Registry 20(2), 1–2 (2012).

Müller, B.

A. Lareida, F. Beckmann, A. Schrott-Fischer, R. Glueckert, W. Freysinger, and B. Müller, “High-resolution X-ray tomography of the human inner ear: synchrotron radiation-based study of nerve fibre bundles, membranes and ganglion cells,” J. Microsc. 234(1), 95–102 (2009).
[Crossref] [PubMed]

Pameijer, F. A.

S. L. van Egmond, F. Visser, F. A. Pameijer, and W. Grolman, “Ex vivo and in vivo imaging of the inner ear at 7 Tesla MRI,” Otol. Neurotol. 35(4), 725–729 (2014).
[Crossref] [PubMed]

Pearl, M. S.

M. S. Pearl, A. Roy, and C. J. Limb, “High-resolution secondary reconstructions with the use of flat panel CT in the clinical assessment of patients with cochlear implants,” AJNR Am. J. Neuroradiol. 35(6), 1202–1208 (2014).
[Crossref] [PubMed]

Pietzsch, T.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Preibisch, S.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Rask-Andersen, H.

S. Agrawal, N. Schart-Morén, W. Liu, H. M. Ladak, H. Rask-Andersen, and H. Li, “The secondary spiral lamina and its relevance in cochlear implant surgery,” Ups. J. Med. Sci. 123(1), 9–18 (2018).
[Crossref] [PubMed]

Rau, C.

C. Rau, M. Hwang, W. K. Lee, and C. P. Richter, “Quantitative X-ray tomography of the mouse cochlea,” PLoS One 7(4), e33568 (2012).
[Crossref] [PubMed]

Rau, T. S.

T. S. Rau, W. Würfel, T. Lenarz, and O. Majdani, “Three-dimensional histological specimen preparation for accurate imaging and spatial reconstruction of the middle and inner ear,” Int. J. CARS 8(4), 481–509 (2013).
[Crossref] [PubMed]

Reed, R. B.

M. A. Brown, R. B. Reed, and R. W. Henry, “Effects of dehydration mediums and temperature on total dehydration time and tissue shrinkage,” J. Int. Soc. Plastination. 33, 28–33 (2002).

Renier, M.

T. W. Wysokinski, D. Chapman, G. Adams, M. Renier, R. Suortti, and W. Thomlinson, “Beamlines of the biomedical imaging and therapy facility at the Canadian light source – part 3,” Nucl. Instrum. Methods Phys. Res. A 775, 1–4 (2015).
[Crossref]

Richter, C. P.

C. P. Richter, H. Young, S. V. Richter, V. Smith-Bronstein, S. R. Stock, X. Xiao, C. Soriano, and D. S. Whitlon, “Fluvastatin protects cochleae from damage by high-level noise,” Sci. Rep. 8(1), 3033 (2018).
[Crossref] [PubMed]

C. Rau, M. Hwang, W. K. Lee, and C. P. Richter, “Quantitative X-ray tomography of the mouse cochlea,” PLoS One 7(4), e33568 (2012).
[Crossref] [PubMed]

Richter, S. V.

C. P. Richter, H. Young, S. V. Richter, V. Smith-Bronstein, S. R. Stock, X. Xiao, C. Soriano, and D. S. Whitlon, “Fluvastatin protects cochleae from damage by high-level noise,” Sci. Rep. 8(1), 3033 (2018).
[Crossref] [PubMed]

Rohani, S. A.

M. Elfarnawany, S. R. Alam, S. A. Rohani, N. Zhu, S. K. Agrawal, and H. M. Ladak, “Micro-CT versus synchrotron radiation phase contrast imaging of human cochlea,” J. Microsc. 265(3), 349–357 (2017).
[Crossref] [PubMed]

Roy, A.

M. S. Pearl, A. Roy, and C. J. Limb, “High-resolution secondary reconstructions with the use of flat panel CT in the clinical assessment of patients with cochlear implants,” AJNR Am. J. Neuroradiol. 35(6), 1202–1208 (2014).
[Crossref] [PubMed]

Rueden, C.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Saalfeld, S.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Salt, A. N.

A. S. Brunschwig and A. N. Salt, “Fixation-induced shrinkage of Reissner’s membrane and its potential influence on the assessment of endolymph volume,” Hear. Res. 114(1-2), 62–68 (1997).
[Crossref] [PubMed]

Schart-Morén, N.

S. Agrawal, N. Schart-Morén, W. Liu, H. M. Ladak, H. Rask-Andersen, and H. Li, “The secondary spiral lamina and its relevance in cochlear implant surgery,” Ups. J. Med. Sci. 123(1), 9–18 (2018).
[Crossref] [PubMed]

Schindelin, J.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Schmid, B.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Schrott-Fischer, A.

A. Lareida, F. Beckmann, A. Schrott-Fischer, R. Glueckert, W. Freysinger, and B. Müller, “High-resolution X-ray tomography of the human inner ear: synchrotron radiation-based study of nerve fibre bundles, membranes and ganglion cells,” J. Microsc. 234(1), 95–102 (2009).
[Crossref] [PubMed]

Smith-Bronstein, V.

C. P. Richter, H. Young, S. V. Richter, V. Smith-Bronstein, S. R. Stock, X. Xiao, C. Soriano, and D. S. Whitlon, “Fluvastatin protects cochleae from damage by high-level noise,” Sci. Rep. 8(1), 3033 (2018).
[Crossref] [PubMed]

Soriano, C.

C. P. Richter, H. Young, S. V. Richter, V. Smith-Bronstein, S. R. Stock, X. Xiao, C. Soriano, and D. S. Whitlon, “Fluvastatin protects cochleae from damage by high-level noise,” Sci. Rep. 8(1), 3033 (2018).
[Crossref] [PubMed]

Stock, S. R.

C. P. Richter, H. Young, S. V. Richter, V. Smith-Bronstein, S. R. Stock, X. Xiao, C. Soriano, and D. S. Whitlon, “Fluvastatin protects cochleae from damage by high-level noise,” Sci. Rep. 8(1), 3033 (2018).
[Crossref] [PubMed]

Suortti, R.

T. W. Wysokinski, D. Chapman, G. Adams, M. Renier, R. Suortti, and W. Thomlinson, “Beamlines of the biomedical imaging and therapy facility at the Canadian light source – part 3,” Nucl. Instrum. Methods Phys. Res. A 775, 1–4 (2015).
[Crossref]

Tan, T. Y.

R. S. Z. Yiin, P. H. Tang, and T. Y. Tan, “Review of congenital inner ear abnormalities on CT temporal bone,” Br. J. Radiol. 84(1005), 859–863 (2011).
[Crossref] [PubMed]

Tang, P. H.

R. S. Z. Yiin, P. H. Tang, and T. Y. Tan, “Review of congenital inner ear abnormalities on CT temporal bone,” Br. J. Radiol. 84(1005), 859–863 (2011).
[Crossref] [PubMed]

Thomlinson, W.

T. W. Wysokinski, D. Chapman, G. Adams, M. Renier, R. Suortti, and W. Thomlinson, “Beamlines of the biomedical imaging and therapy facility at the Canadian light source – part 3,” Nucl. Instrum. Methods Phys. Res. A 775, 1–4 (2015).
[Crossref]

Tinevez, J. Y.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Tomancak, P.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

van Egmond, S. L.

S. L. van Egmond, F. Visser, F. A. Pameijer, and W. Grolman, “Ex vivo and in vivo imaging of the inner ear at 7 Tesla MRI,” Otol. Neurotol. 35(4), 725–729 (2014).
[Crossref] [PubMed]

Visser, F.

S. L. van Egmond, F. Visser, F. A. Pameijer, and W. Grolman, “Ex vivo and in vivo imaging of the inner ear at 7 Tesla MRI,” Otol. Neurotol. 35(4), 725–729 (2014).
[Crossref] [PubMed]

Vogel, U.

U. Vogel, “New approach for 3D imaging and geometry modeling of the human inner ear,” ORL J. Otorhinolaryngol. Relat. Spec. 61(5), 259–267 (1999).
[Crossref] [PubMed]

Wang, Z. M.

S. F. Li, T. Y. Zhang, and Z. M. Wang, “An approach for precise three-dimensional modeling of the human inner ear,” ORL J. Otorhinolaryngol. Relat. Spec. 68(5), 302–310 (2006).
[Crossref] [PubMed]

White, D. J.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Whitlon, D. S.

C. P. Richter, H. Young, S. V. Richter, V. Smith-Bronstein, S. R. Stock, X. Xiao, C. Soriano, and D. S. Whitlon, “Fluvastatin protects cochleae from damage by high-level noise,” Sci. Rep. 8(1), 3033 (2018).
[Crossref] [PubMed]

Wu, F.

C. Liu, X. Bu, F. Wu, and G. Xing, “Unilateral auditory neuropathy caused by cochlear nerve deficiency,” Int. J. Otolaryngol. 2012, 1 (2012).
[Crossref] [PubMed]

Würfel, W.

T. S. Rau, W. Würfel, T. Lenarz, and O. Majdani, “Three-dimensional histological specimen preparation for accurate imaging and spatial reconstruction of the middle and inner ear,” Int. J. CARS 8(4), 481–509 (2013).
[Crossref] [PubMed]

Wysokinski, T. W.

T. W. Wysokinski, D. Chapman, G. Adams, M. Renier, R. Suortti, and W. Thomlinson, “Beamlines of the biomedical imaging and therapy facility at the Canadian light source – part 3,” Nucl. Instrum. Methods Phys. Res. A 775, 1–4 (2015).
[Crossref]

Xiao, X.

C. P. Richter, H. Young, S. V. Richter, V. Smith-Bronstein, S. R. Stock, X. Xiao, C. Soriano, and D. S. Whitlon, “Fluvastatin protects cochleae from damage by high-level noise,” Sci. Rep. 8(1), 3033 (2018).
[Crossref] [PubMed]

Xing, G.

C. Liu, X. Bu, F. Wu, and G. Xing, “Unilateral auditory neuropathy caused by cochlear nerve deficiency,” Int. J. Otolaryngol. 2012, 1 (2012).
[Crossref] [PubMed]

Yiin, R. S. Z.

R. S. Z. Yiin, P. H. Tang, and T. Y. Tan, “Review of congenital inner ear abnormalities on CT temporal bone,” Br. J. Radiol. 84(1005), 859–863 (2011).
[Crossref] [PubMed]

Young, H.

C. P. Richter, H. Young, S. V. Richter, V. Smith-Bronstein, S. R. Stock, X. Xiao, C. Soriano, and D. S. Whitlon, “Fluvastatin protects cochleae from damage by high-level noise,” Sci. Rep. 8(1), 3033 (2018).
[Crossref] [PubMed]

Zhang, T. Y.

S. F. Li, T. Y. Zhang, and Z. M. Wang, “An approach for precise three-dimensional modeling of the human inner ear,” ORL J. Otorhinolaryngol. Relat. Spec. 68(5), 302–310 (2006).
[Crossref] [PubMed]

Zhu, N.

M. Elfarnawany, S. R. Alam, S. A. Rohani, N. Zhu, S. K. Agrawal, and H. M. Ladak, “Micro-CT versus synchrotron radiation phase contrast imaging of human cochlea,” J. Microsc. 265(3), 349–357 (2017).
[Crossref] [PubMed]

R. W. Koch, M. Elfarnawany, N. Zhu, H. M. Ladak, and S. K. Agrawal, “Evaluation of cochlear duct length computations using synchrotron radiation phase-contrast imaging,” Otol. Neurotol. 38(6), e92–e99 (2017).
[Crossref] [PubMed]

AJNR Am. J. Neuroradiol. (1)

M. S. Pearl, A. Roy, and C. J. Limb, “High-resolution secondary reconstructions with the use of flat panel CT in the clinical assessment of patients with cochlear implants,” AJNR Am. J. Neuroradiol. 35(6), 1202–1208 (2014).
[Crossref] [PubMed]

Br. J. Radiol. (1)

R. S. Z. Yiin, P. H. Tang, and T. Y. Tan, “Review of congenital inner ear abnormalities on CT temporal bone,” Br. J. Radiol. 84(1005), 859–863 (2011).
[Crossref] [PubMed]

Hear. Res. (1)

A. S. Brunschwig and A. N. Salt, “Fixation-induced shrinkage of Reissner’s membrane and its potential influence on the assessment of endolymph volume,” Hear. Res. 114(1-2), 62–68 (1997).
[Crossref] [PubMed]

Int. J. CARS (1)

T. S. Rau, W. Würfel, T. Lenarz, and O. Majdani, “Three-dimensional histological specimen preparation for accurate imaging and spatial reconstruction of the middle and inner ear,” Int. J. CARS 8(4), 481–509 (2013).
[Crossref] [PubMed]

Int. J. Otolaryngol. (1)

C. Liu, X. Bu, F. Wu, and G. Xing, “Unilateral auditory neuropathy caused by cochlear nerve deficiency,” Int. J. Otolaryngol. 2012, 1 (2012).
[Crossref] [PubMed]

J. Acoust. Soc. Am. (2)

D. D. Greenwood, “Audtory masking and the critical band,” J. Acoust. Soc. Am. 33(4), 484–502 (1961).
[Crossref]

D. D. Greenwood, “Critical bandwidth and the frequency coordinates of the basilar membrane,” J. Acoust. Soc. Am. 33(10), 1344–1356 (1961).
[Crossref]

J. Int. Soc. Plastination. (1)

M. A. Brown, R. B. Reed, and R. W. Henry, “Effects of dehydration mediums and temperature on total dehydration time and tissue shrinkage,” J. Int. Soc. Plastination. 33, 28–33 (2002).

J. Microsc. (2)

M. Elfarnawany, S. R. Alam, S. A. Rohani, N. Zhu, S. K. Agrawal, and H. M. Ladak, “Micro-CT versus synchrotron radiation phase contrast imaging of human cochlea,” J. Microsc. 265(3), 349–357 (2017).
[Crossref] [PubMed]

A. Lareida, F. Beckmann, A. Schrott-Fischer, R. Glueckert, W. Freysinger, and B. Müller, “High-resolution X-ray tomography of the human inner ear: synchrotron radiation-based study of nerve fibre bundles, membranes and ganglion cells,” J. Microsc. 234(1), 95–102 (2009).
[Crossref] [PubMed]

J. Oral Maxillofac. Pathol. (1)

S. Chatterjee, “Artefacts in histopathology,” J. Oral Maxillofac. Pathol. 18(4), S111–S116 (2014).
[Crossref] [PubMed]

Nat. Methods (1)

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Nucl. Instrum. Methods Phys. Res. A (1)

T. W. Wysokinski, D. Chapman, G. Adams, M. Renier, R. Suortti, and W. Thomlinson, “Beamlines of the biomedical imaging and therapy facility at the Canadian light source – part 3,” Nucl. Instrum. Methods Phys. Res. A 775, 1–4 (2015).
[Crossref]

ORL J. Otorhinolaryngol. Relat. Spec. (2)

S. F. Li, T. Y. Zhang, and Z. M. Wang, “An approach for precise three-dimensional modeling of the human inner ear,” ORL J. Otorhinolaryngol. Relat. Spec. 68(5), 302–310 (2006).
[Crossref] [PubMed]

U. Vogel, “New approach for 3D imaging and geometry modeling of the human inner ear,” ORL J. Otorhinolaryngol. Relat. Spec. 61(5), 259–267 (1999).
[Crossref] [PubMed]

Otol. Neurotol. (2)

S. L. van Egmond, F. Visser, F. A. Pameijer, and W. Grolman, “Ex vivo and in vivo imaging of the inner ear at 7 Tesla MRI,” Otol. Neurotol. 35(4), 725–729 (2014).
[Crossref] [PubMed]

R. W. Koch, M. Elfarnawany, N. Zhu, H. M. Ladak, and S. K. Agrawal, “Evaluation of cochlear duct length computations using synchrotron radiation phase-contrast imaging,” Otol. Neurotol. 38(6), e92–e99 (2017).
[Crossref] [PubMed]

PLoS One (1)

C. Rau, M. Hwang, W. K. Lee, and C. P. Richter, “Quantitative X-ray tomography of the mouse cochlea,” PLoS One 7(4), e33568 (2012).
[Crossref] [PubMed]

Sci. Rep. (1)

C. P. Richter, H. Young, S. V. Richter, V. Smith-Bronstein, S. R. Stock, X. Xiao, C. Soriano, and D. S. Whitlon, “Fluvastatin protects cochleae from damage by high-level noise,” Sci. Rep. 8(1), 3033 (2018).
[Crossref] [PubMed]

The Registry (1)

R. A. Chole and M. J. McKenna, “A silent and imminent threat,” The Registry 20(2), 1–2 (2012).

Ups. J. Med. Sci. (1)

S. Agrawal, N. Schart-Morén, W. Liu, H. M. Ladak, H. Rask-Andersen, and H. Li, “The secondary spiral lamina and its relevance in cochlear implant surgery,” Ups. J. Med. Sci. 123(1), 9–18 (2018).
[Crossref] [PubMed]

Other (6)

M. C. Liberman, “The auditory nerve in profoundly deaf ears,” presented at the Association for Research in Otolaryngology, San Diego, CA, USA, 9–14 Feb. 2018.

A. Politzer, The Anatomical and Histological Dissection of the Human Inner Ear: in the Normal and Diseased Condition (Baillière, Tindall and Cox, 1892).

S. N. Merchant and J. B. Nadol, Schuknecht’s Pathology of the Ear (Lea and Febiger, Malvern, 1993).

World Health Organization Fact Sheet, “Deafness and hearing loss,” (World Health Organization, 2017), http://www.who.int/mediacentre/factsheets/fs300/en/

D. Ali and A. F. Chatziioannou, Basic Sciences in Nuclear Medicine, (Springer-Verlag, 2011).

S. G. Nekolla and A. Saraste, Cardiac CT, PET, and MR (Wiley-Blackwell, 2010).

Supplementary Material (3)

NameDescription
» Visualization 1       Visualization 1: SR-PCI-facilitated visualization of the facial nerve, two trunks of the vestibulocochlear nerve, and individual nerve fiber bundles and branches of the labyrinthine artery.
» Visualization 2       Visualization 2: SR-PCI-facilitated visualization of the organ of Corti’s cellular composition via a “fly-through” video reconstruction. Individual rows of auditory hair cells are seen spiraling up toward the cochlea’s apex.
» Visualization 3       Visualization 3: SR-PCI-facilitated visualization of the vestibular sensory epithelia, highlighting the locations of the superior semicircular canal, the cristae ampullaris of the superior and posterior ampullae, and the utricular macula.

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Figures (8)

Fig. 1
Fig. 1 Micro-CT image of the human head, virtually sectioned through the temporal bone to reveal the outer, middle, and inner ear portions of the peripheral auditory system. The cochlea (•)’s spiral shape and deep encasement within bone are appreciated. * = auricle (outer ear); ■ = malleus, first of the three middle ear ossicles. Scale = 2.5cm.

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Fig. 2
Fig. 2 (A) Mid-modiolar section of an H&E-stained human cochlea. Five cochlear half-turns, corresponding to the 2 ¾ cochlear turns in the human cochlea, are seen spiraling around the modiolus (MOD), the bony trunk that contains spiral ganglion neuronal cell bodies and axons traveling to and from the auditory nerve (AN). The basilar membrane (*) and Reissner’s membrane (•) define the boundaries between the cochlea’s three fluid-filled lumina: scala tympani (ST), scala media (SM), and scala vestibuli (SV). The lateral wall (■) attaches the basilar membrane to the cochlea’s osseous shell, the otic capsule. Standard CT (B), μCT (C), and SR-PCI (D) images of virtual mid-modiolar sections through a human cochlea in situ are also shown. The differences in visualizability of intracochlear structures across the three X-ray-based imaging modalities are dramatic. All scales = 2mm.

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Fig. 3
Fig. 3 (A) Mid-modiolar 3D virtual cross-section through the dehydrated human cochlea. Three rows of outer hair cells (red dots), one row of inner hair cells (blue dots), the region of the spiral ligament and stria vascularis (pink dot), and Rosenthal’s canal (orange dot) are clearly visualized. Individual bundles of spiral ganglion neuronal fibers (green arrow) and the auditory nerve trunk (green outline) are also visualized. (B) Mid-modiolar 3D virtual cross-section through the non-dehydrated human cochlea, illustrating that similar visualization is achieved through dehydration and fixation without dehydration. Lateral wall is damaged in (B) due to simulated poor electrode array insertion. Both scales = 1mm.

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Fig. 4
Fig. 4 Endoscopic still images allowing clear visualization of the internal auditory meatus’ contents in a right ear, highlighting the facial nerve (VII) and two trunks of the vestibulocochlear nerve (VIIIc, VIIIv; (A), and bundles of nerve fiber axons and branches of the labyrinthine artery (B); white arrows). VIIIc = cochlear branch; VIIIv = vestibular branch. Figure corresponds to Visualization 1.

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Fig. 5
Fig. 5 3D virtual whole mount section revealing a surface view of the organ of Corti in situ in the temporal bone using SR-PCI. The complex cytoarchitecture of the organ of Corti, including the three rows of outer hair cells (red dots), single row of inner pillar cells (yellow dot), single row of inner hair cells (blue dot), spiral limbus (pink underline), and fan of auditory nerve fiber bundles (green underline) is clearly visualized. Scale = 1mm.

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Fig. 6
Fig. 6 Virtual whole mounts of three regions of the human organ of Corti, illustrating SR-PCI’s ability to distinguish between healthy (A) and damaged (B, C) tissue. (A) SR-PCI virtual whole mount sectioned from the upper basal-to-middle turn; individual rows of hair cells and the fan of auditory nerve fibers are clearly visible. (B) SR-PCI virtual whole mount sectioned from the base; hypothesized region of presbycusis is outlined in green. (C) SR-PCI virtual whole mount sectioned from the base of a cochlear specimen which had undergone simulated insertion trauma (pink outline). All scales = 1mm.

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Fig. 7
Fig. 7 Still images acquired at three different time points (A, B, C) in an endoscopic “fly-through” video (Visualization 2) allowing the viewer to fly into scala vestibuli to view the cochlea’s interior in 3D from within.

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Fig. 8
Fig. 8 3D volumetric analysis of the vestibular organs in a right human temporal bone. (A) Bone was virtually sectioned along several planes to reveal two of the vestibular system’s sensory epithelia. A schematic orienting the reader to these structures is in panel (B). V = vestibule; M = utricular macula; C = cochlea; OW = oval window; RW = round window; CA = crista ampullaris (posterior ampulla). (C) Still image highlighting the vestibular structures seen in Visualization 3; the black arrow indicates the position and orientation of the superior semicircular canal; double white asterisks mark the utricular macula; single white asterisk marks the crista ampullaris of the posterior ampulla; single black asterisk marks the crista ampullaris of the superior ampulla. Scales = 0.5mm.

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