Abstract

Human vocal folds (VFs) possess a unique anatomical structure and mechanical properties for human communication. However, VFs are prone to scarring as a consequence of overuse, injury, disease or surgery. Accumulation of scar tissue on VFs inhibits proper phonation and leads to partial or complete loss of voice, with significant consequences for the patient’s quality of life. VF regeneration after scarring provides a significant challenge for tissue engineering therapies given the complexity of tissue microarchitecture. To establish an effective animal model for VF injury and scarring, new histological methods are required to visualize the wound repair process of the tissue in its three-dimensional native environment. In this work, we propose the use of a combination of nonlinear microscopy and nanotomography as contrast methods for virtual histology of rabbit VFs. We apply these methods to rabbit VF tissue to demonstrate their use as alternatives to conventional VF histology that may enable future clinical studies of this injury model.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

Full Article  |  PDF Article
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References

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2018 (2)

L. Bailly, T. Cochereau, L. Orgéas, N. Henrich Bernardoni, S. Rolland du Roscoat, A. McLeer-Florin, Y. Robert, X. Laval, T. Laurencin, P. Chaffanjon, B. Fayard, and E. Boller, “3D multiscale imaging of human vocal folds using synchrotron X-ray microtomography in phase retrieval mode,” Sci. Rep. 8(1), 14003 (2018).
[Crossref] [PubMed]

L. Nolte, G. C. Antonopoulos, L. Rämisch, A. Heisterkamp, T. Ripken, and H. Meyer, “Enabling second harmonic generation as a contrast mechanism for optical projection tomography (OPT) and scanning laser optical tomography (SLOT),” Biomed. Opt. Express 9(6), 2627–2639 (2018).
[Crossref] [PubMed]

2017 (4)

A. Mattei, J. Magalon, B. Bertrand, C. Philandrianos, J. Veran, and A. Giovanni, “Cell therapy and vocal fold scarring,” Eur. Ann. Otorhinolaryngol. Head Neck Dis. 134(5), 339–345 (2017).
[Crossref] [PubMed]

W. Chen, P. Woo, and T. Murry, “Vocal Fold Vibration Following Surgical Intervention in Three Vocal Pathologies: A Preliminary Study,” J. Voice 31(5), 610–614 (2017).
[Crossref] [PubMed]

P. Ariel, “A beginner’s guide to tissue clearing,” Int. J. Biochem. Cell Biol. 84, 35–39 (2017).
[Crossref] [PubMed]

M. J. Ban, J. H. Park, J. W. Kim, K. N. Park, J. Y. Lee, H. K. Kim, and S. W. Lee, “The Efficacy of Fibroblast Growth Factor for the Treatment of Chronic Vocal Fold Scarring: From Animal Model to Clinical Application,” Clin. Exp. Otorhinolaryngol. 10(4), 349–356 (2017).
[Crossref] [PubMed]

2016 (4)

M. Senter-Zapata, K. Patel, P. A. Bautista, M. Griffin, J. Michaelson, and Y. Yagi, “The role of micro-CT in 3D histology imaging,” Pathobiology 83(2-3), 140–147 (2016).
[Crossref] [PubMed]

C. Pan, R. Cai, F. P. Quacquarelli, A. Ghasemigharagoz, A. Lourbopoulos, P. Matryba, N. Plesnila, M. Dichgans, F. Hellal, and A. Ertürk, “Shrinkage-mediated imaging of entire organs and organisms using uDISCO,” Nat. Methods 13(10), 859–867 (2016).
[Crossref] [PubMed]

L. E. Tracy, R. A. Minasian, and E. J. Caterson, “Extracellular Matrix and Dermal Fibroblast Function in the Healing Wound,” Adv. Wound Care (New Rochelle) 5(3), 119–136 (2016).
[Crossref] [PubMed]

A. O. Kishimoto, Y. Kishimoto, D. L. Young, J. Zhang, I. J. Rowland, and N. V. Welham, “High- and ultrahigh-field magnetic resonance imaging of naïve, injured and scarred vocal fold mucosae in rats,” Dis. Model. Mech. 9(11), 1397–1403 (2016).
[Crossref] [PubMed]

2015 (2)

D. S. Richardson and J. W. Lichtman, “Clarifying Tissue Clearing,” Cell 162(2), 246–257 (2015).
[Crossref] [PubMed]

H. K. Heris, A. K. Miri, N. R. Ghattamaneni, N. Y. Li, S. L. Thibeault, P. W. Wiseman, and L. Mongeau, “Microstructural and mechanical characterization of scarred vocal folds,” J. Biomech. 48(4), 708–711 (2015).
[Crossref] [PubMed]

2014 (4)

K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Ukai-Tadenuma, H. Ukai, and H. R. Ueda, “Whole-body imaging with single-cell resolution by tissue decolorization,” Cell 159(4), 911–924 (2014).
[Crossref] [PubMed]

R. Tomer, L. Ye, B. Hsueh, and K. Deisseroth, “Advanced CLARITY for rapid and high-resolution imaging of intact tissues,” Nat. Protoc. 9(7), 1682–1697 (2014).
[Crossref] [PubMed]

J. M. Coppoolse, T. G. Van Kooten, H. K. Heris, L. Mongeau, N. Y. Li, S. L. Thibeault, J. Pitaro, O. Akinpelu, and S. J. Daniel, “An in vivo study of composite microgels based on hyaluronic acid and gelatin for the reconstruction of surgically injured rat vocal folds,” J. Speech Lang. Hear. Res. 57(2), S658–S673 (2014).
[Crossref] [PubMed]

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

2013 (5)

F. O. Fahrbach, V. Gurchenkov, K. Alessandri, P. Nassoy, and A. Rohrbach, “Light-sheet microscopy in thick media using scanned Bessel beams and two-photon fluorescence excitation,” Opt. Express 21(11), 13824–13839 (2013).
[Crossref] [PubMed]

F. Cella Zanacchi, Z. Lavagnino, M. Faretta, L. Furia, and A. Diaspro, “Light-Sheet Confined Super-Resolution Using Two-Photon Photoactivation,” PLoS One 8(7), e67667 (2013).
[Crossref] [PubMed]

A. K. Miri, H. K. Heris, U. Tripathy, P. W. Wiseman, and L. Mongeau, “Microstructural characterization of vocal folds toward a strain-energy model of collagen remodeling,” Acta Biomater. 9(8), 7957–7967 (2013).
[Crossref] [PubMed]

H. K. Heris, A. K. Miri, U. Tripathy, F. Barthelat, and L. Mongeau, “Indentation of poroviscoelastic vocal fold tissue using an atomic force microscope,” J. Mech. Behav. Biomed. Mater. 28, 383–392 (2013).
[Crossref] [PubMed]

G. Friedrich, F. G. Dikkers, C. Arens, M. Remacle, M. Hess, A. Giovanni, S. Duflo, A. Hantzakos, V. Bachy, M. Gugatschka, and European Laryngological Society. Phonosurgery Committee, “Vocal fold scars: current concepts and future directions. Consensus report of the Phonosurgery Committee of the European Laryngological Society,” Eur. Arch. Otorhinolaryngol. 270(9), 2491–2507 (2013).
[Crossref] [PubMed]

2012 (2)

A. K. Miri, U. Tripathy, L. Mongeau, and P. W. Wiseman, “Nonlinear laser scanning microscopy of human vocal folds,” Laryngoscope 122(2), 356–363 (2012).
[Crossref] [PubMed]

A. Suehiro, J. M. Bock, J. E. Hall, C. G. Garrett, and B. Rousseau, “Feasibility and acute healing of vocal fold microflap incisions in a rabbit model,” Laryngoscope 122(3), 600–605 (2012).
[Crossref] [PubMed]

2010 (1)

A. M. Campagnolo, D. H. Tsuji, L. U. Sennes, R. Imamura, and P. H. Saldiva, “Histologic study of acute vocal fold wound healing after corticosteroid injection in a rabbit model,” Ann. Otol. Rhinol. Laryngol. 119(2), 133–139 (2010).
[Crossref] [PubMed]

2009 (2)

B. D. Metscher, “MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions,” Dev. Dyn. 238(3), 632–640 (2009).
[Crossref] [PubMed]

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the Second-Order Hyperpolarizability of the Collagen Triple Helix and Determination of Its Physical Origin,” J. Phys. Chem. B 113(40), 13437–13445 (2009).
[Crossref] [PubMed]

2008 (1)

P. P. Mondal and A. Diaspro, “Lateral resolution improvement in two-photon excitation microscopy by aperture engineering,” Opt. Commun. 281(7), 1855–1859 (2008).
[Crossref]

2007 (1)

P. J. Withers, “X-ray nanotomography,” Mater. Today 10(12), 26–34 (2007).
[Crossref]

2006 (2)

J. K. Hansen and S. L. Thibeault, “Current understanding and review of the literature: vocal fold scarring,” J. Voice 20(1), 110–120 (2006).
[Crossref] [PubMed]

P. Theer and W. Denk, “On the fundamental imaging-depth limit in two-photon microscopy,” J. Opt. Soc. Am. A 23(12), 3139–3149 (2006).
[Crossref] [PubMed]

2005 (3)

M. Titford, “The long history of hematoxylin,” Biotech. Histochem. 80(2), 73–78 (2005).
[Crossref] [PubMed]

S. Krischke, S. Weigelt, U. Hoppe, V. Köllner, M. Klotz, U. Eysholdt, and F. Rosanowski, “Quality of life in dysphonic patients,” J. Voice 19(1), 132–137 (2005).
[Crossref] [PubMed]

S. Hirano, “Current treatment of vocal fold scarring,” Curr. Opin. Otolaryngol. Head Neck Surg. 13(3), 143–147 (2005).
[Crossref] [PubMed]

2004 (1)

B. Rousseau, S. Hirano, R. W. Chan, N. V. Welham, S. L. Thibeault, C. N. Ford, and D. M. Bless, “Characterization of chronic vocal fold scarring in a rabbit model,” J. Voice 18(1), 116–124 (2004).
[Crossref] [PubMed]

2003 (3)

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[Crossref] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[Crossref] [PubMed]

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
[Crossref] [PubMed]

2002 (1)

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-Modulated Second Harmonic Generation in Collagen,” Biophys. J. 82(6), 3330–3342 (2002).
[Crossref] [PubMed]

1996 (1)

M. S. Benninger, D. Alessi, S. Archer, R. Bastian, C. Ford, J. Koufman, R. T. Sataloff, J. R. Spiegel, and P. Woo, “Vocal fold scarring: current concepts and management,” Otolaryngol. Head Neck Surg. 115(5), 474–482 (1996).
[PubMed]

1974 (1)

M. Hirano, “Morphological Structure of the Vocal Cord as a Vibrator and its Variations,” Folia Phoniatr. (Basel) 26(2), 89–94 (1974).
[Crossref] [PubMed]

Akinpelu, O.

J. M. Coppoolse, T. G. Van Kooten, H. K. Heris, L. Mongeau, N. Y. Li, S. L. Thibeault, J. Pitaro, O. Akinpelu, and S. J. Daniel, “An in vivo study of composite microgels based on hyaluronic acid and gelatin for the reconstruction of surgically injured rat vocal folds,” J. Speech Lang. Hear. Res. 57(2), S658–S673 (2014).
[Crossref] [PubMed]

Alessandri, K.

Alessi, D.

M. S. Benninger, D. Alessi, S. Archer, R. Bastian, C. Ford, J. Koufman, R. T. Sataloff, J. R. Spiegel, and P. Woo, “Vocal fold scarring: current concepts and management,” Otolaryngol. Head Neck Surg. 115(5), 474–482 (1996).
[PubMed]

Antonopoulos, G. C.

Archer, S.

M. S. Benninger, D. Alessi, S. Archer, R. Bastian, C. Ford, J. Koufman, R. T. Sataloff, J. R. Spiegel, and P. Woo, “Vocal fold scarring: current concepts and management,” Otolaryngol. Head Neck Surg. 115(5), 474–482 (1996).
[PubMed]

Arens, C.

G. Friedrich, F. G. Dikkers, C. Arens, M. Remacle, M. Hess, A. Giovanni, S. Duflo, A. Hantzakos, V. Bachy, M. Gugatschka, and European Laryngological Society. Phonosurgery Committee, “Vocal fold scars: current concepts and future directions. Consensus report of the Phonosurgery Committee of the European Laryngological Society,” Eur. Arch. Otorhinolaryngol. 270(9), 2491–2507 (2013).
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M. Senter-Zapata, K. Patel, P. A. Bautista, M. Griffin, J. Michaelson, and Y. Yagi, “The role of micro-CT in 3D histology imaging,” Pathobiology 83(2-3), 140–147 (2016).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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A. Suehiro, J. M. Bock, J. E. Hall, C. G. Garrett, and B. Rousseau, “Feasibility and acute healing of vocal fold microflap incisions in a rabbit model,” Laryngoscope 122(3), 600–605 (2012).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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Diaspro, A.

F. Cella Zanacchi, Z. Lavagnino, M. Faretta, L. Furia, and A. Diaspro, “Light-Sheet Confined Super-Resolution Using Two-Photon Photoactivation,” PLoS One 8(7), e67667 (2013).
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A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the Second-Order Hyperpolarizability of the Collagen Triple Helix and Determination of Its Physical Origin,” J. Phys. Chem. B 113(40), 13437–13445 (2009).
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G. Friedrich, F. G. Dikkers, C. Arens, M. Remacle, M. Hess, A. Giovanni, S. Duflo, A. Hantzakos, V. Bachy, M. Gugatschka, and European Laryngological Society. Phonosurgery Committee, “Vocal fold scars: current concepts and future directions. Consensus report of the Phonosurgery Committee of the European Laryngological Society,” Eur. Arch. Otorhinolaryngol. 270(9), 2491–2507 (2013).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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F. Cella Zanacchi, Z. Lavagnino, M. Faretta, L. Furia, and A. Diaspro, “Light-Sheet Confined Super-Resolution Using Two-Photon Photoactivation,” PLoS One 8(7), e67667 (2013).
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L. Bailly, T. Cochereau, L. Orgéas, N. Henrich Bernardoni, S. Rolland du Roscoat, A. McLeer-Florin, Y. Robert, X. Laval, T. Laurencin, P. Chaffanjon, B. Fayard, and E. Boller, “3D multiscale imaging of human vocal folds using synchrotron X-ray microtomography in phase retrieval mode,” Sci. Rep. 8(1), 14003 (2018).
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M. S. Benninger, D. Alessi, S. Archer, R. Bastian, C. Ford, J. Koufman, R. T. Sataloff, J. R. Spiegel, and P. Woo, “Vocal fold scarring: current concepts and management,” Otolaryngol. Head Neck Surg. 115(5), 474–482 (1996).
[PubMed]

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B. Rousseau, S. Hirano, R. W. Chan, N. V. Welham, S. L. Thibeault, C. N. Ford, and D. M. Bless, “Characterization of chronic vocal fold scarring in a rabbit model,” J. Voice 18(1), 116–124 (2004).
[Crossref] [PubMed]

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G. Friedrich, F. G. Dikkers, C. Arens, M. Remacle, M. Hess, A. Giovanni, S. Duflo, A. Hantzakos, V. Bachy, M. Gugatschka, and European Laryngological Society. Phonosurgery Committee, “Vocal fold scars: current concepts and future directions. Consensus report of the Phonosurgery Committee of the European Laryngological Society,” Eur. Arch. Otorhinolaryngol. 270(9), 2491–2507 (2013).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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F. Cella Zanacchi, Z. Lavagnino, M. Faretta, L. Furia, and A. Diaspro, “Light-Sheet Confined Super-Resolution Using Two-Photon Photoactivation,” PLoS One 8(7), e67667 (2013).
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Garrett, C. G.

A. Suehiro, J. M. Bock, J. E. Hall, C. G. Garrett, and B. Rousseau, “Feasibility and acute healing of vocal fold microflap incisions in a rabbit model,” Laryngoscope 122(3), 600–605 (2012).
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C. Pan, R. Cai, F. P. Quacquarelli, A. Ghasemigharagoz, A. Lourbopoulos, P. Matryba, N. Plesnila, M. Dichgans, F. Hellal, and A. Ertürk, “Shrinkage-mediated imaging of entire organs and organisms using uDISCO,” Nat. Methods 13(10), 859–867 (2016).
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A. Mattei, J. Magalon, B. Bertrand, C. Philandrianos, J. Veran, and A. Giovanni, “Cell therapy and vocal fold scarring,” Eur. Ann. Otorhinolaryngol. Head Neck Dis. 134(5), 339–345 (2017).
[Crossref] [PubMed]

G. Friedrich, F. G. Dikkers, C. Arens, M. Remacle, M. Hess, A. Giovanni, S. Duflo, A. Hantzakos, V. Bachy, M. Gugatschka, and European Laryngological Society. Phonosurgery Committee, “Vocal fold scars: current concepts and future directions. Consensus report of the Phonosurgery Committee of the European Laryngological Society,” Eur. Arch. Otorhinolaryngol. 270(9), 2491–2507 (2013).
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Griffin, M.

M. Senter-Zapata, K. Patel, P. A. Bautista, M. Griffin, J. Michaelson, and Y. Yagi, “The role of micro-CT in 3D histology imaging,” Pathobiology 83(2-3), 140–147 (2016).
[Crossref] [PubMed]

Grill, S. W.

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Gugatschka, M.

G. Friedrich, F. G. Dikkers, C. Arens, M. Remacle, M. Hess, A. Giovanni, S. Duflo, A. Hantzakos, V. Bachy, M. Gugatschka, and European Laryngological Society. Phonosurgery Committee, “Vocal fold scars: current concepts and future directions. Consensus report of the Phonosurgery Committee of the European Laryngological Society,” Eur. Arch. Otorhinolaryngol. 270(9), 2491–2507 (2013).
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Hache, F.

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the Second-Order Hyperpolarizability of the Collagen Triple Helix and Determination of Its Physical Origin,” J. Phys. Chem. B 113(40), 13437–13445 (2009).
[Crossref] [PubMed]

Hall, J. E.

A. Suehiro, J. M. Bock, J. E. Hall, C. G. Garrett, and B. Rousseau, “Feasibility and acute healing of vocal fold microflap incisions in a rabbit model,” Laryngoscope 122(3), 600–605 (2012).
[Crossref] [PubMed]

Hammer, J. A.

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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J. K. Hansen and S. L. Thibeault, “Current understanding and review of the literature: vocal fold scarring,” J. Voice 20(1), 110–120 (2006).
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G. Friedrich, F. G. Dikkers, C. Arens, M. Remacle, M. Hess, A. Giovanni, S. Duflo, A. Hantzakos, V. Bachy, M. Gugatschka, and European Laryngological Society. Phonosurgery Committee, “Vocal fold scars: current concepts and future directions. Consensus report of the Phonosurgery Committee of the European Laryngological Society,” Eur. Arch. Otorhinolaryngol. 270(9), 2491–2507 (2013).
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M. Senter-Zapata, K. Patel, P. A. Bautista, M. Griffin, J. Michaelson, and Y. Yagi, “The role of micro-CT in 3D histology imaging,” Pathobiology 83(2-3), 140–147 (2016).
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A. Mattei, J. Magalon, B. Bertrand, C. Philandrianos, J. Veran, and A. Giovanni, “Cell therapy and vocal fold scarring,” Eur. Ann. Otorhinolaryngol. Head Neck Dis. 134(5), 339–345 (2017).
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P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-Modulated Second Harmonic Generation in Collagen,” Biophys. J. 82(6), 3330–3342 (2002).
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P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-Modulated Second Harmonic Generation in Collagen,” Biophys. J. 82(6), 3330–3342 (2002).
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A. Suehiro, J. M. Bock, J. E. Hall, C. G. Garrett, and B. Rousseau, “Feasibility and acute healing of vocal fold microflap incisions in a rabbit model,” Laryngoscope 122(3), 600–605 (2012).
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K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Ukai-Tadenuma, H. Ukai, and H. R. Ueda, “Whole-body imaging with single-cell resolution by tissue decolorization,” Cell 159(4), 911–924 (2014).
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K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Ukai-Tadenuma, H. Ukai, and H. R. Ueda, “Whole-body imaging with single-cell resolution by tissue decolorization,” Cell 159(4), 911–924 (2014).
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L. E. Tracy, R. A. Minasian, and E. J. Caterson, “Extracellular Matrix and Dermal Fibroblast Function in the Healing Wound,” Adv. Wound Care (New Rochelle) 5(3), 119–136 (2016).
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A. K. Miri, U. Tripathy, L. Mongeau, and P. W. Wiseman, “Nonlinear laser scanning microscopy of human vocal folds,” Laryngoscope 122(2), 356–363 (2012).
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A. M. Campagnolo, D. H. Tsuji, L. U. Sennes, R. Imamura, and P. H. Saldiva, “Histologic study of acute vocal fold wound healing after corticosteroid injection in a rabbit model,” Ann. Otol. Rhinol. Laryngol. 119(2), 133–139 (2010).
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B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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J. M. Coppoolse, T. G. Van Kooten, H. K. Heris, L. Mongeau, N. Y. Li, S. L. Thibeault, J. Pitaro, O. Akinpelu, and S. J. Daniel, “An in vivo study of composite microgels based on hyaluronic acid and gelatin for the reconstruction of surgically injured rat vocal folds,” J. Speech Lang. Hear. Res. 57(2), S658–S673 (2014).
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S. Krischke, S. Weigelt, U. Hoppe, V. Köllner, M. Klotz, U. Eysholdt, and F. Rosanowski, “Quality of life in dysphonic patients,” J. Voice 19(1), 132–137 (2005).
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W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
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Wiseman, P. W.

H. K. Heris, A. K. Miri, N. R. Ghattamaneni, N. Y. Li, S. L. Thibeault, P. W. Wiseman, and L. Mongeau, “Microstructural and mechanical characterization of scarred vocal folds,” J. Biomech. 48(4), 708–711 (2015).
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A. K. Miri, H. K. Heris, U. Tripathy, P. W. Wiseman, and L. Mongeau, “Microstructural characterization of vocal folds toward a strain-energy model of collagen remodeling,” Acta Biomater. 9(8), 7957–7967 (2013).
[Crossref] [PubMed]

A. K. Miri, U. Tripathy, L. Mongeau, and P. W. Wiseman, “Nonlinear laser scanning microscopy of human vocal folds,” Laryngoscope 122(2), 356–363 (2012).
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Wu, X. S.

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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Yagi, Y.

M. Senter-Zapata, K. Patel, P. A. Bautista, M. Griffin, J. Michaelson, and Y. Yagi, “The role of micro-CT in 3D histology imaging,” Pathobiology 83(2-3), 140–147 (2016).
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Ye, L.

R. Tomer, L. Ye, B. Hsueh, and K. Deisseroth, “Advanced CLARITY for rapid and high-resolution imaging of intact tissues,” Nat. Protoc. 9(7), 1682–1697 (2014).
[Crossref] [PubMed]

Young, D. L.

A. O. Kishimoto, Y. Kishimoto, D. L. Young, J. Zhang, I. J. Rowland, and N. V. Welham, “High- and ultrahigh-field magnetic resonance imaging of naïve, injured and scarred vocal fold mucosae in rats,” Dis. Model. Mech. 9(11), 1397–1403 (2016).
[Crossref] [PubMed]

Zhang, J.

A. O. Kishimoto, Y. Kishimoto, D. L. Young, J. Zhang, I. J. Rowland, and N. V. Welham, “High- and ultrahigh-field magnetic resonance imaging of naïve, injured and scarred vocal fold mucosae in rats,” Dis. Model. Mech. 9(11), 1397–1403 (2016).
[Crossref] [PubMed]

Zipfel, W. R.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[Crossref] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[Crossref] [PubMed]

Acta Biomater. (1)

A. K. Miri, H. K. Heris, U. Tripathy, P. W. Wiseman, and L. Mongeau, “Microstructural characterization of vocal folds toward a strain-energy model of collagen remodeling,” Acta Biomater. 9(8), 7957–7967 (2013).
[Crossref] [PubMed]

Adv. Wound Care (New Rochelle) (1)

L. E. Tracy, R. A. Minasian, and E. J. Caterson, “Extracellular Matrix and Dermal Fibroblast Function in the Healing Wound,” Adv. Wound Care (New Rochelle) 5(3), 119–136 (2016).
[Crossref] [PubMed]

Ann. Otol. Rhinol. Laryngol. (1)

A. M. Campagnolo, D. H. Tsuji, L. U. Sennes, R. Imamura, and P. H. Saldiva, “Histologic study of acute vocal fold wound healing after corticosteroid injection in a rabbit model,” Ann. Otol. Rhinol. Laryngol. 119(2), 133–139 (2010).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

Biophys. J. (1)

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-Modulated Second Harmonic Generation in Collagen,” Biophys. J. 82(6), 3330–3342 (2002).
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Biotech. Histochem. (1)

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Cell (2)

D. S. Richardson and J. W. Lichtman, “Clarifying Tissue Clearing,” Cell 162(2), 246–257 (2015).
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K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Ukai-Tadenuma, H. Ukai, and H. R. Ueda, “Whole-body imaging with single-cell resolution by tissue decolorization,” Cell 159(4), 911–924 (2014).
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Clin. Exp. Otorhinolaryngol. (1)

M. J. Ban, J. H. Park, J. W. Kim, K. N. Park, J. Y. Lee, H. K. Kim, and S. W. Lee, “The Efficacy of Fibroblast Growth Factor for the Treatment of Chronic Vocal Fold Scarring: From Animal Model to Clinical Application,” Clin. Exp. Otorhinolaryngol. 10(4), 349–356 (2017).
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Curr. Opin. Otolaryngol. Head Neck Surg. (1)

S. Hirano, “Current treatment of vocal fold scarring,” Curr. Opin. Otolaryngol. Head Neck Surg. 13(3), 143–147 (2005).
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Dev. Dyn. (1)

B. D. Metscher, “MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions,” Dev. Dyn. 238(3), 632–640 (2009).
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Dis. Model. Mech. (1)

A. O. Kishimoto, Y. Kishimoto, D. L. Young, J. Zhang, I. J. Rowland, and N. V. Welham, “High- and ultrahigh-field magnetic resonance imaging of naïve, injured and scarred vocal fold mucosae in rats,” Dis. Model. Mech. 9(11), 1397–1403 (2016).
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Eur. Ann. Otorhinolaryngol. Head Neck Dis. (1)

A. Mattei, J. Magalon, B. Bertrand, C. Philandrianos, J. Veran, and A. Giovanni, “Cell therapy and vocal fold scarring,” Eur. Ann. Otorhinolaryngol. Head Neck Dis. 134(5), 339–345 (2017).
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Eur. Arch. Otorhinolaryngol. (1)

G. Friedrich, F. G. Dikkers, C. Arens, M. Remacle, M. Hess, A. Giovanni, S. Duflo, A. Hantzakos, V. Bachy, M. Gugatschka, and European Laryngological Society. Phonosurgery Committee, “Vocal fold scars: current concepts and future directions. Consensus report of the Phonosurgery Committee of the European Laryngological Society,” Eur. Arch. Otorhinolaryngol. 270(9), 2491–2507 (2013).
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Folia Phoniatr. (Basel) (1)

M. Hirano, “Morphological Structure of the Vocal Cord as a Vibrator and its Variations,” Folia Phoniatr. (Basel) 26(2), 89–94 (1974).
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Int. J. Biochem. Cell Biol. (1)

P. Ariel, “A beginner’s guide to tissue clearing,” Int. J. Biochem. Cell Biol. 84, 35–39 (2017).
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H. K. Heris, A. K. Miri, N. R. Ghattamaneni, N. Y. Li, S. L. Thibeault, P. W. Wiseman, and L. Mongeau, “Microstructural and mechanical characterization of scarred vocal folds,” J. Biomech. 48(4), 708–711 (2015).
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J. Mech. Behav. Biomed. Mater. (1)

H. K. Heris, A. K. Miri, U. Tripathy, F. Barthelat, and L. Mongeau, “Indentation of poroviscoelastic vocal fold tissue using an atomic force microscope,” J. Mech. Behav. Biomed. Mater. 28, 383–392 (2013).
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J. Opt. Soc. Am. A (1)

J. Phys. Chem. B (1)

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the Second-Order Hyperpolarizability of the Collagen Triple Helix and Determination of Its Physical Origin,” J. Phys. Chem. B 113(40), 13437–13445 (2009).
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J. Speech Lang. Hear. Res. (1)

J. M. Coppoolse, T. G. Van Kooten, H. K. Heris, L. Mongeau, N. Y. Li, S. L. Thibeault, J. Pitaro, O. Akinpelu, and S. J. Daniel, “An in vivo study of composite microgels based on hyaluronic acid and gelatin for the reconstruction of surgically injured rat vocal folds,” J. Speech Lang. Hear. Res. 57(2), S658–S673 (2014).
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J. Voice (4)

S. Krischke, S. Weigelt, U. Hoppe, V. Köllner, M. Klotz, U. Eysholdt, and F. Rosanowski, “Quality of life in dysphonic patients,” J. Voice 19(1), 132–137 (2005).
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J. K. Hansen and S. L. Thibeault, “Current understanding and review of the literature: vocal fold scarring,” J. Voice 20(1), 110–120 (2006).
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W. Chen, P. Woo, and T. Murry, “Vocal Fold Vibration Following Surgical Intervention in Three Vocal Pathologies: A Preliminary Study,” J. Voice 31(5), 610–614 (2017).
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B. Rousseau, S. Hirano, R. W. Chan, N. V. Welham, S. L. Thibeault, C. N. Ford, and D. M. Bless, “Characterization of chronic vocal fold scarring in a rabbit model,” J. Voice 18(1), 116–124 (2004).
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Laryngoscope (2)

A. K. Miri, U. Tripathy, L. Mongeau, and P. W. Wiseman, “Nonlinear laser scanning microscopy of human vocal folds,” Laryngoscope 122(2), 356–363 (2012).
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A. Suehiro, J. M. Bock, J. E. Hall, C. G. Garrett, and B. Rousseau, “Feasibility and acute healing of vocal fold microflap incisions in a rabbit model,” Laryngoscope 122(3), 600–605 (2012).
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Mater. Today (1)

P. J. Withers, “X-ray nanotomography,” Mater. Today 10(12), 26–34 (2007).
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Nat. Biotechnol. (1)

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
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Nat. Methods (1)

C. Pan, R. Cai, F. P. Quacquarelli, A. Ghasemigharagoz, A. Lourbopoulos, P. Matryba, N. Plesnila, M. Dichgans, F. Hellal, and A. Ertürk, “Shrinkage-mediated imaging of entire organs and organisms using uDISCO,” Nat. Methods 13(10), 859–867 (2016).
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Nat. Protoc. (1)

R. Tomer, L. Ye, B. Hsueh, and K. Deisseroth, “Advanced CLARITY for rapid and high-resolution imaging of intact tissues,” Nat. Protoc. 9(7), 1682–1697 (2014).
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Opt. Commun. (1)

P. P. Mondal and A. Diaspro, “Lateral resolution improvement in two-photon excitation microscopy by aperture engineering,” Opt. Commun. 281(7), 1855–1859 (2008).
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M. S. Benninger, D. Alessi, S. Archer, R. Bastian, C. Ford, J. Koufman, R. T. Sataloff, J. R. Spiegel, and P. Woo, “Vocal fold scarring: current concepts and management,” Otolaryngol. Head Neck Surg. 115(5), 474–482 (1996).
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Pathobiology (1)

M. Senter-Zapata, K. Patel, P. A. Bautista, M. Griffin, J. Michaelson, and Y. Yagi, “The role of micro-CT in 3D histology imaging,” Pathobiology 83(2-3), 140–147 (2016).
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PLoS One (1)

F. Cella Zanacchi, Z. Lavagnino, M. Faretta, L. Furia, and A. Diaspro, “Light-Sheet Confined Super-Resolution Using Two-Photon Photoactivation,” PLoS One 8(7), e67667 (2013).
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Proc. Natl. Acad. Sci. U.S.A. (2)

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
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Science (1)

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Figures (8)

Fig. 1
Fig. 1 Schematic comparison of the concepts of conventional histology (A) with virtual histology by nanotomography and nonlinear microscopy (B).
Fig. 2
Fig. 2 Optical clearing of rabbit vocal folds. (A) Uncleared vocal fold tissue after dissection, (B) the same tissue after clearing with the uDISCO protocol, (C) render of imaging chamber used for nonlinear microscopy of the cleared tissue, inset showing brightfield microscopy image of the sample and chamber. Dotted lines in (A) and (B) are spaced 1mm apart.
Fig. 3
Fig. 3 A schematic diagram of the nonlinear microscopy imaging system. The Verdi (532 nm) laser pumps the Ti:Sapphire laser (780 nm) that is directed into the microscope base with computer control over the power. A 25X 1.05NA water immersion objective is used to focus the excitation light onto the sample. Forward detection was achieved using a condenser lens, where the emission was separated into two channels: the second harmonic generation channel (Channel 1) and the two-photon fluorescence channel (Channel 2) and subsequently detected by photomultipliers (PMTs).
Fig. 4
Fig. 4 Coarse tomography of a rabbit larynx. (A) 3D volume render of the entire rabbit larynx. (B) Cross sectional plane across the rabbit larynx. Scale bars are 1 mm.
Fig. 5
Fig. 5 Comparison of histology methods applied to rabbit vocal folds. (A) Virtual histology by Nano-CT. (B) Classical histology example by hematoxylin and eosin staining of a thin tissue slice of rabbit larynx. White arrow indicates the vocal fold lamina propria, yellow arrow points to muscle while the magenta arrow denotes an area of cartilage. Scale bars are 1 mm.
Fig. 6
Fig. 6 3D volume render of dissected rabbit vocal folds imaged by nonlinear microscopy and nanotomography (coarse). (A) Channel 1: Second Harmonic Generation highlighting collagen type I & III fibers. Green arrow highlights structural laryngeal cartilage. (B) Channel 2: Two Photon Autofluorescence showing primarily muscle cell NADH (magenta arrow) and blood vessel (yellow arrow). (C) Composite of (A) and (B). (D) Coarse nanotomography of the same dissected rabbit larynx performed after nonlinear microscopy. (A-C) are at the same scale. Scale bars are 1 mm.
Fig. 7
Fig. 7 High resolution nanotomography of rabbit vocal fold tissue and the surrounding area. (A) 3D volume render of the epithelium (highlighted by white arrow), vocal fold lamina propria, and surrounding muscle. (B) Cross section of cartilage and muscle (highlighted by white arrow) in the surrounding tissue of the vocal fold. (C) Vocal fold lamina propria (white arrow) cross section. Scale bars are 100 µm.
Fig. 8
Fig. 8 High resolution nonlinear microscopy of optically cleared rabbit vocal fold and surrounding tissue. (A) 3D Volume render combining SHG (magenta) and TPAF (green), yellow arrow highlights the presence of red blood cells via autofluorescence from hemoglobin. (B-D) Imaged area including structural collagen (green arrow in SHG channel B), vocal fold lamina propria (magenta arrow in TPAF channel C), and surrounding muscle fibers (white arrow in composite D). (E-G) Imaged area showing surrounding cartilage, where E is the SHG channel, F is the TPAF channel highlighting chondrocytes (magenta arrow), and composite G shows presence of elastic fibers (white arrow). Scale bars are 25 µm.

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