Abstract

High tensile strength and optical clarity are unique properties of the cornea. These features are dictated by the three-dimensional architecture of corneal lamellae. Therefore, understanding the microscopic details of the cornea’s structural organization may contribute to the development of artificial cornea for the treatment of corneal diseases. In this study, the combination of forward second harmonic generation (SHG) microcopy and fast Fourier-transform based image analysis was used to characterize the depth-dependent superstructure of chicken corneal stroma. Our results show that from the surface, adjacent lamellae of anterior chicken cornea lamella rotate in a counterclockwise direction, and the same rotational helicity is observed in left and right corneas. Furthermore, the overall average rotational pitch of lamellae is 0.92 ± 0.11 degree/µm which persists for 176 ± 14 µm in the anterior stroma. As depth further increased, the rate of lamellar rotation decreases. Upon reaching posterior stroma, lamellar orientation remains constant. Throughout the stroma, collagen lamellae in chicken rotate a total of 169 ± 21 degrees. The lack of lamellar rotation in posterior stroma suggests that packing efficiency cannot be used to explain the helicity of depth-dependent rotation of anterior stroma. In addition, although the right cornea has a higher rotational pitch (0.95 ± 11 vs 0.90 ± 10 degrees/µm) and thinner anterior stroma (173 ± 13 vs 179 ± 14 µm) than the left cornea, the two effects cancel each other out and result in similar total angular rotation of anterior stroma (161 ± 23 and 165 degrees ± 21). Finally, our observation of a total angular rotation of 169 ± 21 degrees shows that within experimental error, chicken cornea lamellae rotate around 180 degrees or half of a complete turn. Additional studies are needed to arrive at an explanation of chicken superstructure in three dimensions.

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

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References

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  7. M. D. Twa and M. J. Giese, “Assessment of corneal thickness and keratocyte density in a rabbit model of laser in situ keratomileusis using scanning laser confocal microscopy,” Am. J. Ophthalmol. 152(6), 941–953.e1 (2011).
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    [Crossref]
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    [Crossref]
  25. N. Morishige, W. M. Petroll, T. Nishida, M. C. Kenney, and J. V. Jester, “Noninvasive corneal stromal collagen imaging using two-photon-generated second-harmonic signals,” J. Cataract Refractive Surg. 32(11), 1784–1791 (2006).
    [Crossref]
  26. P. Matteini, F. Ratto, F. Rossi, R. Cicchi, C. Stringari, D. Kapsokalyvas, F. S. Pavone, and R. Pini, “Photothermally-induced disordered patterns of corneal collagen revealed by SHG imaging,” Opt. Express 17(6), 4868–4878 (2009).
    [Crossref]
  27. N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
    [Crossref]
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    [Crossref]
  30. C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
    [Crossref]
  31. R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
    [Crossref]
  32. J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
    [Crossref]
  33. M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
    [Crossref]
  34. K. M. Meek and C. Knupp, “Corneal structure and transparency,” Prog. Retinal Eye Res. 49, 1–16 (2015).
    [Crossref]
  35. T. Y. Lau, R. Ambekar, and K. C. Toussaint, “Quantification of collagen fiber organization using three-dimensional Fourier transform-second-harmonic generation imaging,” Opt. Express 20(19), 21821–21832 (2012).
    [Crossref]
  36. R. A. R. Rao, M. R. Mehta, and K. C. Toussaint, “Fourier transform-second-harmonic generation imaging of biological tissues,” Opt. Express 17(17), 14534–14542 (2009).
    [Crossref]
  37. J. M. Bueno, R. Palacios, M. K. Chessey, and H. Ginis, “Analysis of spatial lamellar distribution from adaptive-optics second harmonic generation corneal images,” Biomed. Opt. Express 4(7), 1006–1013 (2013).
    [Crossref]

2019 (1)

J. M. Bueno, F. J. Avila, and M. C. Martinez-Garcia, “Quantitative Analysis of the Corneal Collagen Distribution after In Vivo Cross-Linking with Second Harmonic Microscopy,” BioMed Res. Int. 2019, 1–12 (2019).
[Crossref]

2017 (2)

S. L. Lee, Y. F. Chen, and C. Y. Dong, “Probing Multiscale Collagenous Tissue by Nonlinear Microscopy,” ACS Biomater. Sci. Eng. 3(11), 2825–2831 (2017).
[Crossref]

R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
[Crossref]

2016 (1)

A. Benoit, G. Latour, S.-K. Marie-Claire, and J.-M. Allain, “Simultaneous microstructural and mechanical characterization of human corneas at increasing pressure,” J. Mech. Behav. Biomed. Mater. 60, 93–105 (2016).
[Crossref]

2015 (4)

M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
[Crossref]

K. M. Meek and C. Knupp, “Corneal structure and transparency,” Prog. Retinal Eye Res. 49, 1–16 (2015).
[Crossref]

A. J. Quantock, M. Winkler, G. J. Parfitt, R. D. Young, D. J. Brown, C. Boote, and J. V. Jester, “From nano to macro: Studying the hierarchical structure of the corneal extracellular matrix,” Exp. Eye Res. 133, 81–99 (2015).
[Crossref]

S. Chen, M. J. Mienaltowski, and D. E. Birk, “Regulation of corneal stroma extracellular matrix assembly,” Exp. Eye Res. 133, 69–80 (2015).
[Crossref]

2014 (1)

N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
[Crossref]

2013 (2)

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
[Crossref]

J. M. Bueno, R. Palacios, M. K. Chessey, and H. Ginis, “Analysis of spatial lamellar distribution from adaptive-optics second harmonic generation corneal images,” Biomed. Opt. Express 4(7), 1006–1013 (2013).
[Crossref]

2012 (5)

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

T. Y. Lau, R. Ambekar, and K. C. Toussaint, “Quantification of collagen fiber organization using three-dimensional Fourier transform-second-harmonic generation imaging,” Opt. Express 20(19), 21821–21832 (2012).
[Crossref]

S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
[Crossref]

W. L. Chen, P. S. Hu, A. Ghazaryan, S. J. Chen, T. H. Tsai, and C. Y. Dong, “Quantitative analysis of multiphoton excitation autofluorescence and second harmonic generation imaging for medical diagnosis,” Computerized Medical Imaging and Graphics 36(7), 519–526 (2012).
[Crossref]

W. Lo, W. L. Chen, C. M. Hsueh, A. A. Ghazaryan, S. J. Chen, D. H. Ma, C. Y. Dong, and H. Y. Tan, “Fast Fourier transform-based analysis of second-harmonic generation image in keratoconic cornea,” Invest. Ophthalmol. Visual Sci. 53(7), 3501–3507 (2012).
[Crossref]

2011 (3)

N. Morishige, Y. Takagi, T. Chikama, A. Takahara, and T. Nishida, “Three-dimensional analysis of collagen lamellae in the anterior stroma of the human cornea visualized by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 52(2), 911–915 (2011).
[Crossref]

M. D. Twa and M. J. Giese, “Assessment of corneal thickness and keratocyte density in a rabbit model of laser in situ keratomileusis using scanning laser confocal microscopy,” Am. J. Ophthalmol. 152(6), 941–953.e1 (2011).
[Crossref]

J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
[Crossref]

2010 (1)

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
[Crossref]

2009 (4)

K. M. Meek and C. Boote, “The use of X-ray scattering techniques to quantify the orientation and distribution of collagen in the corneal stroma,” Prog. Retinal Eye Res. 28(5), 369–392 (2009).
[Crossref]

C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
[Crossref]

R. A. R. Rao, M. R. Mehta, and K. C. Toussaint, “Fourier transform-second-harmonic generation imaging of biological tissues,” Opt. Express 17(17), 14534–14542 (2009).
[Crossref]

P. Matteini, F. Ratto, F. Rossi, R. Cicchi, C. Stringari, D. Kapsokalyvas, F. S. Pavone, and R. Pini, “Photothermally-induced disordered patterns of corneal collagen revealed by SHG imaging,” Opt. Express 17(6), 4868–4878 (2009).
[Crossref]

2008 (1)

J. V. Jester, “Corneal crystallins and the development of cellular transparency,” Semin. Cell Dev. Biol. 19(2), 82–93 (2008).
[Crossref]

2007 (3)

S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
[Crossref]

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
[Crossref]

N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Visual Sci. 48(3), 1087–1094 (2007).
[Crossref]

2006 (1)

N. Morishige, W. M. Petroll, T. Nishida, M. C. Kenney, and J. V. Jester, “Noninvasive corneal stromal collagen imaging using two-photon-generated second-harmonic signals,” J. Cataract Refractive Surg. 32(11), 1784–1791 (2006).
[Crossref]

2005 (1)

J. P. Bergmanson, J. Horne, M. J. Doughty, M. Garcia, and M. Gondo, “Assessment of the number of lamellae in the central region of the normal human corneal stroma at the resolution of the transmission electron microscope,” Eye Contact Lens 31(6), 281–287 (2005).
[Crossref]

2004 (1)

K. M. Meek and C. Boote, “The organization of collagen in the corneal stroma,” Exp. Eye Res. 78(3), 503–512 (2004).
[Crossref]

2003 (2)

K. M. Meek, D. W. Leonard, C. J. Connon, S. Dennis, and S. Khan, “Transparency, swelling and scarring in the corneal stroma,” Eye 17(8), 927–936 (2003).
[Crossref]

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref]

2002 (1)

K. K. Svoboda and W. R. Reenstra, “Approaches to studying cellular signaling: a primer for morphologists,” Anat. Rec. 269(2), 123–139 (2002).
[Crossref]

1999 (1)

R. P. Copt, R. Thomas, and A. Mermoud, “Corneal thickness in ocular hypertension, primary open-angle glaucoma, and normal tension glaucoma,” Arch. Ophthalmol. 117(1), 14–16 (1999).
[Crossref]

1995 (1)

J. V. Jester, W. M. Petroll, P. A. Barry, and H. D. Cavanagh, “Expression of alpha-smooth muscle (alpha-SM) actin during corneal stromal wound healing,” Invest. Ophthalmol. Visual Sci. 36(5), 809–819 (1995).

1971 (1)

R. L. Trelstad and A. J. Coulombre, “Morphogenesis of the collagenous stroma in the chick cornea,” J. Cell Biol. 50(3), 840–858 (1971).
[Crossref]

Abahussin, M.

S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
[Crossref]

Akens, M. K.

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

Allain, J.-M.

A. Benoit, G. Latour, S.-K. Marie-Claire, and J.-M. Allain, “Simultaneous microstructural and mechanical characterization of human corneas at increasing pressure,” J. Mech. Behav. Biomed. Mater. 60, 93–105 (2016).
[Crossref]

Ambekar, R.

Artal, P.

J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
[Crossref]

Avila, F. J.

J. M. Bueno, F. J. Avila, and M. C. Martinez-Garcia, “Quantitative Analysis of the Corneal Collagen Distribution after In Vivo Cross-Linking with Second Harmonic Microscopy,” BioMed Res. Int. 2019, 1–12 (2019).
[Crossref]

Azumi, H.

N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
[Crossref]

Barry, P. A.

J. V. Jester, W. M. Petroll, P. A. Barry, and H. D. Cavanagh, “Expression of alpha-smooth muscle (alpha-SM) actin during corneal stromal wound healing,” Invest. Ophthalmol. Visual Sci. 36(5), 809–819 (1995).

Barzda, V.

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

Benoit, A.

A. Benoit, G. Latour, S.-K. Marie-Claire, and J.-M. Allain, “Simultaneous microstructural and mechanical characterization of human corneas at increasing pressure,” J. Mech. Behav. Biomed. Mater. 60, 93–105 (2016).
[Crossref]

Bergmanson, J. P.

J. P. Bergmanson, J. Horne, M. J. Doughty, M. Garcia, and M. Gondo, “Assessment of the number of lamellae in the central region of the normal human corneal stroma at the resolution of the transmission electron microscope,” Eye Contact Lens 31(6), 281–287 (2005).
[Crossref]

Birk, D. E.

S. Chen, M. J. Mienaltowski, and D. E. Birk, “Regulation of corneal stroma extracellular matrix assembly,” Exp. Eye Res. 133, 69–80 (2015).
[Crossref]

Boote, C.

A. J. Quantock, M. Winkler, G. J. Parfitt, R. D. Young, D. J. Brown, C. Boote, and J. V. Jester, “From nano to macro: Studying the hierarchical structure of the corneal extracellular matrix,” Exp. Eye Res. 133, 81–99 (2015).
[Crossref]

K. M. Meek and C. Boote, “The use of X-ray scattering techniques to quantify the orientation and distribution of collagen in the corneal stroma,” Prog. Retinal Eye Res. 28(5), 369–392 (2009).
[Crossref]

S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
[Crossref]

K. M. Meek and C. Boote, “The organization of collagen in the corneal stroma,” Exp. Eye Res. 78(3), 503–512 (2004).
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Brown, D. J.

A. J. Quantock, M. Winkler, G. J. Parfitt, R. D. Young, D. J. Brown, C. Boote, and J. V. Jester, “From nano to macro: Studying the hierarchical structure of the corneal extracellular matrix,” Exp. Eye Res. 133, 81–99 (2015).
[Crossref]

M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
[Crossref]

N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Visual Sci. 48(3), 1087–1094 (2007).
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Bueno, J. M.

J. M. Bueno, F. J. Avila, and M. C. Martinez-Garcia, “Quantitative Analysis of the Corneal Collagen Distribution after In Vivo Cross-Linking with Second Harmonic Microscopy,” BioMed Res. Int. 2019, 1–12 (2019).
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J. M. Bueno, R. Palacios, M. K. Chessey, and H. Ginis, “Analysis of spatial lamellar distribution from adaptive-optics second harmonic generation corneal images,” Biomed. Opt. Express 4(7), 1006–1013 (2013).
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J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
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S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
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Cavanagh, H. D.

J. V. Jester, W. M. Petroll, P. A. Barry, and H. D. Cavanagh, “Expression of alpha-smooth muscle (alpha-SM) actin during corneal stromal wound healing,” Invest. Ophthalmol. Visual Sci. 36(5), 809–819 (1995).

Chang, Y. L.

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
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Chen, H. C.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
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Chen, S.

S. Chen, M. J. Mienaltowski, and D. E. Birk, “Regulation of corneal stroma extracellular matrix assembly,” Exp. Eye Res. 133, 69–80 (2015).
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Chen, S. J.

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
[Crossref]

W. Lo, W. L. Chen, C. M. Hsueh, A. A. Ghazaryan, S. J. Chen, D. H. Ma, C. Y. Dong, and H. Y. Tan, “Fast Fourier transform-based analysis of second-harmonic generation image in keratoconic cornea,” Invest. Ophthalmol. Visual Sci. 53(7), 3501–3507 (2012).
[Crossref]

W. L. Chen, P. S. Hu, A. Ghazaryan, S. J. Chen, T. H. Tsai, and C. Y. Dong, “Quantitative analysis of multiphoton excitation autofluorescence and second harmonic generation imaging for medical diagnosis,” Computerized Medical Imaging and Graphics 36(7), 519–526 (2012).
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Chen, W. L.

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
[Crossref]

W. Lo, W. L. Chen, C. M. Hsueh, A. A. Ghazaryan, S. J. Chen, D. H. Ma, C. Y. Dong, and H. Y. Tan, “Fast Fourier transform-based analysis of second-harmonic generation image in keratoconic cornea,” Invest. Ophthalmol. Visual Sci. 53(7), 3501–3507 (2012).
[Crossref]

W. L. Chen, P. S. Hu, A. Ghazaryan, S. J. Chen, T. H. Tsai, and C. Y. Dong, “Quantitative analysis of multiphoton excitation autofluorescence and second harmonic generation imaging for medical diagnosis,” Computerized Medical Imaging and Graphics 36(7), 519–526 (2012).
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T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
[Crossref]

C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
[Crossref]

Chen, Y. F.

S. L. Lee, Y. F. Chen, and C. Y. Dong, “Probing Multiscale Collagenous Tissue by Nonlinear Microscopy,” ACS Biomater. Sci. Eng. 3(11), 2825–2831 (2017).
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T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
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H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
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Chessey, M. K.

Chikama, T.

N. Morishige, Y. Takagi, T. Chikama, A. Takahara, and T. Nishida, “Three-dimensional analysis of collagen lamellae in the anterior stroma of the human cornea visualized by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 52(2), 911–915 (2011).
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N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Visual Sci. 48(3), 1087–1094 (2007).
[Crossref]

Chiou, L. L.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
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Cicchi, R.

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P. Matteini, F. Ratto, F. Rossi, R. Cicchi, C. Stringari, D. Kapsokalyvas, F. S. Pavone, and R. Pini, “Photothermally-induced disordered patterns of corneal collagen revealed by SHG imaging,” Opt. Express 17(6), 4868–4878 (2009).
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K. M. Meek, D. W. Leonard, C. J. Connon, S. Dennis, and S. Khan, “Transparency, swelling and scarring in the corneal stroma,” Eye 17(8), 927–936 (2003).
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R. P. Copt, R. Thomas, and A. Mermoud, “Corneal thickness in ocular hypertension, primary open-angle glaucoma, and normal tension glaucoma,” Arch. Ophthalmol. 117(1), 14–16 (1999).
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Coulombre, A. J.

R. L. Trelstad and A. J. Coulombre, “Morphogenesis of the collagenous stroma in the chick cornea,” J. Cell Biol. 50(3), 840–858 (1971).
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Cox, G.

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref]

Dennis, S.

K. M. Meek, D. W. Leonard, C. J. Connon, S. Dennis, and S. Khan, “Transparency, swelling and scarring in the corneal stroma,” Eye 17(8), 927–936 (2003).
[Crossref]

Dong, C. Y.

S. L. Lee, Y. F. Chen, and C. Y. Dong, “Probing Multiscale Collagenous Tissue by Nonlinear Microscopy,” ACS Biomater. Sci. Eng. 3(11), 2825–2831 (2017).
[Crossref]

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
[Crossref]

W. L. Chen, P. S. Hu, A. Ghazaryan, S. J. Chen, T. H. Tsai, and C. Y. Dong, “Quantitative analysis of multiphoton excitation autofluorescence and second harmonic generation imaging for medical diagnosis,” Computerized Medical Imaging and Graphics 36(7), 519–526 (2012).
[Crossref]

W. Lo, W. L. Chen, C. M. Hsueh, A. A. Ghazaryan, S. J. Chen, D. H. Ma, C. Y. Dong, and H. Y. Tan, “Fast Fourier transform-based analysis of second-harmonic generation image in keratoconic cornea,” Invest. Ophthalmol. Visual Sci. 53(7), 3501–3507 (2012).
[Crossref]

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
[Crossref]

C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
[Crossref]

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
[Crossref]

Doughty, M. J.

J. P. Bergmanson, J. Horne, M. J. Doughty, M. Garcia, and M. Gondo, “Assessment of the number of lamellae in the central region of the normal human corneal stroma at the resolution of the transmission electron microscope,” Eye Contact Lens 31(6), 281–287 (2005).
[Crossref]

Elson, E. L.

S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
[Crossref]

Fraser, I.

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref]

Garcia, M.

J. P. Bergmanson, J. Horne, M. J. Doughty, M. Garcia, and M. Gondo, “Assessment of the number of lamellae in the central region of the normal human corneal stroma at the resolution of the transmission electron microscope,” Eye Contact Lens 31(6), 281–287 (2005).
[Crossref]

Genin, G. M.

S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
[Crossref]

Ghazaryan, A.

W. L. Chen, P. S. Hu, A. Ghazaryan, S. J. Chen, T. H. Tsai, and C. Y. Dong, “Quantitative analysis of multiphoton excitation autofluorescence and second harmonic generation imaging for medical diagnosis,” Computerized Medical Imaging and Graphics 36(7), 519–526 (2012).
[Crossref]

Ghazaryan, A. A.

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
[Crossref]

W. Lo, W. L. Chen, C. M. Hsueh, A. A. Ghazaryan, S. J. Chen, D. H. Ma, C. Y. Dong, and H. Y. Tan, “Fast Fourier transform-based analysis of second-harmonic generation image in keratoconic cornea,” Invest. Ophthalmol. Visual Sci. 53(7), 3501–3507 (2012).
[Crossref]

Giese, M. J.

M. D. Twa and M. J. Giese, “Assessment of corneal thickness and keratocyte density in a rabbit model of laser in situ keratomileusis using scanning laser confocal microscopy,” Am. J. Ophthalmol. 152(6), 941–953.e1 (2011).
[Crossref]

Ginis, H.

Gondo, M.

J. P. Bergmanson, J. Horne, M. J. Doughty, M. Garcia, and M. Gondo, “Assessment of the number of lamellae in the central region of the normal human corneal stroma at the resolution of the transmission electron microscope,” Eye Contact Lens 31(6), 281–287 (2005).
[Crossref]

Gorrell, M. D.

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref]

Gualda, E. J.

J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
[Crossref]

Hayes, S.

S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
[Crossref]

Horne, J.

J. P. Bergmanson, J. Horne, M. J. Doughty, M. Garcia, and M. Gondo, “Assessment of the number of lamellae in the central region of the normal human corneal stroma at the resolution of the transmission electron microscope,” Eye Contact Lens 31(6), 281–287 (2005).
[Crossref]

Hovhannisyan, V.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
[Crossref]

Hovhannisyan, V. A.

C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
[Crossref]

Hsiao, C. H.

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
[Crossref]

Hsueh, C. M.

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
[Crossref]

W. Lo, W. L. Chen, C. M. Hsueh, A. A. Ghazaryan, S. J. Chen, D. H. Ma, C. Y. Dong, and H. Y. Tan, “Fast Fourier transform-based analysis of second-harmonic generation image in keratoconic cornea,” Invest. Ophthalmol. Visual Sci. 53(7), 3501–3507 (2012).
[Crossref]

C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
[Crossref]

Hu, P. S.

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
[Crossref]

W. L. Chen, P. S. Hu, A. Ghazaryan, S. J. Chen, T. H. Tsai, and C. Y. Dong, “Quantitative analysis of multiphoton excitation autofluorescence and second harmonic generation imaging for medical diagnosis,” Computerized Medical Imaging and Graphics 36(7), 519–526 (2012).
[Crossref]

Huang, G. T.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
[Crossref]

Huang, S. C.

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
[Crossref]

Jee, S. H.

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
[Crossref]

Jeng, Y. M.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
[Crossref]

Jester, J. V.

A. J. Quantock, M. Winkler, G. J. Parfitt, R. D. Young, D. J. Brown, C. Boote, and J. V. Jester, “From nano to macro: Studying the hierarchical structure of the corneal extracellular matrix,” Exp. Eye Res. 133, 81–99 (2015).
[Crossref]

M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
[Crossref]

J. V. Jester, “Corneal crystallins and the development of cellular transparency,” Semin. Cell Dev. Biol. 19(2), 82–93 (2008).
[Crossref]

N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Visual Sci. 48(3), 1087–1094 (2007).
[Crossref]

N. Morishige, W. M. Petroll, T. Nishida, M. C. Kenney, and J. V. Jester, “Noninvasive corneal stromal collagen imaging using two-photon-generated second-harmonic signals,” J. Cataract Refractive Surg. 32(11), 1784–1791 (2006).
[Crossref]

J. V. Jester, W. M. Petroll, P. A. Barry, and H. D. Cavanagh, “Expression of alpha-smooth muscle (alpha-SM) actin during corneal stromal wound healing,” Invest. Ophthalmol. Visual Sci. 36(5), 809–819 (1995).

Jones, A.

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref]

Kable, E.

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref]

Kapsokalyvas, D.

Kawamoto, K.

N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Visual Sci. 48(3), 1087–1094 (2007).
[Crossref]

Kenney, M. C.

N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Visual Sci. 48(3), 1087–1094 (2007).
[Crossref]

N. Morishige, W. M. Petroll, T. Nishida, M. C. Kenney, and J. V. Jester, “Noninvasive corneal stromal collagen imaging using two-photon-generated second-harmonic signals,” J. Cataract Refractive Surg. 32(11), 1784–1791 (2006).
[Crossref]

Khan, S.

K. M. Meek, D. W. Leonard, C. J. Connon, S. Dennis, and S. Khan, “Transparency, swelling and scarring in the corneal stroma,” Eye 17(8), 927–936 (2003).
[Crossref]

Kim, K. H.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
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Kimura, K.

N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
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K. M. Meek and C. Knupp, “Corneal structure and transparency,” Prog. Retinal Eye Res. 49, 1–16 (2015).
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A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
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Latour, G.

A. Benoit, G. Latour, S.-K. Marie-Claire, and J.-M. Allain, “Simultaneous microstructural and mechanical characterization of human corneas at increasing pressure,” J. Mech. Behav. Biomed. Mater. 60, 93–105 (2016).
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Lee, H. S.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
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S. L. Lee, Y. F. Chen, and C. Y. Dong, “Probing Multiscale Collagenous Tissue by Nonlinear Microscopy,” ACS Biomater. Sci. Eng. 3(11), 2825–2831 (2017).
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S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
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Leonard, D. W.

K. M. Meek, D. W. Leonard, C. J. Connon, S. Dennis, and S. Khan, “Transparency, swelling and scarring in the corneal stroma,” Eye 17(8), 927–936 (2003).
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S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
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H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
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H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
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Lin, W. C.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
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H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
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Liu, G. Y.

C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
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T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
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H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
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W. Lo, W. L. Chen, C. M. Hsueh, A. A. Ghazaryan, S. J. Chen, D. H. Ma, C. Y. Dong, and H. Y. Tan, “Fast Fourier transform-based analysis of second-harmonic generation image in keratoconic cornea,” Invest. Ophthalmol. Visual Sci. 53(7), 3501–3507 (2012).
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C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
[Crossref]

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
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Ma, D. H.

W. Lo, W. L. Chen, C. M. Hsueh, A. A. Ghazaryan, S. J. Chen, D. H. Ma, C. Y. Dong, and H. Y. Tan, “Fast Fourier transform-based analysis of second-harmonic generation image in keratoconic cornea,” Invest. Ophthalmol. Visual Sci. 53(7), 3501–3507 (2012).
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H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
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R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
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A. Benoit, G. Latour, S.-K. Marie-Claire, and J.-M. Allain, “Simultaneous microstructural and mechanical characterization of human corneas at increasing pressure,” J. Mech. Behav. Biomed. Mater. 60, 93–105 (2016).
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J. M. Bueno, F. J. Avila, and M. C. Martinez-Garcia, “Quantitative Analysis of the Corneal Collagen Distribution after In Vivo Cross-Linking with Second Harmonic Microscopy,” BioMed Res. Int. 2019, 1–12 (2019).
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S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
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K. M. Meek and C. Knupp, “Corneal structure and transparency,” Prog. Retinal Eye Res. 49, 1–16 (2015).
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K. M. Meek and C. Boote, “The use of X-ray scattering techniques to quantify the orientation and distribution of collagen in the corneal stroma,” Prog. Retinal Eye Res. 28(5), 369–392 (2009).
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S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
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K. M. Meek and C. Boote, “The organization of collagen in the corneal stroma,” Exp. Eye Res. 78(3), 503–512 (2004).
[Crossref]

K. M. Meek, D. W. Leonard, C. J. Connon, S. Dennis, and S. Khan, “Transparency, swelling and scarring in the corneal stroma,” Eye 17(8), 927–936 (2003).
[Crossref]

Mehta, M. R.

Menabuoni, L.

R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
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R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
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N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
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N. Morishige, Y. Takagi, T. Chikama, A. Takahara, and T. Nishida, “Three-dimensional analysis of collagen lamellae in the anterior stroma of the human cornea visualized by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 52(2), 911–915 (2011).
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N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Visual Sci. 48(3), 1087–1094 (2007).
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N. Morishige, W. M. Petroll, T. Nishida, M. C. Kenney, and J. V. Jester, “Noninvasive corneal stromal collagen imaging using two-photon-generated second-harmonic signals,” J. Cataract Refractive Surg. 32(11), 1784–1791 (2006).
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N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
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M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
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S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
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R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
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N. Morishige, Y. Takagi, T. Chikama, A. Takahara, and T. Nishida, “Three-dimensional analysis of collagen lamellae in the anterior stroma of the human cornea visualized by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 52(2), 911–915 (2011).
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N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Visual Sci. 48(3), 1087–1094 (2007).
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N. Morishige, W. M. Petroll, T. Nishida, M. C. Kenney, and J. V. Jester, “Noninvasive corneal stromal collagen imaging using two-photon-generated second-harmonic signals,” J. Cataract Refractive Surg. 32(11), 1784–1791 (2006).
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N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
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Parfitt, G. J.

A. J. Quantock, M. Winkler, G. J. Parfitt, R. D. Young, D. J. Brown, C. Boote, and J. V. Jester, “From nano to macro: Studying the hierarchical structure of the corneal extracellular matrix,” Exp. Eye Res. 133, 81–99 (2015).
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Pavone, F. S.

R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
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P. Matteini, F. Ratto, F. Rossi, R. Cicchi, C. Stringari, D. Kapsokalyvas, F. S. Pavone, and R. Pini, “Photothermally-induced disordered patterns of corneal collagen revealed by SHG imaging,” Opt. Express 17(6), 4868–4878 (2009).
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N. Morishige, W. M. Petroll, T. Nishida, M. C. Kenney, and J. V. Jester, “Noninvasive corneal stromal collagen imaging using two-photon-generated second-harmonic signals,” J. Cataract Refractive Surg. 32(11), 1784–1791 (2006).
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J. V. Jester, W. M. Petroll, P. A. Barry, and H. D. Cavanagh, “Expression of alpha-smooth muscle (alpha-SM) actin during corneal stromal wound healing,” Invest. Ophthalmol. Visual Sci. 36(5), 809–819 (1995).

Pini, R.

R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
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P. Matteini, F. Ratto, F. Rossi, R. Cicchi, C. Stringari, D. Kapsokalyvas, F. S. Pavone, and R. Pini, “Photothermally-induced disordered patterns of corneal collagen revealed by SHG imaging,” Opt. Express 17(6), 4868–4878 (2009).
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Pless, R. B.

S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
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Pryse, K. M.

S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
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Purslow, C.

S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
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Quantock, A. J.

A. J. Quantock, M. Winkler, G. J. Parfitt, R. D. Young, D. J. Brown, C. Boote, and J. V. Jester, “From nano to macro: Studying the hierarchical structure of the corneal extracellular matrix,” Exp. Eye Res. 133, 81–99 (2015).
[Crossref]

S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
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Raghunathan, V. K.

M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
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Rao, R. A. R.

Ratto, F.

R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
[Crossref]

P. Matteini, F. Ratto, F. Rossi, R. Cicchi, C. Stringari, D. Kapsokalyvas, F. S. Pavone, and R. Pini, “Photothermally-induced disordered patterns of corneal collagen revealed by SHG imaging,” Opt. Express 17(6), 4868–4878 (2009).
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K. K. Svoboda and W. R. Reenstra, “Approaches to studying cellular signaling: a primer for morphologists,” Anat. Rec. 269(2), 123–139 (2002).
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Rossi, F.

R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
[Crossref]

P. Matteini, F. Ratto, F. Rossi, R. Cicchi, C. Stringari, D. Kapsokalyvas, F. S. Pavone, and R. Pini, “Photothermally-induced disordered patterns of corneal collagen revealed by SHG imaging,” Opt. Express 17(6), 4868–4878 (2009).
[Crossref]

Sandkuijl, D.

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
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Schaefer, P. M.

S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
[Crossref]

Sheppard, J.

S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
[Crossref]

Shin-Gyou-Uchi, R.

N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
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Shoa, G.

M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
[Crossref]

So, P. T.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
[Crossref]

Sonoda, K. H.

N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
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Stringari, C.

Sun, T. L.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
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Sun, Y.

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
[Crossref]

Sung, M. C.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
[Crossref]

Svoboda, K. K.

K. K. Svoboda and W. R. Reenstra, “Approaches to studying cellular signaling: a primer for morphologists,” Anat. Rec. 269(2), 123–139 (2002).
[Crossref]

Takagi, Y.

N. Morishige, Y. Takagi, T. Chikama, A. Takahara, and T. Nishida, “Three-dimensional analysis of collagen lamellae in the anterior stroma of the human cornea visualized by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 52(2), 911–915 (2011).
[Crossref]

Takahara, A.

N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
[Crossref]

N. Morishige, Y. Takagi, T. Chikama, A. Takahara, and T. Nishida, “Three-dimensional analysis of collagen lamellae in the anterior stroma of the human cornea visualized by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 52(2), 911–915 (2011).
[Crossref]

Tan, H. Y.

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
[Crossref]

W. Lo, W. L. Chen, C. M. Hsueh, A. A. Ghazaryan, S. J. Chen, D. H. Ma, C. Y. Dong, and H. Y. Tan, “Fast Fourier transform-based analysis of second-harmonic generation image in keratoconic cornea,” Invest. Ophthalmol. Visual Sci. 53(7), 3501–3507 (2012).
[Crossref]

C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
[Crossref]

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
[Crossref]

Tatini, F.

R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
[Crossref]

Teng, S. W.

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
[Crossref]

Thomas, R.

R. P. Copt, R. Thomas, and A. Mermoud, “Corneal thickness in ocular hypertension, primary open-angle glaucoma, and normal tension glaucoma,” Arch. Ophthalmol. 117(1), 14–16 (1999).
[Crossref]

Thomasy, S.

M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
[Crossref]

Toussaint, K. C.

Tran, S. T.

M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
[Crossref]

Trelstad, R. L.

R. L. Trelstad and A. J. Coulombre, “Morphogenesis of the collagenous stroma in the chick cornea,” J. Cell Biol. 50(3), 840–858 (1971).
[Crossref]

Tsai, T. H.

W. L. Chen, P. S. Hu, A. Ghazaryan, S. J. Chen, T. H. Tsai, and C. Y. Dong, “Quantitative analysis of multiphoton excitation autofluorescence and second harmonic generation imaging for medical diagnosis,” Computerized Medical Imaging and Graphics 36(7), 519–526 (2012).
[Crossref]

Tuer, A. E.

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

Twa, M. D.

M. D. Twa and M. J. Giese, “Assessment of corneal thickness and keratocyte density in a rabbit model of laser in situ keratomileusis using scanning laser confocal microscopy,” Am. J. Ophthalmol. 152(6), 941–953.e1 (2011).
[Crossref]

Votruba, M.

S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
[Crossref]

Wahlert, A. J.

N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Visual Sci. 48(3), 1087–1094 (2007).
[Crossref]

Wang, S. S.

C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
[Crossref]

Whyne, C. M.

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

Wilson, B. C.

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

Winkler, M.

A. J. Quantock, M. Winkler, G. J. Parfitt, R. D. Young, D. J. Brown, C. Boote, and J. V. Jester, “From nano to macro: Studying the hierarchical structure of the corneal extracellular matrix,” Exp. Eye Res. 133, 81–99 (2015).
[Crossref]

M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
[Crossref]

Wu, R. J.

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
[Crossref]

Xie, Y.

M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
[Crossref]

Yamada, N.

N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
[Crossref]

Yang, C. H.

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
[Crossref]

Young, R. D.

A. J. Quantock, M. Winkler, G. J. Parfitt, R. D. Young, D. J. Brown, C. Boote, and J. V. Jester, “From nano to macro: Studying the hierarchical structure of the corneal extracellular matrix,” Exp. Eye Res. 133, 81–99 (2015).
[Crossref]

Young, T. H.

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
[Crossref]

ACS Biomater. Sci. Eng. (1)

S. L. Lee, Y. F. Chen, and C. Y. Dong, “Probing Multiscale Collagenous Tissue by Nonlinear Microscopy,” ACS Biomater. Sci. Eng. 3(11), 2825–2831 (2017).
[Crossref]

Am. J. Ophthalmol. (1)

M. D. Twa and M. J. Giese, “Assessment of corneal thickness and keratocyte density in a rabbit model of laser in situ keratomileusis using scanning laser confocal microscopy,” Am. J. Ophthalmol. 152(6), 941–953.e1 (2011).
[Crossref]

Anat. Rec. (2)

K. K. Svoboda and W. R. Reenstra, “Approaches to studying cellular signaling: a primer for morphologists,” Anat. Rec. 269(2), 123–139 (2002).
[Crossref]

S. Hayes, C. Boote, J. Lewis, J. Sheppard, M. Abahussin, A. J. Quantock, C. Purslow, M. Votruba, and K. M. Meek, “Comparative study of fibrillar collagen arrangement in the corneas of primates and other mammals,” Anat. Rec. 290(12), 1542–1550 (2007).
[Crossref]

Arch. Ophthalmol. (1)

R. P. Copt, R. Thomas, and A. Mermoud, “Corneal thickness in ocular hypertension, primary open-angle glaucoma, and normal tension glaucoma,” Arch. Ophthalmol. 117(1), 14–16 (1999).
[Crossref]

BioMed Res. Int. (1)

J. M. Bueno, F. J. Avila, and M. C. Martinez-Garcia, “Quantitative Analysis of the Corneal Collagen Distribution after In Vivo Cross-Linking with Second Harmonic Microscopy,” BioMed Res. Int. 2019, 1–12 (2019).
[Crossref]

Biomed. Opt. Express (1)

Biophys. J. (2)

C. M. Hsueh, W. Lo, W. L. Chen, V. A. Hovhannisyan, G. Y. Liu, S. S. Wang, H. Y. Tan, and C. Y. Dong, “Structural characterization of edematous corneas by forward and backward second harmonic generation imaging,” Biophys. J. 97(4), 1198–1205 (2009).
[Crossref]

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref]

Computerized Medical Imaging and Graphics (1)

W. L. Chen, P. S. Hu, A. Ghazaryan, S. J. Chen, T. H. Tsai, and C. Y. Dong, “Quantitative analysis of multiphoton excitation autofluorescence and second harmonic generation imaging for medical diagnosis,” Computerized Medical Imaging and Graphics 36(7), 519–526 (2012).
[Crossref]

Cornea (1)

J. M. Bueno, E. J. Gualda, and P. Artal, “Analysis of corneal stroma organization with wavefront optimized nonlinear microscopy,” Cornea 30(6), 692–701 (2011).
[Crossref]

Exp. Eye Res. (3)

A. J. Quantock, M. Winkler, G. J. Parfitt, R. D. Young, D. J. Brown, C. Boote, and J. V. Jester, “From nano to macro: Studying the hierarchical structure of the corneal extracellular matrix,” Exp. Eye Res. 133, 81–99 (2015).
[Crossref]

K. M. Meek and C. Boote, “The organization of collagen in the corneal stroma,” Exp. Eye Res. 78(3), 503–512 (2004).
[Crossref]

S. Chen, M. J. Mienaltowski, and D. E. Birk, “Regulation of corneal stroma extracellular matrix assembly,” Exp. Eye Res. 133, 69–80 (2015).
[Crossref]

Eye (1)

K. M. Meek, D. W. Leonard, C. J. Connon, S. Dennis, and S. Khan, “Transparency, swelling and scarring in the corneal stroma,” Eye 17(8), 927–936 (2003).
[Crossref]

Eye Contact Lens (1)

J. P. Bergmanson, J. Horne, M. J. Doughty, M. Garcia, and M. Gondo, “Assessment of the number of lamellae in the central region of the normal human corneal stroma at the resolution of the transmission electron microscope,” Eye Contact Lens 31(6), 281–287 (2005).
[Crossref]

Invest. Ophthalmol. Visual Sci. (6)

N. Morishige, Y. Takagi, T. Chikama, A. Takahara, and T. Nishida, “Three-dimensional analysis of collagen lamellae in the anterior stroma of the human cornea visualized by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 52(2), 911–915 (2011).
[Crossref]

J. V. Jester, W. M. Petroll, P. A. Barry, and H. D. Cavanagh, “Expression of alpha-smooth muscle (alpha-SM) actin during corneal stromal wound healing,” Invest. Ophthalmol. Visual Sci. 36(5), 809–819 (1995).

W. Lo, W. L. Chen, C. M. Hsueh, A. A. Ghazaryan, S. J. Chen, D. H. Ma, C. Y. Dong, and H. Y. Tan, “Fast Fourier transform-based analysis of second-harmonic generation image in keratoconic cornea,” Invest. Ophthalmol. Visual Sci. 53(7), 3501–3507 (2012).
[Crossref]

N. Morishige, R. Shin-Gyou-Uchi, H. Azumi, H. Ohta, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K. H. Sonoda, “Quantitative analysis of collagen lamellae in the normal and keratoconic human cornea by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Visual Sci. 55(12), 8377–8385 (2014).
[Crossref]

N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Visual Sci. 48(3), 1087–1094 (2007).
[Crossref]

M. Winkler, G. Shoa, S. T. Tran, Y. Xie, S. Thomasy, V. K. Raghunathan, C. Murphy, D. J. Brown, and J. V. Jester, “A Comparative Study of Vertebrate Corneal Structure: The Evolution of a Refractive Lens,” Invest. Ophthalmol. Visual Sci. 56(4), 2764–2772 (2015).
[Crossref]

J. Biomed. Opt. (2)

H. Y. Tan, Y. Sun, W. Lo, S. W. Teng, R. J. Wu, S. H. Jee, W. C. Lin, C. H. Hsiao, H. C. Lin, Y. F. Chen, D. H. Ma, S. C. Huang, S. J. Lin, and C. Y. Dong, “Multiphoton fluorescence and second harmonic generation microscopy for imaging infectious keratitis,” J. Biomed. Opt. 12(2), 024013 (2007).
[Crossref]

T. L. Sun, Y. Liu, M. C. Sung, H. C. Chen, C. H. Yang, V. Hovhannisyan, W. C. Lin, Y. M. Jeng, W. L. Chen, L. L. Chiou, G. T. Huang, K. H. Kim, P. T. So, Y. F. Chen, H. S. Lee, and C. Y. Dong, “Ex vivo imaging and quantification of liver fibrosis using second-harmonic generation microscopy,” J. Biomed. Opt. 15(3), 036002 (2010).
[Crossref]

J. Biophotonics (1)

R. Mercatelli, F. Ratto, F. Rossi, F. Tatini, L. Menabuoni, A. Malandrini, R. Nicoletti, R. Pini, F. S. Pavone, and R. Cicchi, “Three-dimensional mapping of the orientation of collagen corneal lamellae in healthy and keratoconic human corneas using SHG microscopy,” J. Biophotonics 10(1), 75–83 (2017).
[Crossref]

J. Cataract Refractive Surg. (2)

N. Morishige, W. M. Petroll, T. Nishida, M. C. Kenney, and J. V. Jester, “Noninvasive corneal stromal collagen imaging using two-photon-generated second-harmonic signals,” J. Cataract Refractive Surg. 32(11), 1784–1791 (2006).
[Crossref]

H. Y. Tan, Y. L. Chang, W. Lo, C. M. Hsueh, W. L. Chen, A. A. Ghazaryan, P. S. Hu, T. H. Young, S. J. Chen, and C. Y. Dong, “Characterizing the morphologic changes in collagen crosslinked-treated corneas by Fourier transform-second harmonic generation imaging,” J. Cataract Refractive Surg. 39(5), 779–788 (2013).
[Crossref]

J. Cell Biol. (1)

R. L. Trelstad and A. J. Coulombre, “Morphogenesis of the collagenous stroma in the chick cornea,” J. Cell Biol. 50(3), 840–858 (1971).
[Crossref]

J. Mech. Behav. Biomed. Mater. (1)

A. Benoit, G. Latour, S.-K. Marie-Claire, and J.-M. Allain, “Simultaneous microstructural and mechanical characterization of human corneas at increasing pressure,” J. Mech. Behav. Biomed. Mater. 60, 93–105 (2016).
[Crossref]

J. Struct. Biol. (1)

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref]

Opt. Express (3)

PLoS One (1)

S. L. Lee, A. Nekouzadeh, B. Butler, K. M. Pryse, W. B. McConnaughey, A. C. Nathan, W. R. Legant, P. M. Schaefer, R. B. Pless, E. L. Elson, and G. M. Genin, “Physically-induced cytoskeleton remodeling of cells in three-dimensional culture,” PLoS One 7(12), e45512 (2012).
[Crossref]

Prog. Retinal Eye Res. (2)

K. M. Meek and C. Boote, “The use of X-ray scattering techniques to quantify the orientation and distribution of collagen in the corneal stroma,” Prog. Retinal Eye Res. 28(5), 369–392 (2009).
[Crossref]

K. M. Meek and C. Knupp, “Corneal structure and transparency,” Prog. Retinal Eye Res. 49, 1–16 (2015).
[Crossref]

Semin. Cell Dev. Biol. (1)

J. V. Jester, “Corneal crystallins and the development of cellular transparency,” Semin. Cell Dev. Biol. 19(2), 82–93 (2008).
[Crossref]

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Figures (5)

Fig. 1.
Fig. 1. Second harmonic generation images of adult chicken cornea. (A) Adult chicken corneas were dissected as horizontal strips along the temporal-nasal axis. (B) The corneal strips were imaged sequentially at five positions at the equivalent distance of 2 mm from temporal-to-nasal side. (C) Three dimensional SHG reconstruction of the entire corneal stroma. (D) Illustration of the depth-dependent rotational pattern of corneal lamellae at different depths: 0 µm is closest to the corneal epithelial layer, and 400 µm is near the corneal endothelium.
Fig. 2.
Fig. 2. SHG image processing of corneal lamellae. (A) The process of computing the orientation of corneal collagen lamellae: 1 is the original SHG image; 2 represents its fast Fourier transform (FFT) result; 3 is the FFT image after adjusting the threshold of intensity; 4 illustrates how the angle was measured; and 5 is the histogram of collagen lamellar angle (blue) along with the fitted curve (red). (B) This procedure was repeated throughout the entire image stack to determine angular orientations as a function of depth.
Fig. 3.
Fig. 3. An example illustrating the depth-dependent variation in chicken corneal lamellar orientations. (A) Corneal SHG signals at different depths are shown in the top row. Images were collected in central cornea, i.e. Position 3 shown in Fig. 1B. (B) The filtered FFT images are displayed in the second row. Each filtered FFT image exhibits two principal directions of corneal lamella and are indicated by black and gray lines. The principal directions were calculated from FFT images by measuring angles in a counterclockwise direction from the positive x-axis. (C) Angular change calculated from adjacent SHG images were plotted as a function of depth.
Fig. 4.
Fig. 4. Depth-dependent orientation profiles of corneal stroma at five different positions. The same pattern of lamellar helicity was observed at all positions and for both left and right corneas.
Fig. 5.
Fig. 5. (A) Determination of Zone 1: anterior stroma, Zone 2: transition region, and Zone 3: posterior stroma. (B) 3D illustration of the variations of one principal direction of corneal lamellae.

Tables (5)

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Table 1. Thicknesses of Zones 1-3 at 5 positions for left and right corneas

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Table 2. Average rotational pitches of cornea lamellae at 5 positions for left and right chicken corneas.

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Table 3. Normalized thicknesses of Zone1, Zone 2 and Zone 3

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Table 4. Average rotational pitch, Zone 1 thickness and total rotational angle

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Table 5. Overall average values of rotational pitch, Zone 1 thickness and total angle of rotation

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