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

1. Introduction

Spatial arrangement of collagen and its interaction with cells in tissue is important in wound healing, tissue engineering and embryonic development [14]. In the case of cornea, stromal collagen is organized into lamellae that act as a highly transparent, protective layer for the eye. However, how the organization of stromal collagen contribute to the cornea’s biomechanical and optical properties is not completely understood. Structurally, the cornea is organized into five layers: epithelium, Bowman's layer, stroma, Descemet's membrane and endothelium. Stroma, the collagen-rich matrix derived from the periocular sulcus, is the thickest layer. Keratocytes located between lamellar collagen fibers secrete collagen and proteoglycans to produce a crystalline architecture which maintains corneal transparency [5]. During wound healing, keratocytes are transformed into fibroblasts and myofibroblasts [6]. Injuries caused by conditions such as infection and trauma are usually accompanied by corneal scarring and can affect corneal clarity. Corneal swelling in conditions such as Fuchs malnutrition contribute to increased scattering and can also lead to vision degradation. Finally, corneal thickness is an important index in the preservation of structure integrity and clinical evaluation of diseases [710]. Therefore, understanding the structural features of cornea in three dimensions is invaluable for basic research and clinical evaluation of corneal diseases.

In order to study corneal structure, a variety of imaging techniques such as optical microscopy, second harmonic generation (SHG) imaging, electron microscopy and X-ray scattering have been used to study normal and abnormal samples in humans and other species [1116]. For example, SHG imaging showed that cross-linking did not significantly affect structures of corneas with well-organized lamellae [17]. Moreover, optical and electron microscopies were used to study corneal development in the chick model and it was found that rotation of collagen lamellae evolves with maturation. [16]. Electron microscopy was also used to measure lamellar number in human corneal specimens [8]. In the optical domain, confocal imaging was used to measure corneal thickness and keratocyte density in the rabbit model [7]. Among these techniques, electron microscopy is laborious in that sample preparation is time-consuming and the information available from the tissue slice is limited to a small volume. X-ray scattering has its limitations in that the structural information obtained represents an integrated average over the entire stromal thickness.

In recent years, SHG microscopy has emerged as an effective technique for studying collagen-containing connective tissues [1821]. Second order non-linear polarization properties in rat tissues have been studied with polarization SHG microscopy [22]. In the case of cornea, SHG imaging was applied to studying structural features such as the density and width of collagen lamellae in human [10]. The effects of keratoconus, mechanical pressure, and photothermal modification on corneal lamellar structure have also been investigated [2331]. Finally, corneal lamellar structure in different species including chicken, fish, bullfrog and others were imaged and compared with SHG imaging [32,33]. Although earlier studies demonstrated a persistent rotational pattern of corneal lamellae in some species, detailed measurement of the lamellar helicity between left and right corneas were not compared. Clearly, a detailed characterization of cornea’s structure in three dimensions is important for understanding self-assembly of extracellular matrix and contribute to improved methodology in corneal tissue engineering.

In this study, we used a combination of a second harmonic generation (SHG) microscopy and fast Fourier transform-based image analysis to image and quantify the three-dimensional structure of cornea in the chicken model.

2. Material and methods

2.1 Preparation of chicken cornea specimens

Corneas from adult chicken of the Arbor Acres breed were acquired from the animal farm of National Taiwan University. Four pairs of left and right corneas from male chicken were used in this study. The diameter of each specimen was close to 8 mm. Prior to the imaging experiment, corneas were cut into strips along the temporal-nasal direction and marked with scissors on the temporal side to identify the specimen orientation. Each chicken cornea strip was stored in a home-made, specimen-containing chamber with 10% formalin. During imaging, the samples were enclosed in a confinement chamber attached to a concave cover slide and sealed with a cover glass and high-vacuum grease. While performing the imaging experiments, the formalin solution was replaced with PBS.

2.2 SHG image acquisition

Cornea specimens each approximately 10 × 10 × 0.7 mm3 in dimension were imaged using a homemade, multiphoton imaging system based on a commercial inverted microscope (TE2000U, Nikon, Japan). The excitation source was a titanium-sapphire laser (Tsunami, Spectra Physics, Mountain View, CA) pumped by a diode-pumped, solid-state (DPSS) laser system (Millennia Pro, Spectra Physics).

The excitation wavelength used was 780 nm. Focusing of the excitation source was achieved through an objective (S Flour, 20x, NA 0.75, WD 1.0, Nikon). The corresponding axial resolution was approximately 5.7 µm. Since the lamellae thickness is around 2-3 µm, we found that two adjacent lamellae can be visualized. The focusing objective is used to collect epi-illuminated signals which were filtered by appropriate band-pass filters. Specifically, the collected signals were spectrally resolved by a combination of dichroic mirrors (405dcxr, 530dcxr Chroma Technology) and filters (HQ390/10, HQ540/70, HQ630/70). In this manner, spectral signals centered at 390, 540, and 630 nm can be respectively collected. In the transmission geometry, forward second harmonic generation (FSHG) was collected by a second objective (S Flour, 20x, NA 0.75, WD 1.0, Nikon) and spectrally resolved by a dichroic mirror (535dcxr) and filter (HQ390/10). Each image 227 × 227 µm2 in area was scanned at 512 × 512 pixels resolution. All signals were detected by single-photon-counting photomultiplier tubes (R7400P, Hamamatsu, Hamamatsu City, Japan).

Image stacks were collected at five different positions, each along the temporal-nasal axis and at a distance 2 mm apart (Fig. 1A, B). At each position, scanning was performed in the anterior-posterior direction. To locate the boundary of the corneal stroma, signals from collagen and corneal cells were simultaneously collected. In this manner, forward SHG signal was used to visualize collagen fibrils and auto-fluorescence indicates the presence of corneal cells. A representative scanned volume is illustrated as an image stack (Fig. 1C). Variation of corneal stroma structure with depth was illustrated as an image series. As can be seen, the angle between two lamellae is close to being orthogonal and remains constant throughout stroma (Fig. 1D).

 figure: 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.

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2.3 Determination of imaging positions

For the five imaged positions, Positions 1 and 5 were chosen to be close to the interface between cornea and limbus, where Position 1 was closest to the temporal side and Position 5 was nearest to the nasal side. Once the Positions 1 and 5 were determined, Position 3 (between Positions 1 and 5) was marked as the central position of the cornea. Positions 2 and 4 were then determined, as the middle points between 1 and 3, and between 3 and 5, respectively. The distance of the adjacent layer in the image stack was 5 µm.

2.4 Fiber orientation analysis

After acquisition of depth-resolved SHG images, fast Fourier transform (FFT) analysis was performed on individual images and used to determine and track the rotational pattern of corneal lamellae in three dimensions. This process is illustrated in Fig. 2(A). The SHG image of corneal lamellae (Fig. 2(A), 1) was fast Fourier transformed into the corresponding frequency domain image (Fig. 2(A), 2). Next, thresholding techniques were applied to reveal the dominant collagen lamellar orientation (Fig. 2(A), 3). The value of thresholding used in the entire stack was between 140∼160 in the 8-bit intensity image. The FFT filtering method filtered out large structures (shading correction) and small structures (smoothing) of the specified size by Gaussian filtering. The optimized FFT images were then processed with custom-programs based on MATLAB R2010a (Mathworks, Cambridge, UK). Principal directions of lamellar orientations can be determined through an angular meter which is the frequency magnitudes plotted as a function of orientation (Fig. 2(A), 4). The distribution of lamellar orientation is shown in the histogram (Fig. 2(A), 5). ImageJ (National Institutes of Health, Bethesda, MD, USA) was used for reading raw data and reconstructing 3D image stacks. Following FFT analysis, the two intensity peaks (marked by circles) in the first two quadrants of the histograms (0-180°) were used to determine the principal directions of collagen lamellae. At succeeding depths, angular orientations of two major directions were determined relative to those at the previous depth. In this manner, depth-dependent variation of dominant lamellar orientations can be determined. In the case that total angular rotation is greater than 180°, our approach would limit a total angular change of the lamellae to be between 0-360° (Fig. 2(B)).

 figure: 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.

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2.5 Statistical analysis

From the measured angular orientations of collagen lamellae, we determined corneal thickness and rotational pitches for left and right corneas. Furthermore, Student’s t-test was used to determine the correlation of the data between left and right corneas. The resultant p values are shown in Tables 14.

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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

3. Results and discussion

3.1 Rotational helicity of lamellae in the stroma

Shown in Fig. 3 is a representative example of depth-dependent SHG images, corresponding FFT results, and lamellar orientations of a chicken cornea specimen. Depth-dependent variations in principal axes of collagen lamellae obtained from SHG images and FFT analysis are shown in Fig. 3(A) and 3(B). Our results show that starting from the corneal surface, angular orientations of the two primary axes vary monotonically in the anterior region (Fig. 3(C)).

 figure: 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.

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To analyze our results further, we obtained the depth-dependent profiles of lamellar orientations at Positions 1-5 for both left and right corneas (Fig. 4). With the results normalized to stroma thickness, we found that at each position, collagen lamellae rotate in a counterclockwise direction in the anterior stroma to approximately half of the cornea thickness. As depth further increases, the rotational pitch of lamellae gradually decreases until the lamella orientation remains constant. Therefore, changes in the rotational pitch of corneal lamellae can be categorized into three zones (Fig. 5(A)). Zone 1 (monotonic change in rotational pitch) is anterior stroma, Zone 2 is the transition region (slowing down of lamella rotation), and Zone 3 (constant lamella orientations) is posterior stroma.

 figure: 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.

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 figure: 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.

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3.2 Zonal definition and rotational pitch of corneal lamellae

To further analyze our results, we quantified zonal thicknesses of corneal collagen lamellae and rotational pitch of the anterior stroma. In determining Zone 1, we noticed that angular orientation as a function of depth fits well to a line. Therefore, we applied linear fitting to the lamellar angle as a function of depth for 40% of the stroma thickness from the corneal surface. When the difference of measured and fitted angles is more than 10 degrees at a given depth, that position would be defined as the end of Zone 1 and start of Zone 2, the transition region. To determine the other end point of Zone 2 and start of Zone 3, another linear model is used to fit angles measured from other 40% of the stromal thickness near the posterior stroma. When a 10-degrees difference is found between measured data and fitted result, the corresponding position is defined as the ending position of Zone 2. The rotational pitch of the anterior stroma is obtained from the slope of fitted angle vs. depth curve. The average rotational pitch at each position for the two principal axes of collagen lamellae are shown in Table 2. In addition to the thickness measurements, we also determined the ratios of the thickness of each zone to the overall stroma thickness (Table 3). We found the overall thickness for Zones 1, 2, and 3 are 176 ± 14, 31 ± 3, and 170 ± 22 µm, respectively.

By averaging the rotational pitch at each position, we found that the rotational pitches for the left cornea is 0.90 ± 0.10 degree/µm and 0.95 ± 0.11 degree/µm for the right cornea. These results differ from the 0.68 degree/µm result obtained in our earlier study [32]. A number of factors may contribute to such differences. First, the adult corneas in the previous study, were obtained from a local market without full knowledge of the species. In comparison, the corneas in the current study were obtained from a single species (Arbor Acres). Secondly, a more significant factor may be the state of the cornea tissues. For the cornea specimens obtained from the market, we did not know the precise time of chicken slaughter. In addition, since these chickens are for consumption, they are treated, possibly with hot water, for feather removal. In comparison, for the chicken obtain from our university farm, we made efforts to obtain the cornea specimens quickly after slaughter. In addition, no additional treatment was performed on the chicken. Therefore, tissue degradation and feather removal procedure from our previous study may contribute to differences in measured rotational pitches. Furthermore, by multiplying the rotational pitch and the thickness for Zone 1, we found that collagen lamellae in chicken cornea rotate 161 ± 23 degrees for the left cornea and 165 ± 21 degrees for the right cornea. However, if we computed the total angular change of Zones 1 and 2, collagen lamellae in chicken cornea rotate 166 ± 22 degrees for the left cornea and 173 ± 19 degrees for the right cornea. The total rotation including Zone 1 and Zone 2 is 169 ± 21 degrees. The results of left and right corneas were tabulated in the Table 4 and the overall values for all corneas were listed in the Table 5.

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

Previous studies had shown that posterior stroma was more ordered, better hydrated, more easily swollen, and has a lower refractive index than the anterior stroma [34]. However, the boundary between the anterior and posterior stroma was not clearly defined. In this study, we quantified the orientation of collagen lamellae as a function of depth. Our findings show that the counterclockwise rotation of corneal lamellae exists in both left and right corneas. In addition, the overall average rotation pitch, total Zone 1 rotational angle, and total Zone 1 thickness are 0.92 ± 0.11 degrees/µm, 163 ± 22 degrees, and 176 ± 14 µm, respectively. The total rotation on average between anterior and posterior stroma is 169 ± 21 degrees. The findings in this study may provide useful bioengineering clues in the further design of artificial cornea.

4. Conclusion

Previously, SHG imaging and Fourier analysis have been used to study the structures of various connective tissues such as trachea, ear and cornea [35,36]. Backward SHG combined with Fourier and aspect ratio analysis was used to investigate corneal collagen orientation [37]. Since forward SHG provides orientation information of corneal collagen fiber, the use of aspect ratio is not needed to define the two principal axes of cornea collagen lamella [28]. Furthermore, earlier electron and optical microscopy studies demonstrated changes in chick lamellar rotation during development [16]. Unlike previous studies, our work on chicken cornea superstructure found the same counterclockwise rotational helicity with depth persisted in both left and right corneas. The reflection symmetry of physical features typically observed along an organism’s sagittal plane is not conserved in the case of depth-dependent helicity of chicken corneal lamellae. While it was suggested to us that geometric packing of collagen molecules may favor such orientation, packing efficiency cannot be used to explain the lack of lamellar rotation in posterior stroma. In addition, we defined and quantitatively determined physical parameters that characterized lamellar geometry. Specifically, we found that the right cornea has a higher rotational pitch (0.95 ± 11 vs 0.90 ± 10 degrees/µm) and thinner Zone 1 (173 ± 13 vs 179 ± 14 µm). Interestingly, the two effects cancel each other out and result in similar angular rotation of Zone 1 (161 ± 23 and 165 degrees ± 21). Furthermore, the p values in Tables 14 show, except for Zone 1, point 2 where the p value is 0.047 (Table 1), all other p values are larger than 0.05, suggesting that differences of the measured thicknesses of different zones and rotational pitches between left and right corneas are insignificant. Finally, our observation of a total angular rotation of 169 ± 21 degrees (Table 5) shows that within experimental error, chicken cornea lamellae rotates around 180 degrees or half of a complete turn. As the current study focused on lamellar orientation and thickness of chicken cornea, additional studies are needed to arrive at an explanation of chicken superstructure in three dimensions.

Funding

Ministry of Science and Technology, Taiwan (MOST-104-2112-M-002-018-MY3, MOST-107-2112-M-002 -023 -MY3).

Disclosures

The authors declare that there are no conflicts of interest related to the article

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References

  • View by:

  1. S. Chen, M. J. Mienaltowski, and D. E. Birk, “Regulation of corneal stroma extracellular matrix assembly,” Exp. Eye Res. 133, 69–80 (2015).
    [Crossref]
  2. 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]
  3. 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]
  4. K. K. Svoboda and W. R. Reenstra, “Approaches to studying cellular signaling: a primer for morphologists,” Anat. Rec. 269(2), 123–139 (2002).
    [Crossref]
  5. J. V. Jester, “Corneal crystallins and the development of cellular transparency,” Semin. Cell Dev. Biol. 19(2), 82–93 (2008).
    [Crossref]
  6. 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).
  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).
    [Crossref]
  8. 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]
  9. 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]
  10. 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]
  11. 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]
  12. K. M. Meek and C. Boote, “The organization of collagen in the corneal stroma,” Exp. Eye Res. 78(3), 503–512 (2004).
    [Crossref]
  13. 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]
  14. 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]
  15. 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]
  16. 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]
  17. 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]
  18. 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]
  19. 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]
  20. 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]
  21. 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]
  22. 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]
  23. 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]
  24. 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]
  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]
  28. 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]
  29. 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]
  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).
[Crossref]

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).
[Crossref]

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).
[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]

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]

Butler, 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).
[Crossref]

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).

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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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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).
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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).
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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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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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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).
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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).
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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. 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).
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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).
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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).
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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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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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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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Lee, S. L.

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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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, 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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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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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).
[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).
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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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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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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).
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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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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, 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, 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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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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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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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).
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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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Reenstra, W. R.

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).
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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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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).
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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).
[Crossref]

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).
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Tatini, F.

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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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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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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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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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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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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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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).
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Biomed. Opt. Express (1)

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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]

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).
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Cornea (1)

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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).
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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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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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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).
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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).
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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).

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).
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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).
[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).
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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).
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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).
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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).
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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).
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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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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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