Abstract

Defining fiber orientation at each voxel within a 3D biomedical image stack is potentially useful for a variety of applications, including cancer, wound healing and tissue regeneration. Current methods are typically computationally intensive or inaccurate. Herein, we present a 3D weighted orientation vector summation algorithm, which is a generalization of a previously reported 2D vector summation technique aimed at quantifying collagen fiber orientations simultaneously at each voxel of an image stack. As a result, voxel-wise fiber orientation information with 4° to 5° accuracy can be determined, and the computational time required to analyze a typical stack with the size of 512x512x100 voxels is less than 5 min. Thus, this technique enables the practical extraction of voxel-specific orientation data for characterizing structural anisotropy in 3D specimens. As examples, we use this approach to characterize the fiber organization in an excised mouse mammary gland and a 3D breast tissue model.

© 2015 Optical Society of America

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References

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2015 (1)

K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
[Crossref] [PubMed]

2014 (2)

L. Speroni, G. S. Whitt, J. Xylas, K. P. Quinn, A. Jondeau-Cabaton, C. Barnes, I. Georgakoudi, C. Sonnenschein, and A. M. Soto, “Hormonal regulation of epithelial organization in a 3D breast tissue culture model,” Tissue Eng. Part C Methods 20(1), 42–51 (2014).
[Crossref] [PubMed]

C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
[Crossref] [PubMed]

2013 (1)

K. P. Quinn and I. Georgakoudi, “Rapid quantification of pixel-wise fiber orientation data in micrographs,” J. Biomed. Opt. 18(4), 046003 (2013).
[Crossref] [PubMed]

2012 (2)

H. Altendorf, E. Decencière, D. Jeulin, P. De sa Peixoto, A. Deniset-Besseau, E. Angelini, G. Mosser, and M.-C. Schanne-Klein, “Imaging and 3D morphological analysis of collagen fibrils,” J. Microsc. 247(2), 161–175 (2012).
[Crossref] [PubMed]

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] [PubMed]

2011 (2)

G. M. Cunniffe and F. J. OBrien, “Collagen scaffolds for orthopedic regenerative medicine,” J. Miner. Met. Mater. Soc. 63(4), 66–73 (2011).
[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. Vis. Sci. 52(2), 911–915 (2011).
[PubMed]

2010 (2)

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. C. 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] [PubMed]

M. Sivaguru, S. Durgam, R. Ambekar, D. Luedtke, G. Fried, A. Stewart, and K. C. Toussaint., “Quantitative analysis of collagen fiber organization in injured tendons using Fourier transform-second harmonic generation imaging,” Opt. Express 18(24), 24983–24993 (2010).
[Crossref] [PubMed]

2009 (5)

A. Rodriguez, D. B. Ehlenberger, P. R. Hof, and S. L. Wearne, “Three-dimensional neuron tracing by voxel scooping,” J. Neurosci. Methods 184(1), 169–175 (2009).
[PubMed]

N. Morishige, N. Yamada, S. Teranishi, T. Chikama, T. Nishida, and A. Takahara, “Detection of subepithelial fibrosis associated with corneal stromal edema by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 50(7), 3145–3150 (2009).
[PubMed]

E. A. Sander and V. H. Barocas, “Comparison of 2D fiber network orientation measurement methods,” J. Biomed. Mater. Res. A 88(2), 322–331 (2009).
[Crossref] [PubMed]

P. S. Robinson and R. T. Tranquillo, “Planar biaxial behavior of fibrin-based tissue-engineered heart valve leaflets,” Tissue Eng. Part A 15(10), 2763–2772 (2009).
[Crossref] [PubMed]

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys. 105(10), 102042 (2009).
[Crossref] [PubMed]

2008 (2)

C. E. Ayres, B. S. Jha, H. Meredith, J. R. Bowman, G. L. Bowlin, S. C. Henderson, and D. G. Simpson, “Measuring fiber alignment in electrospun scaffolds: a user’s guide to the 2D fast Fourier transform approach,” J. Biomater. Sci. Polym. Ed. 19(5), 603–621 (2008).
[Crossref] [PubMed]

Y. Zhou and Y. P. Zheng, “Estimation of muscle fiber orientation in ultrasound images using revoting hough transform (RVHT),” Ultrasound Med. Biol. 34(9), 1474–1481 (2008).
[Crossref] [PubMed]

2007 (3)

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
[Crossref] [PubMed]

M. Hadian, B. M. Corcoran, R. I. Han, J. G. Grossmann, and J. P. Bradshaw, “Collagen organization in canine myxomatous mitral valve disease: an x-ray diffraction study,” Biophys. J. 93(7), 2472–2476 (2007).
[Crossref] [PubMed]

K. Sandau and J. Ohser, “The chord length transform and the segmentation of crossing fibres,” J. Microsc. 226(1), 43–53 (2007).
[Crossref] [PubMed]

2006 (4)

O. Friman, G. Farnebäck, and C. F. Westin, “A Bayesian approach for stochastic white matter tractography,” IEEE Trans. Med. Imaging 25(8), 965–978 (2006).
[Crossref] [PubMed]

M. J. Buehler, “Nature designs tough collagen: Explaining the nanostructure of collagen fibrils,” Proc. Natl. Acad. Sci. U.S.A. 103(33), 12285–12290 (2006).
[Crossref] [PubMed]

S. Thomopoulos, J. P. Marquez, B. Weinberger, V. Birman, and G. M. Genin, “Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations,” J. Biomech. 39(10), 1842–1851 (2006).
[Crossref] [PubMed]

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
[Crossref] [PubMed]

2005 (1)

B. Josso, D. R. Burton, and M. J. Lalor, “Texture orientation and anisotropy calculation by Fourier transform and principal component analysis,” Mech. Syst. Signal Process. 19(5), 1152–1161 (2005).
[Crossref]

2004 (2)

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

F. Rosso, A. Giordano, M. Barbarisi, and A. Barbarisi, “From cell-ECM interactions to tissue engineering,” J. Cell. Physiol. 199(2), 174–180 (2004).
[Crossref] [PubMed]

2003 (1)

J. Wu, B. Rajwa, D. L. Filmer, C. M. Hoffmann, B. Yuan, C. S. Chiang, J. Sturgis, and J. P. Robinson, “Analysis of orientations of collagen fibers by novel fiber-tracking software,” Microsc. Microanal. 9(6), 574–580 (2003).
[Crossref] [PubMed]

2002 (2)

S. Mori and P. C. M. van Zijl, “Fiber tracking: principles and strategies - a technical review,” NMR Biomed. 15(7-8), 468–480 (2002).
[Crossref] [PubMed]

G. A. Di Lullo, S. M. Sweeney, J. Körkkö, L. Ala-Kokko, and J. D. San Antonio, “Mapping the Ligand-binding Sites and Disease-associated Mutations on the Most Abundant Protein in the Human, Type I Collagen,” J. Biol. Chem. 277(6), 4223–4231 (2002).
[Crossref] [PubMed]

2000 (1)

W. Yi and S. Marshall, “Principal component analysis in application to object orientation,” Geo-Spat. Inf. Sci. 3(3), 76–78 (2000).

1998 (1)

L. Hong, Y. F. Wan, and A. Jain, “Fingerprint image enhancement: algorithm and performance evaluation,” IEEE T. Pattern Anal. 20(8), 777–789 (1998).

1991 (1)

A. R. Rao and B. G. Schunck, “Computing oriented texture fields,” CVGIP Graph. Model. Im. 53(2), 157–185 (1991).
[Crossref]

1980 (1)

D. R. Eyre, “Collagen: Molecular Diversity in the Body’s Protein Scaffold,” Science 207(4437), 1315–1322 (1980).
[Crossref] [PubMed]

Ala-Kokko, L.

G. A. Di Lullo, S. M. Sweeney, J. Körkkö, L. Ala-Kokko, and J. D. San Antonio, “Mapping the Ligand-binding Sites and Disease-associated Mutations on the Most Abundant Protein in the Human, Type I Collagen,” J. Biol. Chem. 277(6), 4223–4231 (2002).
[Crossref] [PubMed]

Albadawi, H.

A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

Altendorf, H.

H. Altendorf, E. Decencière, D. Jeulin, P. De sa Peixoto, A. Deniset-Besseau, E. Angelini, G. Mosser, and M.-C. Schanne-Klein, “Imaging and 3D morphological analysis of collagen fibrils,” J. Microsc. 247(2), 161–175 (2012).
[Crossref] [PubMed]

Ambekar, R.

Angelini, E.

H. Altendorf, E. Decencière, D. Jeulin, P. De sa Peixoto, A. Deniset-Besseau, E. Angelini, G. Mosser, and M.-C. Schanne-Klein, “Imaging and 3D morphological analysis of collagen fibrils,” J. Microsc. 247(2), 161–175 (2012).
[Crossref] [PubMed]

Austen, W. G.

K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
[Crossref] [PubMed]

A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

Ayres, C. E.

C. E. Ayres, B. S. Jha, H. Meredith, J. R. Bowman, G. L. Bowlin, S. C. Henderson, and D. G. Simpson, “Measuring fiber alignment in electrospun scaffolds: a user’s guide to the 2D fast Fourier transform approach,” J. Biomater. Sci. Polym. Ed. 19(5), 603–621 (2008).
[Crossref] [PubMed]

Barbarisi, A.

F. Rosso, A. Giordano, M. Barbarisi, and A. Barbarisi, “From cell-ECM interactions to tissue engineering,” J. Cell. Physiol. 199(2), 174–180 (2004).
[Crossref] [PubMed]

Barbarisi, M.

F. Rosso, A. Giordano, M. Barbarisi, and A. Barbarisi, “From cell-ECM interactions to tissue engineering,” J. Cell. Physiol. 199(2), 174–180 (2004).
[Crossref] [PubMed]

Barnes, C.

L. Speroni, G. S. Whitt, J. Xylas, K. P. Quinn, A. Jondeau-Cabaton, C. Barnes, I. Georgakoudi, C. Sonnenschein, and A. M. Soto, “Hormonal regulation of epithelial organization in a 3D breast tissue culture model,” Tissue Eng. Part C Methods 20(1), 42–51 (2014).
[Crossref] [PubMed]

C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
[Crossref] [PubMed]

Barocas, V. H.

E. A. Sander and V. H. Barocas, “Comparison of 2D fiber network orientation measurement methods,” J. Biomed. Mater. Res. A 88(2), 322–331 (2009).
[Crossref] [PubMed]

Bayan, C.

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys. 105(10), 102042 (2009).
[Crossref] [PubMed]

Beaurepaire, E.

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
[Crossref] [PubMed]

Belov, V.

A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

Birman, V.

S. Thomopoulos, J. P. Marquez, B. Weinberger, V. Birman, and G. M. Genin, “Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations,” J. Biomech. 39(10), 1842–1851 (2006).
[Crossref] [PubMed]

Bode-Animashaun, G.

C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
[Crossref] [PubMed]

Bouma, B.

K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
[Crossref] [PubMed]

Bowlin, G. L.

C. E. Ayres, B. S. Jha, H. Meredith, J. R. Bowman, G. L. Bowlin, S. C. Henderson, and D. G. Simpson, “Measuring fiber alignment in electrospun scaffolds: a user’s guide to the 2D fast Fourier transform approach,” J. Biomater. Sci. Polym. Ed. 19(5), 603–621 (2008).
[Crossref] [PubMed]

Bowman, J. R.

C. E. Ayres, B. S. Jha, H. Meredith, J. R. Bowman, G. L. Bowlin, S. C. Henderson, and D. G. Simpson, “Measuring fiber alignment in electrospun scaffolds: a user’s guide to the 2D fast Fourier transform approach,” J. Biomater. Sci. Polym. Ed. 19(5), 603–621 (2008).
[Crossref] [PubMed]

Bradshaw, J. P.

M. Hadian, B. M. Corcoran, R. I. Han, J. G. Grossmann, and J. P. Bradshaw, “Collagen organization in canine myxomatous mitral valve disease: an x-ray diffraction study,” Biophys. J. 93(7), 2472–2476 (2007).
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K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
[Crossref] [PubMed]

A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

Brun, A.

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
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B. Josso, D. R. Burton, and M. J. Lalor, “Texture orientation and anisotropy calculation by Fourier transform and principal component analysis,” Mech. Syst. Signal Process. 19(5), 1152–1161 (2005).
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P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
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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. C. 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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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. C. 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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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. C. 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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J. Wu, B. Rajwa, D. L. Filmer, C. M. Hoffmann, B. Yuan, C. S. Chiang, J. Sturgis, and J. P. Robinson, “Analysis of orientations of collagen fibers by novel fiber-tracking software,” Microsc. Microanal. 9(6), 574–580 (2003).
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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. Vis. Sci. 52(2), 911–915 (2011).
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N. Morishige, N. Yamada, S. Teranishi, T. Chikama, T. Nishida, and A. Takahara, “Detection of subepithelial fibrosis associated with corneal stromal edema by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 50(7), 3145–3150 (2009).
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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. C. 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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M. Hadian, B. M. Corcoran, R. I. Han, J. G. Grossmann, and J. P. Bradshaw, “Collagen organization in canine myxomatous mitral valve disease: an x-ray diffraction study,” Biophys. J. 93(7), 2472–2476 (2007).
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Crestani, B.

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
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A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
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H. Altendorf, E. Decencière, D. Jeulin, P. De sa Peixoto, A. Deniset-Besseau, E. Angelini, G. Mosser, and M.-C. Schanne-Klein, “Imaging and 3D morphological analysis of collagen fibrils,” J. Microsc. 247(2), 161–175 (2012).
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H. Altendorf, E. Decencière, D. Jeulin, P. De sa Peixoto, A. Deniset-Besseau, E. Angelini, G. Mosser, and M.-C. Schanne-Klein, “Imaging and 3D morphological analysis of collagen fibrils,” J. Microsc. 247(2), 161–175 (2012).
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G. A. Di Lullo, S. M. Sweeney, J. Körkkö, L. Ala-Kokko, and J. D. San Antonio, “Mapping the Ligand-binding Sites and Disease-associated Mutations on the Most Abundant Protein in the Human, Type I Collagen,” J. Biol. Chem. 277(6), 4223–4231 (2002).
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Dong, C. Y.

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. C. 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] [PubMed]

Downes, C. S.

C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
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Durgam, S.

Ehlenberger, D. B.

A. Rodriguez, D. B. Ehlenberger, P. R. Hof, and S. L. Wearne, “Three-dimensional neuron tracing by voxel scooping,” J. Neurosci. Methods 184(1), 169–175 (2009).
[PubMed]

Eliceiri, K. W.

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
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A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
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O. Friman, G. Farnebäck, and C. F. Westin, “A Bayesian approach for stochastic white matter tractography,” IEEE Trans. Med. Imaging 25(8), 965–978 (2006).
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J. Wu, B. Rajwa, D. L. Filmer, C. M. Hoffmann, B. Yuan, C. S. Chiang, J. Sturgis, and J. P. Robinson, “Analysis of orientations of collagen fibers by novel fiber-tracking software,” Microsc. Microanal. 9(6), 574–580 (2003).
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Friman, O.

O. Friman, G. Farnebäck, and C. F. Westin, “A Bayesian approach for stochastic white matter tractography,” IEEE Trans. Med. Imaging 25(8), 965–978 (2006).
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S. Thomopoulos, J. P. Marquez, B. Weinberger, V. Birman, and G. M. Genin, “Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations,” J. Biomech. 39(10), 1842–1851 (2006).
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Georgakoudi, I.

K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
[Crossref] [PubMed]

C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
[Crossref] [PubMed]

L. Speroni, G. S. Whitt, J. Xylas, K. P. Quinn, A. Jondeau-Cabaton, C. Barnes, I. Georgakoudi, C. Sonnenschein, and A. M. Soto, “Hormonal regulation of epithelial organization in a 3D breast tissue culture model,” Tissue Eng. Part C Methods 20(1), 42–51 (2014).
[Crossref] [PubMed]

K. P. Quinn and I. Georgakoudi, “Rapid quantification of pixel-wise fiber orientation data in micrographs,” J. Biomed. Opt. 18(4), 046003 (2013).
[Crossref] [PubMed]

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys. 105(10), 102042 (2009).
[Crossref] [PubMed]

A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

Giordano, A.

F. Rosso, A. Giordano, M. Barbarisi, and A. Barbarisi, “From cell-ECM interactions to tissue engineering,” J. Cell. Physiol. 199(2), 174–180 (2004).
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Golberg, A.

K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
[Crossref] [PubMed]

A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

Grossmann, J. G.

M. Hadian, B. M. Corcoran, R. I. Han, J. G. Grossmann, and J. P. Bradshaw, “Collagen organization in canine myxomatous mitral valve disease: an x-ray diffraction study,” Biophys. J. 93(7), 2472–2476 (2007).
[Crossref] [PubMed]

Hadian, M.

M. Hadian, B. M. Corcoran, R. I. Han, J. G. Grossmann, and J. P. Bradshaw, “Collagen organization in canine myxomatous mitral valve disease: an x-ray diffraction study,” Biophys. J. 93(7), 2472–2476 (2007).
[Crossref] [PubMed]

Han, R. I.

M. Hadian, B. M. Corcoran, R. I. Han, J. G. Grossmann, and J. P. Bradshaw, “Collagen organization in canine myxomatous mitral valve disease: an x-ray diffraction study,” Biophys. J. 93(7), 2472–2476 (2007).
[Crossref] [PubMed]

Henderson, S. C.

C. E. Ayres, B. S. Jha, H. Meredith, J. R. Bowman, G. L. Bowlin, S. C. Henderson, and D. G. Simpson, “Measuring fiber alignment in electrospun scaffolds: a user’s guide to the 2D fast Fourier transform approach,” J. Biomater. Sci. Polym. Ed. 19(5), 603–621 (2008).
[Crossref] [PubMed]

Hof, P. R.

A. Rodriguez, D. B. Ehlenberger, P. R. Hof, and S. L. Wearne, “Three-dimensional neuron tracing by voxel scooping,” J. Neurosci. Methods 184(1), 169–175 (2009).
[PubMed]

Hoffmann, C. M.

J. Wu, B. Rajwa, D. L. Filmer, C. M. Hoffmann, B. Yuan, C. S. Chiang, J. Sturgis, and J. P. Robinson, “Analysis of orientations of collagen fibers by novel fiber-tracking software,” Microsc. Microanal. 9(6), 574–580 (2003).
[Crossref] [PubMed]

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L. Hong, Y. F. Wan, and A. Jain, “Fingerprint image enhancement: algorithm and performance evaluation,” IEEE T. Pattern Anal. 20(8), 777–789 (1998).

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. C. 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] [PubMed]

Howard, C. V.

C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
[Crossref] [PubMed]

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. C. 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] [PubMed]

Inman, D. R.

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
[Crossref] [PubMed]

Jain, A.

L. Hong, Y. F. Wan, and A. Jain, “Fingerprint image enhancement: algorithm and performance evaluation,” IEEE T. Pattern Anal. 20(8), 777–789 (1998).

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. C. 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] [PubMed]

Jeulin, D.

H. Altendorf, E. Decencière, D. Jeulin, P. De sa Peixoto, A. Deniset-Besseau, E. Angelini, G. Mosser, and M.-C. Schanne-Klein, “Imaging and 3D morphological analysis of collagen fibrils,” J. Microsc. 247(2), 161–175 (2012).
[Crossref] [PubMed]

Jha, B. S.

C. E. Ayres, B. S. Jha, H. Meredith, J. R. Bowman, G. L. Bowlin, S. C. Henderson, and D. G. Simpson, “Measuring fiber alignment in electrospun scaffolds: a user’s guide to the 2D fast Fourier transform approach,” J. Biomater. Sci. Polym. Ed. 19(5), 603–621 (2008).
[Crossref] [PubMed]

Jolesz, F. A.

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

Jondeau-Cabaton, A.

L. Speroni, G. S. Whitt, J. Xylas, K. P. Quinn, A. Jondeau-Cabaton, C. Barnes, I. Georgakoudi, C. Sonnenschein, and A. M. Soto, “Hormonal regulation of epithelial organization in a 3D breast tissue culture model,” Tissue Eng. Part C Methods 20(1), 42–51 (2014).
[Crossref] [PubMed]

Josso, B.

B. Josso, D. R. Burton, and M. J. Lalor, “Texture orientation and anisotropy calculation by Fourier transform and principal component analysis,” Mech. Syst. Signal Process. 19(5), 1152–1161 (2005).
[Crossref]

Kaplan, D.

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys. 105(10), 102042 (2009).
[Crossref] [PubMed]

Keely, P. J.

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
[Crossref] [PubMed]

Khan, S.

K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
[Crossref] [PubMed]

A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

Kikinis, R.

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

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. C. 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] [PubMed]

Körkkö, J.

G. A. Di Lullo, S. M. Sweeney, J. Körkkö, L. Ala-Kokko, and J. D. San Antonio, “Mapping the Ligand-binding Sites and Disease-associated Mutations on the Most Abundant Protein in the Human, Type I Collagen,” J. Biol. Chem. 277(6), 4223–4231 (2002).
[Crossref] [PubMed]

Kubicki, M.

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

Lalor, M. J.

B. Josso, D. R. Burton, and M. J. Lalor, “Texture orientation and anisotropy calculation by Fourier transform and principal component analysis,” Mech. Syst. Signal Process. 19(5), 1152–1161 (2005).
[Crossref]

Lau, T. Y.

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. C. 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] [PubMed]

Levitt, J. M.

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys. 105(10), 102042 (2009).
[Crossref] [PubMed]

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. C. 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, Y.

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. C. 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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Luedtke, D.

Marchal-Somme, J.

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
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S. Thomopoulos, J. P. Marquez, B. Weinberger, V. Birman, and G. M. Genin, “Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations,” J. Biomech. 39(10), 1842–1851 (2006).
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McCarley, R. W.

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

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C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
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C. E. Ayres, B. S. Jha, H. Meredith, J. R. Bowman, G. L. Bowlin, S. C. Henderson, and D. G. Simpson, “Measuring fiber alignment in electrospun scaffolds: a user’s guide to the 2D fast Fourier transform approach,” J. Biomater. Sci. Polym. Ed. 19(5), 603–621 (2008).
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Mihm, M. C.

K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
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A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

Miller, E.

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys. 105(10), 102042 (2009).
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C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
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S. Mori and P. C. M. van Zijl, “Fiber tracking: principles and strategies - a technical review,” NMR Biomed. 15(7-8), 468–480 (2002).
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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. Vis. Sci. 52(2), 911–915 (2011).
[PubMed]

N. Morishige, N. Yamada, S. Teranishi, T. Chikama, T. Nishida, and A. Takahara, “Detection of subepithelial fibrosis associated with corneal stromal edema by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 50(7), 3145–3150 (2009).
[PubMed]

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H. Altendorf, E. Decencière, D. Jeulin, P. De sa Peixoto, A. Deniset-Besseau, E. Angelini, G. Mosser, and M.-C. Schanne-Klein, “Imaging and 3D morphological analysis of collagen fibrils,” J. Microsc. 247(2), 161–175 (2012).
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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. Vis. Sci. 52(2), 911–915 (2011).
[PubMed]

N. Morishige, N. Yamada, S. Teranishi, T. Chikama, T. Nishida, and A. Takahara, “Detection of subepithelial fibrosis associated with corneal stromal edema by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 50(7), 3145–3150 (2009).
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A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

Park, H. J.

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

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H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

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A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech. 70(2), 162–170 (2007).
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P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
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K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
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C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
[Crossref] [PubMed]

L. Speroni, G. S. Whitt, J. Xylas, K. P. Quinn, A. Jondeau-Cabaton, C. Barnes, I. Georgakoudi, C. Sonnenschein, and A. M. Soto, “Hormonal regulation of epithelial organization in a 3D breast tissue culture model,” Tissue Eng. Part C Methods 20(1), 42–51 (2014).
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K. P. Quinn and I. Georgakoudi, “Rapid quantification of pixel-wise fiber orientation data in micrographs,” J. Biomed. Opt. 18(4), 046003 (2013).
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A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

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J. Wu, B. Rajwa, D. L. Filmer, C. M. Hoffmann, B. Yuan, C. S. Chiang, J. Sturgis, and J. P. Robinson, “Analysis of orientations of collagen fibers by novel fiber-tracking software,” Microsc. Microanal. 9(6), 574–580 (2003).
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J. Wu, B. Rajwa, D. L. Filmer, C. M. Hoffmann, B. Yuan, C. S. Chiang, J. Sturgis, and J. P. Robinson, “Analysis of orientations of collagen fibers by novel fiber-tracking software,” Microsc. Microanal. 9(6), 574–580 (2003).
[Crossref] [PubMed]

Robinson, P. S.

P. S. Robinson and R. T. Tranquillo, “Planar biaxial behavior of fibrin-based tissue-engineered heart valve leaflets,” Tissue Eng. Part A 15(10), 2763–2772 (2009).
[Crossref] [PubMed]

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G. A. Di Lullo, S. M. Sweeney, J. Körkkö, L. Ala-Kokko, and J. D. San Antonio, “Mapping the Ligand-binding Sites and Disease-associated Mutations on the Most Abundant Protein in the Human, Type I Collagen,” J. Biol. Chem. 277(6), 4223–4231 (2002).
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K. Sandau and J. Ohser, “The chord length transform and the segmentation of crossing fibres,” J. Microsc. 226(1), 43–53 (2007).
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[Crossref] [PubMed]

Schanne-Klein, M.-C.

H. Altendorf, E. Decencière, D. Jeulin, P. De sa Peixoto, A. Deniset-Besseau, E. Angelini, G. Mosser, and M.-C. Schanne-Klein, “Imaging and 3D morphological analysis of collagen fibrils,” J. Microsc. 247(2), 161–175 (2012).
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A. R. Rao and B. G. Schunck, “Computing oriented texture fields,” CVGIP Graph. Model. Im. 53(2), 157–185 (1991).
[Crossref]

Shenton, M. E.

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

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K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
[Crossref] [PubMed]

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C. E. Ayres, B. S. Jha, H. Meredith, J. R. Bowman, G. L. Bowlin, S. C. Henderson, and D. G. Simpson, “Measuring fiber alignment in electrospun scaffolds: a user’s guide to the 2D fast Fourier transform approach,” J. Biomater. Sci. Polym. Ed. 19(5), 603–621 (2008).
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So, P. T. 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. C. 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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C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
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L. Speroni, G. S. Whitt, J. Xylas, K. P. Quinn, A. Jondeau-Cabaton, C. Barnes, I. Georgakoudi, C. Sonnenschein, and A. M. Soto, “Hormonal regulation of epithelial organization in a 3D breast tissue culture model,” Tissue Eng. Part C Methods 20(1), 42–51 (2014).
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Soto, A. M.

L. Speroni, G. S. Whitt, J. Xylas, K. P. Quinn, A. Jondeau-Cabaton, C. Barnes, I. Georgakoudi, C. Sonnenschein, and A. M. Soto, “Hormonal regulation of epithelial organization in a 3D breast tissue culture model,” Tissue Eng. Part C Methods 20(1), 42–51 (2014).
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C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
[Crossref] [PubMed]

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C. Barnes, L. Speroni, K. P. Quinn, M. Montevil, K. Saetzler, G. Bode-Animashaun, G. McKerr, I. Georgakoudi, C. S. Downes, C. Sonnenschein, C. V. Howard, and A. M. Soto, “From single cells to tissues: interactions between the matrix and human breast cells in real time,” PLoS ONE 9(4), e93325 (2014).
[Crossref] [PubMed]

L. Speroni, G. S. Whitt, J. Xylas, K. P. Quinn, A. Jondeau-Cabaton, C. Barnes, I. Georgakoudi, C. Sonnenschein, and A. M. Soto, “Hormonal regulation of epithelial organization in a 3D breast tissue culture model,” Tissue Eng. Part C Methods 20(1), 42–51 (2014).
[Crossref] [PubMed]

Stewart, A.

Sturgis, J.

J. Wu, B. Rajwa, D. L. Filmer, C. M. Hoffmann, B. Yuan, C. S. Chiang, J. Sturgis, and J. P. Robinson, “Analysis of orientations of collagen fibers by novel fiber-tracking software,” Microsc. Microanal. 9(6), 574–580 (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. C. 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] [PubMed]

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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. C. 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] [PubMed]

Sweeney, S. M.

G. A. Di Lullo, S. M. Sweeney, J. Körkkö, L. Ala-Kokko, and J. D. San Antonio, “Mapping the Ligand-binding Sites and Disease-associated Mutations on the Most Abundant Protein in the Human, Type I Collagen,” J. Biol. Chem. 277(6), 4223–4231 (2002).
[Crossref] [PubMed]

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. Vis. Sci. 52(2), 911–915 (2011).
[PubMed]

Takahara, A.

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. Vis. Sci. 52(2), 911–915 (2011).
[PubMed]

N. Morishige, N. Yamada, S. Teranishi, T. Chikama, T. Nishida, and A. Takahara, “Detection of subepithelial fibrosis associated with corneal stromal edema by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 50(7), 3145–3150 (2009).
[PubMed]

Talos, I. F.

H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

Teranishi, S.

N. Morishige, N. Yamada, S. Teranishi, T. Chikama, T. Nishida, and A. Takahara, “Detection of subepithelial fibrosis associated with corneal stromal edema by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 50(7), 3145–3150 (2009).
[PubMed]

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S. Thomopoulos, J. P. Marquez, B. Weinberger, V. Birman, and G. M. Genin, “Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations,” J. Biomech. 39(10), 1842–1851 (2006).
[Crossref] [PubMed]

Toussaint, K. C.

Tranquillo, R. T.

P. S. Robinson and R. T. Tranquillo, “Planar biaxial behavior of fibrin-based tissue-engineered heart valve leaflets,” Tissue Eng. Part A 15(10), 2763–2772 (2009).
[Crossref] [PubMed]

van Zijl, P. C. M.

S. Mori and P. C. M. van Zijl, “Fiber tracking: principles and strategies - a technical review,” NMR Biomed. 15(7-8), 468–480 (2002).
[Crossref] [PubMed]

Villiger, M.

K. P. Quinn, A. Golberg, G. F. Broelsch, S. Khan, M. Villiger, B. Bouma, W. G. Austen, R. L. Sheridan, M. C. Mihm, M. L. Yarmush, and I. Georgakoudi, “An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue,” Exp. Dermatol. 24(1), 78–80 (2015).
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L. Hong, Y. F. Wan, and A. Jain, “Fingerprint image enhancement: algorithm and performance evaluation,” IEEE T. Pattern Anal. 20(8), 777–789 (1998).

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A. Golberg, S. Khan, V. Belov, K. P. Quinn, H. Albadawi, G. F. Broelsch, M. T. Watkins, I. Georgakoudi, M. Papisov, M. C. Mihm, W. G. Austen, and M. L. Yarmush, “Skin rejuvenation with non-invasive pulsed elecdtric fields,” Sci. Rep. (to be published).

Wearne, S. L.

A. Rodriguez, D. B. Ehlenberger, P. R. Hof, and S. L. Wearne, “Three-dimensional neuron tracing by voxel scooping,” J. Neurosci. Methods 184(1), 169–175 (2009).
[PubMed]

Weinberger, B.

S. Thomopoulos, J. P. Marquez, B. Weinberger, V. Birman, and G. M. Genin, “Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations,” J. Biomech. 39(10), 1842–1851 (2006).
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H. J. Park, M. Kubicki, C. F. Westin, I. F. Talos, A. Brun, S. Peiper, R. Kikinis, F. A. Jolesz, R. W. McCarley, and M. E. Shenton, “Method for combining information from white matter fiber tracking and gray matter parcellation,” AJNR Am. J. Neuroradiol. 25(8), 1318–1324 (2004).
[PubMed]

White, J. G.

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
[Crossref] [PubMed]

Whitt, G. S.

L. Speroni, G. S. Whitt, J. Xylas, K. P. Quinn, A. Jondeau-Cabaton, C. Barnes, I. Georgakoudi, C. Sonnenschein, and A. M. Soto, “Hormonal regulation of epithelial organization in a 3D breast tissue culture model,” Tissue Eng. Part C Methods 20(1), 42–51 (2014).
[Crossref] [PubMed]

Wu, J.

J. Wu, B. Rajwa, D. L. Filmer, C. M. Hoffmann, B. Yuan, C. S. Chiang, J. Sturgis, and J. P. Robinson, “Analysis of orientations of collagen fibers by novel fiber-tracking software,” Microsc. Microanal. 9(6), 574–580 (2003).
[Crossref] [PubMed]

Xylas, J.

L. Speroni, G. S. Whitt, J. Xylas, K. P. Quinn, A. Jondeau-Cabaton, C. Barnes, I. Georgakoudi, C. Sonnenschein, and A. M. Soto, “Hormonal regulation of epithelial organization in a 3D breast tissue culture model,” Tissue Eng. Part C Methods 20(1), 42–51 (2014).
[Crossref] [PubMed]

Yamada, N.

N. Morishige, N. Yamada, S. Teranishi, T. Chikama, T. Nishida, and A. Takahara, “Detection of subepithelial fibrosis associated with corneal stromal edema by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci. 50(7), 3145–3150 (2009).
[PubMed]

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. C. 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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Figures (12)

Fig. 1
Fig. 1 Schematic of the angle definition in this study. (a) Basic angles defined for orientation calculation and error assessment. (b) Angles defined to reveal the case of varied axial-to-lateral sampling ratio.
Fig. 2
Fig. 2 Summary of 3D weighted orientation vector summation technique for voxel-wise fiber orientation detection. (a) 3D reconstruction of the test image stack. (b) One single frame in the x y plane. (c) The same frame as (b) but with neighboring frames averaged. (d) One averaged frame in the y z plane. (e) One averaged frame in the z x plane. (f) An analysis window with all the orientation vectors. (g) Vectors modified by weight factor 1 ( W 1 ). (h) Vectors modified by weight factor 2 ( W 2 ). (i) Vectors modified by combining weight factors 1 and 2. (j) The orientation of the center pixel calculated by summation of all the weighted orientation vectors.
Fig. 3
Fig. 3 Errors of (a) θ , (b) φ and (c) δ in fiber orientation measurements with respect to different fiber thickness and window size. (d) Error of δ with respect to different fiber density and window size. (e) 3D reconstruction of stacks with different fiber thickness. (f) 3D reconstruction of stacks with different fiber density.
Fig. 4
Fig. 4 Error in orientation detection using the 3D vector summation technique for a simulated image stack containing regions with varying orientations. (a) Errors of θ and φ , and the overall angle error δ in fiber orientation measurements with respect to different window size. 3D reconstructions of (b) intensity, (c) θ , and (d) φ map stacks. 3D reconstructions of δ with a window size of (e) 7 × 7 × 7 voxels, (f) 11 × 11 × 11 voxels and (g) 15 × 15 × 15 voxels. The insets in (f) and (g) zoom in the same region in the image stack.
Fig. 5
Fig. 5 Errors of θ , φ and δ in fiber orientation measurements with respect to different axial-to-lateral sampling ratio and window size. Insets show voxel size during calculation.
Fig. 6
Fig. 6 Errors of θ , φ and δ in fiber orientation measurements with respect to different (a) φ and (b) θ range, corresponding to a window of 13 × 13 × 13 voxels.
Fig. 7
Fig. 7 Computational time of this 3D technique with respect to different image and window sizes. Inset zooms in the region with large image sizes.
Fig. 8
Fig. 8 Error in orientation detection for simulated dense stacks. (a) A dense stack with 334 fibers with different fiber diameter and length, but uniform signal intensity. (b) The same stack as in (a), but variant signal intensity. (c) and (d) The δ error maps corresponding to (a) and (b), respectively, achieved by a window of 11 × 11 × 11 voxels. (e) Errors of δ , corresponding to the uniform and variant intensity stacks, with respect to different window size.
Fig. 9
Fig. 9 Error in orientation detection for simulated spiral stacks. (a) and (b) 3D reconstructions of θ and φ maps of the spiral fiber stack, respectively. Insets show top-view images. (c) Errors of θ and φ , and the overall angle error δ in spiral fiber orientation measurements with respect to different window size.
Fig. 10
Fig. 10 A comparison between 2D and 3D techniques. (a) 3D reconstruction of the 8 test stacks. (b) Schematic of the frame-by-frame manner of 2D analysis. Only the top 10 frames are zoomed in here for illustration. (c) Histograms showing the error of the mean θ determination. *, significant difference.
Fig. 11
Fig. 11 Orientation analysis of fibers from the mammary gland sample. (a) Combined fluorescence (red) and SHG (green) image. Scale bar: 100 μm. (b) The 3D stack of the marked region in (a). Scale bar: 50 μm. (c) One frame of the θ orientation map from the 3D stack, calculated by the 3D algorithm. Scale bar: 50 μm. The two regions shown in (c) are zoomed in to show the details of fiber orientation. (d) Original SHG intensity of region 1. (e) θ orientation map of region 1. Scale bar: 30 μm. The arrows shown in (d) and (e) point out the branched structure. (f) Original SHG intensity of region 2. (g) θ orientation map of region 2. Scale bar: 15 μm. (h) The distribution histogram of θ corresponding to this frame.
Fig. 12
Fig. 12 Applicability of the 3D vector summation technique to the analysis of an image stack from a 3D breast tissue model. 3D reconstructions of (a) a combination of SHG and TPEF signals, (b) θ and (c) φ orientation maps. (d), (e), and (f) show one frame of these stacks. (h) The two regions surrounding the epithelial structures marked in yellow are investigated, and the distribution histograms of both θ and φ within these two regions are shown in (g) and (i), respectively, as pointed by the arrows.

Equations (3)

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tan 2 φ = 1 tan 2 β + 1 tan 2 γ .
cos δ = sin φ d e f sin φ e x p cos ( Δ θ ) + cos φ d e f cos φ e x p ,
tan ( π / 2 φ t r u e ) = r tan ( π / 2 φ e x p ) ,

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