Abstract

Quantitative second harmonic generation microscopy was used to investigate collagen organization in the fibrillar capsules of human benign and malignant thyroid nodules. We demonstrate that the combination of texture analysis and second harmonic generation images of collagen can be used to differentiate between capsules surrounding the thyroid follicular adenoma and papillary carcinoma nodules. Our findings indicate that second harmonic generation microscopy can provide quantitative information about the collagenous capsule surrounding both the thyroid and thyroid nodules, which may complement traditional histopathological examination.

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

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  8. J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J. Biophotonics 7(1-2), 37–48 (2014).
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  17. A. Buttgereit, C. Weber, C. S. Garbe, and O. Friedrich, “From chaos to split-ups-SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle,” J. Pathol. 229(3), 477–485 (2013).
    [Crossref] [PubMed]
  18. P. Campagnola, “Second harmonic generation imaging microscopy: applications to diseases diagnostics,” Anal. Chem. 83(9), 3224–3231 (2011).
    [Crossref] [PubMed]
  19. S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  22. A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  24. Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
    [Crossref] [PubMed]
  25. L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
    [Crossref] [PubMed]
  26. N. D. Kirkpatrick, M. A. Brewer, and U. Utzinger, “Endogenous optical biomarkers of ovarian cancer evaluated with multiphoton microscopy,” Cancer Epidemiol. Biomarkers Prev. 16(10), 2048–2057 (2007).
    [Crossref] [PubMed]
  27. F. J. Ávila and J. M. Bueno, “Analysis and quantification of collagen organization with the structure tensor in second harmonic microscopy images of ocular tissues,” Appl. Opt. 54(33), 9848–9854 (2015).
    [Crossref] [PubMed]
  28. K. E. Frisch, S. E. Duenwald-Kuehl, H. Kobayashi, C. S. Chamberlain, R. S. Lakes, and R. Vanderby., “Quantification of collagen organization using fractal dimensions and Fourier transforms,” Acta Histochem. 114(2), 140–144 (2012).
    [Crossref] [PubMed]
  29. S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
    [Crossref] [PubMed]
  30. S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
    [Crossref] [PubMed]
  31. S. G. Stanciu, F. J. Ávila, R. Hristu, and J. M. Bueno, “A study on image quality in polarization-resolved second harmonic generation microscopy,” Sci. Rep. 7(1), 15476 (2017).
    [Crossref] [PubMed]
  32. C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
    [Crossref] [PubMed]
  33. M. Strupler, A. M. Pena, M. Hernest, P. L. Tharaux, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express 15(7), 4054–4065 (2007).
    [Crossref] [PubMed]
  34. J. Adur, H. F. Carvalho, C. L. Cesar, and V. H. Casco, “Nonlinear optical microscopy signal processing strategies in cancer,” Cancer Inform. 13, 67–76 (2014).
    [Crossref] [PubMed]
  35. I. Pantic, S. Pantic, and G. Basta-Jovanovic, “Gray level co-occurrence matrix texture analysis of germinal center light zone lymphocyte nuclei: physiology viewpoint with focus on apoptosis,” Microsc. Microanal. 18(3), 470–475 (2012).
    [Crossref] [PubMed]
  36. M. J. Chow, R. Turcotte, C. P. Lin, and Y. Zhang, “Arterial extracellular matrix: a mechanobiological study of the contributions and interactions of elastin and collagen,” Biophys. J. 106(12), 2684–2692 (2014).
    [Crossref] [PubMed]
  37. 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]
  38. R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
    [Crossref] [PubMed]
  39. V. Kumar and P. Gupta P, “Importance of statistical measures in digital image processing,” Int. J. Emerg. Technol. Adv. Eng. 2(8), 56–62 (2012).
  40. K. Klein, T. Maier, V. C. Hirschfeld-Warneken, and J. P. Spatz, “Marker-free phenotyping of tumor cells by fractal analysis of reflection interference contrast microscopy images,” Nano Lett. 13(11), 5474–5479 (2013).
    [Crossref] [PubMed]
  41. H. Bao, A. Boussioutas, R. Jeremy, S. Russell, and M. Gu, “Second harmonic generation imaging via nonlinear endomicroscopy,” Opt. Express 18(2), 1255–1260 (2010).
    [Crossref] [PubMed]

2017 (2)

R. Hristu, S. G. Stanciu, D. E. Tranca, and G. A. Stanciu, “Improved quantification of collagen anisotropy with polarization-resolved second harmonic generation microscopy,” J. Biophotonics 10(9), 1171–1179 (2017).
[Crossref] [PubMed]

S. G. Stanciu, F. J. Ávila, R. Hristu, and J. M. Bueno, “A study on image quality in polarization-resolved second harmonic generation microscopy,” Sci. Rep. 7(1), 15476 (2017).
[Crossref] [PubMed]

2016 (3)

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref] [PubMed]

S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
[Crossref] [PubMed]

A. Golaraei, L. Kontenis, R. Cisek, D. Tokarz, S. J. Done, B. C. Wilson, and V. Barzda, “Changes of collagen ultrastructure in breast cancer tissue determined by second-harmonic generation double Stokes-Mueller polarimetric microscopy,” Biomed. Opt. Express 7(10), 4054–4068 (2016).
[Crossref] [PubMed]

2015 (4)

D. Tokarz, R. Cisek, A. Golaraei, S. L. Asa, V. Barzda, and B. C. Wilson, “Ultrastructural features of collagen in thyroid carcinoma tissue observed by polarization second harmonic generation microscopy,” Biomed. Opt. Express 6(9), 3475–3481 (2015).
[Crossref] [PubMed]

S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
[Crossref] [PubMed]

Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
[Crossref] [PubMed]

F. J. Ávila and J. M. Bueno, “Analysis and quantification of collagen organization with the structure tensor in second harmonic microscopy images of ocular tissues,” Appl. Opt. 54(33), 9848–9854 (2015).
[Crossref] [PubMed]

2014 (4)

J. Adur, H. F. Carvalho, C. L. Cesar, and V. H. Casco, “Nonlinear optical microscopy signal processing strategies in cancer,” Cancer Inform. 13, 67–76 (2014).
[Crossref] [PubMed]

M. J. Chow, R. Turcotte, C. P. Lin, and Y. Zhang, “Arterial extracellular matrix: a mechanobiological study of the contributions and interactions of elastin and collagen,” Biophys. J. 106(12), 2684–2692 (2014).
[Crossref] [PubMed]

J. W. Birk, M. Tadros, K. Moezardalan, O. Nadyarnykh, F. Forouhar, J. Anderson, and P. Campagnola, “Second harmonic generation imaging distinguishes both high-grade dysplasia and cancer from normal colonic mucosa,” Dig. Dis. Sci. 59(7), 1529–1534 (2014).
[Crossref] [PubMed]

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J. Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

2013 (5)

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J. Biophotonics 6(2), 129–142 (2013).
[Crossref] [PubMed]

A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
[Crossref] [PubMed]

A. Buttgereit, C. Weber, C. S. Garbe, and O. Friedrich, “From chaos to split-ups-SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle,” J. Pathol. 229(3), 477–485 (2013).
[Crossref] [PubMed]

K. Klein, T. Maier, V. C. Hirschfeld-Warneken, and J. P. Spatz, “Marker-free phenotyping of tumor cells by fractal analysis of reflection interference contrast microscopy images,” Nano Lett. 13(11), 5474–5479 (2013).
[Crossref] [PubMed]

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
[Crossref] [PubMed]

2012 (5)

K. E. Frisch, S. E. Duenwald-Kuehl, H. Kobayashi, C. S. Chamberlain, R. S. Lakes, and R. Vanderby., “Quantification of collagen organization using fractal dimensions and Fourier transforms,” Acta Histochem. 114(2), 140–144 (2012).
[Crossref] [PubMed]

I. Pantic, S. Pantic, and G. Basta-Jovanovic, “Gray level co-occurrence matrix texture analysis of germinal center light zone lymphocyte nuclei: physiology viewpoint with focus on apoptosis,” Microsc. Microanal. 18(3), 470–475 (2012).
[Crossref] [PubMed]

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

V. Kumar and P. Gupta P, “Importance of statistical measures in digital image processing,” Int. J. Emerg. Technol. Adv. Eng. 2(8), 56–62 (2012).

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
[Crossref] [PubMed]

2011 (1)

P. Campagnola, “Second harmonic generation imaging microscopy: applications to diseases diagnostics,” Anal. Chem. 83(9), 3224–3231 (2011).
[Crossref] [PubMed]

2010 (3)

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics 3(1-2), 34–43 (2010).
[Crossref] [PubMed]

Z. Huang, Z. Li, R. Chen, J. Lin, Y. Li, and C. Li, “In vitro imaging of thyroid tissues using two-photon excited fluorescence and second harmonic generation,” Photomed. Laser Surg. 28(S1), S129–S133 (2010).
[Crossref] [PubMed]

H. Bao, A. Boussioutas, R. Jeremy, S. Russell, and M. Gu, “Second harmonic generation imaging via nonlinear endomicroscopy,” Opt. Express 18(2), 1255–1260 (2010).
[Crossref] [PubMed]

2009 (2)

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] [PubMed]

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
[Crossref] [PubMed]

2008 (2)

A. C. Kwan, D. A. Dombeck, and W. W. Webb, “Polarized microtubule arrays in apical dendrites and axons,” Proc. Natl. Acad. Sci. U.S.A. 105(32), 11370–11375 (2008).
[Crossref] [PubMed]

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
[Crossref] [PubMed]

2007 (2)

N. D. Kirkpatrick, M. A. Brewer, and U. Utzinger, “Endogenous optical biomarkers of ovarian cancer evaluated with multiphoton microscopy,” Cancer Epidemiol. Biomarkers Prev. 16(10), 2048–2057 (2007).
[Crossref] [PubMed]

M. Strupler, A. M. Pena, M. Hernest, P. L. Tharaux, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express 15(7), 4054–4065 (2007).
[Crossref] [PubMed]

2006 (1)

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)

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[Crossref] [PubMed]

2003 (2)

W. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods 29(1), 97–109 (2003).
[Crossref] [PubMed]

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

2001 (1)

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
[Crossref] [PubMed]

Adams, D. J.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
[Crossref] [PubMed]

Adur, J.

J. Adur, H. F. Carvalho, C. L. Cesar, and V. H. Casco, “Nonlinear optical microscopy signal processing strategies in cancer,” Cancer Inform. 13, 67–76 (2014).
[Crossref] [PubMed]

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J. Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

Anderson, J.

J. W. Birk, M. Tadros, K. Moezardalan, O. Nadyarnykh, F. Forouhar, J. Anderson, and P. Campagnola, “Second harmonic generation imaging distinguishes both high-grade dysplasia and cancer from normal colonic mucosa,” Dig. Dis. Sci. 59(7), 1529–1534 (2014).
[Crossref] [PubMed]

Andrade, L. A.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J. Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

Asa, S. L.

Ávila, F. J.

S. G. Stanciu, F. J. Ávila, R. Hristu, and J. M. Bueno, “A study on image quality in polarization-resolved second harmonic generation microscopy,” Sci. Rep. 7(1), 15476 (2017).
[Crossref] [PubMed]

F. J. Ávila and J. M. Bueno, “Analysis and quantification of collagen organization with the structure tensor in second harmonic microscopy images of ocular tissues,” Appl. Opt. 54(33), 9848–9854 (2015).
[Crossref] [PubMed]

Bao, H.

Baratti, M. O.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J. Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

Barzda, V.

Basta-Jovanovic, G.

I. Pantic, S. Pantic, and G. Basta-Jovanovic, “Gray level co-occurrence matrix texture analysis of germinal center light zone lymphocyte nuclei: physiology viewpoint with focus on apoptosis,” Microsc. Microanal. 18(3), 470–475 (2012).
[Crossref] [PubMed]

Beaurepaire, E.

Birk, J. W.

J. W. Birk, M. Tadros, K. Moezardalan, O. Nadyarnykh, F. Forouhar, J. Anderson, and P. Campagnola, “Second harmonic generation imaging distinguishes both high-grade dysplasia and cancer from normal colonic mucosa,” Dig. Dis. Sci. 59(7), 1529–1534 (2014).
[Crossref] [PubMed]

Bottcher-Luiz, F.

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N. D. Kirkpatrick, M. A. Brewer, and U. Utzinger, “Endogenous optical biomarkers of ovarian cancer evaluated with multiphoton microscopy,” Cancer Epidemiol. Biomarkers Prev. 16(10), 2048–2057 (2007).
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S. G. Stanciu, F. J. Ávila, R. Hristu, and J. M. Bueno, “A study on image quality in polarization-resolved second harmonic generation microscopy,” Sci. Rep. 7(1), 15476 (2017).
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F. J. Ávila and J. M. Bueno, “Analysis and quantification of collagen organization with the structure tensor in second harmonic microscopy images of ocular tissues,” Appl. Opt. 54(33), 9848–9854 (2015).
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A. Buttgereit, C. Weber, C. S. Garbe, and O. Friedrich, “From chaos to split-ups-SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle,” J. Pathol. 229(3), 477–485 (2013).
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Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
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J. W. Birk, M. Tadros, K. Moezardalan, O. Nadyarnykh, F. Forouhar, J. Anderson, and P. Campagnola, “Second harmonic generation imaging distinguishes both high-grade dysplasia and cancer from normal colonic mucosa,” Dig. Dis. Sci. 59(7), 1529–1534 (2014).
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X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
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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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J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J. Biophotonics 7(1-2), 37–48 (2014).
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J. Adur, H. F. Carvalho, C. L. Cesar, and V. H. Casco, “Nonlinear optical microscopy signal processing strategies in cancer,” Cancer Inform. 13, 67–76 (2014).
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K. E. Frisch, S. E. Duenwald-Kuehl, H. Kobayashi, C. S. Chamberlain, R. S. Lakes, and R. Vanderby., “Quantification of collagen organization using fractal dimensions and Fourier transforms,” Acta Histochem. 114(2), 140–144 (2012).
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Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
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Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
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Z. Huang, Z. Li, R. Chen, J. Lin, Y. Li, and C. Li, “In vitro imaging of thyroid tissues using two-photon excited fluorescence and second harmonic generation,” Photomed. Laser Surg. 28(S1), S129–S133 (2010).
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A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
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Chen, W. L.

A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
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Chen, X.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
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A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
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S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
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R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J. Biophotonics 6(2), 129–142 (2013).
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R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics 3(1-2), 34–43 (2010).
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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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Cisek, R.

Cooper, D. S.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
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S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
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De Giorgi, V.

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics 3(1-2), 34–43 (2010).
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J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J. Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

Dietzek, B.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J. Biophotonics 6(2), 129–142 (2013).
[Crossref] [PubMed]

Doherty, G. M.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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A. C. Kwan, D. A. Dombeck, and W. W. Webb, “Polarized microtubule arrays in apical dendrites and axons,” Proc. Natl. Acad. Sci. U.S.A. 105(32), 11370–11375 (2008).
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Dong, C. Y.

A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
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Dougherty, R. P.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
[Crossref] [PubMed]

Duenwald-Kuehl, S. E.

K. E. Frisch, S. E. Duenwald-Kuehl, H. Kobayashi, C. S. Chamberlain, R. S. Lakes, and R. Vanderby., “Quantification of collagen organization using fractal dimensions and Fourier transforms,” Acta Histochem. 114(2), 140–144 (2012).
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C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
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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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Feinmesser, R.

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
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Forouhar, F.

J. W. Birk, M. Tadros, K. Moezardalan, O. Nadyarnykh, F. Forouhar, J. Anderson, and P. Campagnola, “Second harmonic generation imaging distinguishes both high-grade dysplasia and cancer from normal colonic mucosa,” Dig. Dis. Sci. 59(7), 1529–1534 (2014).
[Crossref] [PubMed]

Friedrich, O.

A. Buttgereit, C. Weber, C. S. Garbe, and O. Friedrich, “From chaos to split-ups-SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle,” J. Pathol. 229(3), 477–485 (2013).
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Frisch, K. E.

K. E. Frisch, S. E. Duenwald-Kuehl, H. Kobayashi, C. S. Chamberlain, R. S. Lakes, and R. Vanderby., “Quantification of collagen organization using fractal dimensions and Fourier transforms,” Acta Histochem. 114(2), 140–144 (2012).
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Gal, R.

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
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Garbe, C. S.

A. Buttgereit, C. Weber, C. S. Garbe, and O. Friedrich, “From chaos to split-ups-SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle,” J. Pathol. 229(3), 477–485 (2013).
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A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
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Gou, X.

S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
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Grushko, I.

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
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V. Kumar and P. Gupta P, “Importance of statistical measures in digital image processing,” Int. J. Emerg. Technol. Adv. Eng. 2(8), 56–62 (2012).

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D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
[Crossref] [PubMed]

Hayrapetyan, G.

A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
[Crossref] [PubMed]

He, Y.

S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
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Hernest, M.

Hewko, M.

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
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Hirschfeld-Warneken, V. C.

K. Klein, T. Maier, V. C. Hirschfeld-Warneken, and J. P. Spatz, “Marker-free phenotyping of tumor cells by fractal analysis of reflection interference contrast microscopy images,” Nano Lett. 13(11), 5474–5479 (2013).
[Crossref] [PubMed]

Hristu, R.

S. G. Stanciu, F. J. Ávila, R. Hristu, and J. M. Bueno, “A study on image quality in polarization-resolved second harmonic generation microscopy,” Sci. Rep. 7(1), 15476 (2017).
[Crossref] [PubMed]

R. Hristu, S. G. Stanciu, D. E. Tranca, and G. A. Stanciu, “Improved quantification of collagen anisotropy with polarization-resolved second harmonic generation microscopy,” J. Biophotonics 10(9), 1171–1179 (2017).
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Huang, Z.

Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
[Crossref] [PubMed]

Z. Huang, Z. Li, R. Chen, J. Lin, Y. Li, and C. Li, “In vitro imaging of thyroid tissues using two-photon excited fluorescence and second harmonic generation,” Photomed. Laser Surg. 28(S1), S129–S133 (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]

Jeong, M. Y.

A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
[Crossref] [PubMed]

Jeremy, R.

Joseph, C.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
[Crossref] [PubMed]

Kang, C. H.

S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
[Crossref] [PubMed]

Kang, Y.

S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
[Crossref] [PubMed]

Kapsokalyvas, D.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J. Biophotonics 6(2), 129–142 (2013).
[Crossref] [PubMed]

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics 3(1-2), 34–43 (2010).
[Crossref] [PubMed]

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] [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]

Kenny, A. M.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
[Crossref] [PubMed]

Kim, C. S.

A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
[Crossref] [PubMed]

Kirkpatrick, N. D.

N. D. Kirkpatrick, M. A. Brewer, and U. Utzinger, “Endogenous optical biomarkers of ovarian cancer evaluated with multiphoton microscopy,” Cancer Epidemiol. Biomarkers Prev. 16(10), 2048–2057 (2007).
[Crossref] [PubMed]

Klein, K.

K. Klein, T. Maier, V. C. Hirschfeld-Warneken, and J. P. Spatz, “Marker-free phenotyping of tumor cells by fractal analysis of reflection interference contrast microscopy images,” Nano Lett. 13(11), 5474–5479 (2013).
[Crossref] [PubMed]

Kloos, R. T.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
[Crossref] [PubMed]

Ko, A. C. T.

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
[Crossref] [PubMed]

Kobayashi, H.

K. E. Frisch, S. E. Duenwald-Kuehl, H. Kobayashi, C. S. Chamberlain, R. S. Lakes, and R. Vanderby., “Quantification of collagen organization using fractal dimensions and Fourier transforms,” Acta Histochem. 114(2), 140–144 (2012).
[Crossref] [PubMed]

Kontenis, L.

Koren, R.

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
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Kristt, D.

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
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Kuchel, G. A.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
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V. Kumar and P. Gupta P, “Importance of statistical measures in digital image processing,” Int. J. Emerg. Technol. Adv. Eng. 2(8), 56–62 (2012).

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A. C. Kwan, D. A. Dombeck, and W. W. Webb, “Polarized microtubule arrays in apical dendrites and axons,” Proc. Natl. Acad. Sci. U.S.A. 105(32), 11370–11375 (2008).
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K. E. Frisch, S. E. Duenwald-Kuehl, H. Kobayashi, C. S. Chamberlain, R. S. Lakes, and R. Vanderby., “Quantification of collagen organization using fractal dimensions and Fourier transforms,” Acta Histochem. 114(2), 140–144 (2012).
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Lee, S. L.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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Z. Huang, Z. Li, R. Chen, J. Lin, Y. Li, and C. Li, “In vitro imaging of thyroid tissues using two-photon excited fluorescence and second harmonic generation,” Photomed. Laser Surg. 28(S1), S129–S133 (2010).
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Li, Y.

Z. Huang, Z. Li, R. Chen, J. Lin, Y. Li, and C. Li, “In vitro imaging of thyroid tissues using two-photon excited fluorescence and second harmonic generation,” Photomed. Laser Surg. 28(S1), S129–S133 (2010).
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Li, Z.

Z. Huang, Z. Li, R. Chen, J. Lin, Y. Li, and C. Li, “In vitro imaging of thyroid tissues using two-photon excited fluorescence and second harmonic generation,” Photomed. Laser Surg. 28(S1), S129–S133 (2010).
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Lin, C. P.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
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M. J. Chow, R. Turcotte, C. P. Lin, and Y. Zhang, “Arterial extracellular matrix: a mechanobiological study of the contributions and interactions of elastin and collagen,” Biophys. J. 106(12), 2684–2692 (2014).
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Lin, J.

Z. Huang, Z. Li, R. Chen, J. Lin, Y. Li, and C. Li, “In vitro imaging of thyroid tissues using two-photon excited fluorescence and second harmonic generation,” Photomed. Laser Surg. 28(S1), S129–S133 (2010).
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Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
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P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
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R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics 3(1-2), 34–43 (2010).
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Maier, T.

K. Klein, T. Maier, V. C. Hirschfeld-Warneken, and J. P. Spatz, “Marker-free phenotyping of tumor cells by fractal analysis of reflection interference contrast microscopy images,” Nano Lett. 13(11), 5474–5479 (2013).
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R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics 3(1-2), 34–43 (2010).
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Major, A.

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
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Mandel, S. J.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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Massi, D.

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics 3(1-2), 34–43 (2010).
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Matteini, P.

Mattson, J. M.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
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Mazzaferri, E. L.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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McIver, B.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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Millard, A. C.

W. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods 29(1), 97–109 (2003).
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Moezardalan, K.

J. W. Birk, M. Tadros, K. Moezardalan, O. Nadyarnykh, F. Forouhar, J. Anderson, and P. Campagnola, “Second harmonic generation imaging distinguishes both high-grade dysplasia and cancer from normal colonic mucosa,” Dig. Dis. Sci. 59(7), 1529–1534 (2014).
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Mohler, W.

W. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods 29(1), 97–109 (2003).
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Mohler, W. A.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
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Mostaço-Guidolin, L. B.

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
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Nadiarynkh, O.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
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Nadyarnykh, O.

J. W. Birk, M. Tadros, K. Moezardalan, O. Nadyarnykh, F. Forouhar, J. Anderson, and P. Campagnola, “Second harmonic generation imaging distinguishes both high-grade dysplasia and cancer from normal colonic mucosa,” Dig. Dis. Sci. 59(7), 1529–1534 (2014).
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Pacini, F.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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Pantic, S.

I. Pantic, S. Pantic, and G. Basta-Jovanovic, “Gray level co-occurrence matrix texture analysis of germinal center light zone lymphocyte nuclei: physiology viewpoint with focus on apoptosis,” Microsc. Microanal. 18(3), 470–475 (2012).
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Pavone, F. S.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J. Biophotonics 6(2), 129–142 (2013).
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R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics 3(1-2), 34–43 (2010).
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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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J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J. Biophotonics 7(1-2), 37–48 (2014).
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Pena, A. M.

Peng, Q.

S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
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S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
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S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
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Pini, R.

Plotnikov, S.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
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S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
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Popp, J.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J. Biophotonics 6(2), 129–142 (2013).
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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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S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
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C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
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Rossi, F.

Russell, S.

Schanne-Klein, M. C.

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D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
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S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
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Sherman, S. I.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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Shiomi, M.

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
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Shvero, J.

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
[Crossref] [PubMed]

So, P. T.

S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
[Crossref] [PubMed]

S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
[Crossref] [PubMed]

Sowa, M. G.

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
[Crossref] [PubMed]

Spatz, J. P.

K. Klein, T. Maier, V. C. Hirschfeld-Warneken, and J. P. Spatz, “Marker-free phenotyping of tumor cells by fractal analysis of reflection interference contrast microscopy images,” Nano Lett. 13(11), 5474–5479 (2013).
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Stanciu, G. A.

R. Hristu, S. G. Stanciu, D. E. Tranca, and G. A. Stanciu, “Improved quantification of collagen anisotropy with polarization-resolved second harmonic generation microscopy,” J. Biophotonics 10(9), 1171–1179 (2017).
[Crossref] [PubMed]

S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
[Crossref] [PubMed]

Stanciu, S. G.

R. Hristu, S. G. Stanciu, D. E. Tranca, and G. A. Stanciu, “Improved quantification of collagen anisotropy with polarization-resolved second harmonic generation microscopy,” J. Biophotonics 10(9), 1171–1179 (2017).
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S. G. Stanciu, F. J. Ávila, R. Hristu, and J. M. Bueno, “A study on image quality in polarization-resolved second harmonic generation microscopy,” Sci. Rep. 7(1), 15476 (2017).
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S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
[Crossref] [PubMed]

Steward, D. L.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
[Crossref] [PubMed]

Stringari, C.

Strupler, M.

Sulkes, J.

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
[Crossref] [PubMed]

Tadros, M.

J. W. Birk, M. Tadros, K. Moezardalan, O. Nadyarnykh, F. Forouhar, J. Anderson, and P. Campagnola, “Second harmonic generation imaging distinguishes both high-grade dysplasia and cancer from normal colonic mucosa,” Dig. Dis. Sci. 59(7), 1529–1534 (2014).
[Crossref] [PubMed]

Tharaux, P. L.

Tian, G.

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
[Crossref] [PubMed]

Tokarz, D.

Tranca, D. E.

R. Hristu, S. G. Stanciu, D. E. Tranca, and G. A. Stanciu, “Improved quantification of collagen anisotropy with polarization-resolved second harmonic generation microscopy,” J. Biophotonics 10(9), 1171–1179 (2017).
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Tsai, H. F.

A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
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Turcotte, R.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref] [PubMed]

M. J. Chow, R. Turcotte, C. P. Lin, and Y. Zhang, “Arterial extracellular matrix: a mechanobiological study of the contributions and interactions of elastin and collagen,” Biophys. J. 106(12), 2684–2692 (2014).
[Crossref] [PubMed]

Tuttle, R. M.

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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N. D. Kirkpatrick, M. A. Brewer, and U. Utzinger, “Endogenous optical biomarkers of ovarian cancer evaluated with multiphoton microscopy,” Cancer Epidemiol. Biomarkers Prev. 16(10), 2048–2057 (2007).
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Van Wiechen, A.

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics 3(1-2), 34–43 (2010).
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Vanderby, R.

K. E. Frisch, S. E. Duenwald-Kuehl, H. Kobayashi, C. S. Chamberlain, R. S. Lakes, and R. Vanderby., “Quantification of collagen organization using fractal dimensions and Fourier transforms,” Acta Histochem. 114(2), 140–144 (2012).
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Veltman, V.

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
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Vogler, N.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J. Biophotonics 6(2), 129–142 (2013).
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Walsh, S. J.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
[Crossref] [PubMed]

Wang, F.

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
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Webb, W. W.

A. C. Kwan, D. A. Dombeck, and W. W. Webb, “Polarized microtubule arrays in apical dendrites and axons,” Proc. Natl. Acad. Sci. U.S.A. 105(32), 11370–11375 (2008).
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Weber, C.

A. Buttgereit, C. Weber, C. S. Garbe, and O. Friedrich, “From chaos to split-ups-SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle,” J. Pathol. 229(3), 477–485 (2013).
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Welsch, R.

S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
[Crossref] [PubMed]

Welsch, R. E.

S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
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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]

Williams, R. M.

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[Crossref] [PubMed]

Wilson, B. C.

Wu, J. W.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref] [PubMed]

Xia, W.

S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
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Xiang, B.

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
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Xiong, S.

Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
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Xu, M.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
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S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
[Crossref] [PubMed]

S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
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Yan, J.

S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
[Crossref] [PubMed]

S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
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Yaniv, E.

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
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S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
[Crossref] [PubMed]

S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
[Crossref] [PubMed]

Zeng, H.

Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
[Crossref] [PubMed]

Zhang, Y.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref] [PubMed]

M. J. Chow, R. Turcotte, C. P. Lin, and Y. Zhang, “Arterial extracellular matrix: a mechanobiological study of the contributions and interactions of elastin and collagen,” Biophys. J. 106(12), 2684–2692 (2014).
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Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
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S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
[Crossref] [PubMed]

Zipfel, W. R.

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[Crossref] [PubMed]

Zubrowski, B.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
[Crossref] [PubMed]

Acta Histochem. (2)

R. Koren, E. Yaniv, D. Kristt, J. Shvero, V. Veltman, I. Grushko, R. Feinmesser, J. Sulkes, and R. Gal, “Capsular collagen staining of follicular thyroid neoplasms by picrosirius red: role in differential diagnosis,” Acta Histochem. 103(2), 151–157 (2001).
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K. E. Frisch, S. E. Duenwald-Kuehl, H. Kobayashi, C. S. Chamberlain, R. S. Lakes, and R. Vanderby., “Quantification of collagen organization using fractal dimensions and Fourier transforms,” Acta Histochem. 114(2), 140–144 (2012).
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Anal. Chem. (1)

P. Campagnola, “Second harmonic generation imaging microscopy: applications to diseases diagnostics,” Anal. Chem. 83(9), 3224–3231 (2011).
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Appl. Opt. (1)

Biomed. Opt. Express (2)

Biophys. J. (3)

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[Crossref] [PubMed]

M. J. Chow, R. Turcotte, C. P. Lin, and Y. Zhang, “Arterial extracellular matrix: a mechanobiological study of the contributions and interactions of elastin and collagen,” Biophys. J. 106(12), 2684–2692 (2014).
[Crossref] [PubMed]

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular order of arterial collagen using circular polarization second-harmonic generation imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref] [PubMed]

BMC Med. (1)

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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Cancer Epidemiol. Biomarkers Prev. (1)

N. D. Kirkpatrick, M. A. Brewer, and U. Utzinger, “Endogenous optical biomarkers of ovarian cancer evaluated with multiphoton microscopy,” Cancer Epidemiol. Biomarkers Prev. 16(10), 2048–2057 (2007).
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Cancer Inform. (1)

J. Adur, H. F. Carvalho, C. L. Cesar, and V. H. Casco, “Nonlinear optical microscopy signal processing strategies in cancer,” Cancer Inform. 13, 67–76 (2014).
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Dig. Dis. Sci. (1)

J. W. Birk, M. Tadros, K. Moezardalan, O. Nadyarnykh, F. Forouhar, J. Anderson, and P. Campagnola, “Second harmonic generation imaging distinguishes both high-grade dysplasia and cancer from normal colonic mucosa,” Dig. Dis. Sci. 59(7), 1529–1534 (2014).
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Int. J. Emerg. Technol. Adv. Eng. (1)

V. Kumar and P. Gupta P, “Importance of statistical measures in digital image processing,” Int. J. Emerg. Technol. Adv. Eng. 2(8), 56–62 (2012).

J. Biomed. Opt. (3)

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
[Crossref] [PubMed]

A. Ghazaryan, H. F. Tsai, G. Hayrapetyan, W. L. Chen, Y. F. Chen, M. Y. Jeong, C. S. Kim, S. J. Chen, and C. Y. Dong, “Analysis of collagen fiber domain organization by Fourier second harmonic generation microscopy,” J. Biomed. Opt. 18(3), 031105 (2013).
[Crossref] [PubMed]

Y. Liu, X. Zhu, Z. Huang, J. Cai, R. Chen, S. Xiong, G. Chen, and H. Zeng, “Texture analysis of collagen second-harmonic generation images based on local difference local binary pattern and wavelets differentiates human skin abnormal scars from normal scars,” J. Biomed. Opt. 20(1), 016021 (2015).
[Crossref] [PubMed]

J. Biophotonics (5)

R. Hristu, S. G. Stanciu, D. E. Tranca, and G. A. Stanciu, “Improved quantification of collagen anisotropy with polarization-resolved second harmonic generation microscopy,” J. Biophotonics 10(9), 1171–1179 (2017).
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S. Xu, C. H. Kang, X. Gou, Q. Peng, J. Yan, S. Zhuo, C. L. Cheng, Y. He, Y. Kang, W. Xia, P. T. So, R. Welsch, J. C. Rajapakse, and H. Yu, “Quantification of liver fibrosis via second harmonic imaging of the Glisson’s capsule from liver surface,” J. Biophotonics 9(4), 351–363 (2016).
[Crossref] [PubMed]

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J. Biophotonics 7(1-2), 37–48 (2014).
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R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, “From molecular structure to tissue architecture: collagen organization probed by SHG microscopy,” J. Biophotonics 6(2), 129–142 (2013).
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R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics 3(1-2), 34–43 (2010).
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J. Pathol. (1)

A. Buttgereit, C. Weber, C. S. Garbe, and O. Friedrich, “From chaos to split-ups-SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle,” J. Pathol. 229(3), 477–485 (2013).
[Crossref] [PubMed]

Methods (1)

W. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods 29(1), 97–109 (2003).
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Microsc. Microanal. (1)

I. Pantic, S. Pantic, and G. Basta-Jovanovic, “Gray level co-occurrence matrix texture analysis of germinal center light zone lymphocyte nuclei: physiology viewpoint with focus on apoptosis,” Microsc. Microanal. 18(3), 470–475 (2012).
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Nano Lett. (1)

K. Klein, T. Maier, V. C. Hirschfeld-Warneken, and J. P. Spatz, “Marker-free phenotyping of tumor cells by fractal analysis of reflection interference contrast microscopy images,” Nano Lett. 13(11), 5474–5479 (2013).
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Nat. Biotechnol. (1)

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

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
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Nat. Protoc. (1)

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
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Opt. Express (3)

Photomed. Laser Surg. (1)

Z. Huang, Z. Li, R. Chen, J. Lin, Y. Li, and C. Li, “In vitro imaging of thyroid tissues using two-photon excited fluorescence and second harmonic generation,” Photomed. Laser Surg. 28(S1), S129–S133 (2010).
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Proc. Natl. Acad. Sci. U.S.A. (1)

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Sci. Rep. (3)

S. G. Stanciu, S. Xu, Q. Peng, J. Yan, G. A. Stanciu, R. E. Welsch, P. T. So, G. Csucs, and H. Yu, “Experimenting liver fibrosis diagnostic by two photon excitation microscopy and Bag-of-Features image classification,” Sci. Rep. 4(1), 4636 (2015).
[Crossref] [PubMed]

L. B. Mostaço-Guidolin, A. C. T. Ko, F. Wang, B. Xiang, M. Hewko, G. Tian, A. Major, M. Shiomi, and M. G. Sowa, “Collagen morphology and texture analysis: from statistics to classification,” Sci. Rep. 3(1), 2190 (2013).
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S. G. Stanciu, F. J. Ávila, R. Hristu, and J. M. Bueno, “A study on image quality in polarization-resolved second harmonic generation microscopy,” Sci. Rep. 7(1), 15476 (2017).
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Thyroid (1)

D. S. Cooper, G. M. Doherty, B. R. Haugen, R. T. Kloos, S. L. Lee, S. J. Mandel, E. L. Mazzaferri, B. McIver, F. Pacini, M. Schlumberger, S. I. Sherman, D. L. Steward, and R. M. Tuttle, “Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer,” Thyroid 19(11), 1167–1214 (2009).
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M. L. Carcangiu, “Thyroid,” in Histology for Pathologists, S. E. Mills, ed. (Lippincott Williams & Wilkins, 2012).

R. V. Lloyd, R. Y. Osamura, G. Kloppel, and J. Rosai, WHO Classification of Tumours of Endocrine Organs (International Agency for Research on Cancer, 2017).

L. L. Y. Tse and J. K. C. Chan, “Thyroid and Parathyroid,” in Modern Surgical Pathology, N. Weidner, R. J. Cote, S. Suster, L. M. Weiss, eds. (Expert Consult, 2009).

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Figures (4)

Fig. 1
Fig. 1 Traditional H&E histopathology (upper row) images acquired with a 20X objective and SHG microscopy images (lower row) for representative areas for the thyroid capsule, a thyroid follicular adenoma and a capsule surrounding a PTC nodule.
Fig. 2
Fig. 2 Parameters computed from SHG image sets for the three investigated capsules. The vertical error bars represent the 95% confidence intervals. Under each parameter the value with which they were normalized is shown. *p<0.05, **p<0.005, ***p<0.0005 are the p-values for the difference between two compared groups.
Fig. 3
Fig. 3 Selected parameters distributions computed from the 32 x 32 pixels SHG image sets for the three investigated capsules. The black curves represent fitting Gaussians with their mean (m) and standard deviation (s) being given in the inset of each graph. A maximum of three Gaussians were fitted to each parameter distribution and the case with the maximum coefficient of determination (R2 is also given in the inset) is shown.
Fig. 4
Fig. 4 Correlation decay rate with the pixel distance for the three types of capsules. The inset displays the decay rate for the three correlation curves with the error bars representing the 95% confidence intervals.

Tables (1)

Tables Icon

Table 1 Parameters used for the texture analysis of capsular collagen in SHG images.

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