Abstract

Collagen fiber alignment derived from second harmonic generation (SHG) microscopy images can be important for disease diagnostics. Image processing algorithms are needed to robustly quantify the alignment in images with high sensitivity and reliability. Fourier transform (FT) magnitude, 2D power spectrum, and image autocorrelation have previously been used to extract fiber information from images by assuming a certain mathematical model (e.g. Gaussian distribution of the fiber-related parameters) and fitting. The fitting process is slow and fails to converge when the data is not Gaussian. Herein we present an efficient constant-time deterministic algorithm which characterizes the symmetricity of the FT magnitude image in terms of a single parameter, named the fiber alignment anisotropy R ranging from 0 (randomized fibers) to 1 (perfect alignment). This represents an important improvement of the technology and may bring us one step closer to utilizing the technology for various applications in real time. In addition, we present a digital image phantom-based framework for characterizing and validating the algorithm, as well as assessing the robustness of the algorithm against different perturbations.

© 2017 Optical Society of America

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2017 (1)

W. Liang, G. Hall, B. Messerschmidt, M.-J. Li, and X. D. Li, “Nonlinear optical endomicroscopy for label-free functional histology in vivo,” Light: Sci. Appl. 6, e17082 (2017).

2014 (2)

B. L. Wen, M. A. Brewer, O. Nadiarnykh, J. Hocker, V. Singh, T. R. Mackie, and P. J. Campagnola, “Texture analysis applied to second harmonic generation image data for ovarian cancer classification,” J. Biomed. Opt. 19(9), 096007 (2014).
[Crossref] [PubMed]

J. S. Bredfeldt, Y. Liu, M. W. Conklin, P. J. Keely, T. R. Mackie, and K. W. Eliceiri, “Automated quantification of aligned collagen for human breast carcinoma prognosis,” J. Pathol. Inform. 5(1), 28 (2014).
[Crossref] [PubMed]

2012 (6)

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]

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 (2012).
[Crossref] [PubMed]

R. Ambekar, M. Chittenden, I. Jasiuk, and K. C. Toussaint., “Quantitative second-harmonic generation microscopy for imaging porcine cortical bone: Comparison to SEM and its potential to investigate age-related changes,” Bone 50(3), 643–650 (2012).
[Crossref] [PubMed]

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. U.S.A. 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

S. M. Kakkad, M. Solaiyappan, P. Argani, S. Sukumar, L. K. Jacobs, D. Leibfritz, Z. M. Bhujwalla, and K. Glunde, “Collagen I fiber density increases in lymph node positive breast cancers: pilot study,” J. Biomed. Opt. 17(11), 116017 (2012).
[Crossref] [PubMed]

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 (2)

K. Murari, Y. Zhang, S. Li, Y. Chen, M.-J. Li, and X. D. Li, “Compensation-free, all-fiber-optic, two-photon endomicroscopy at 1.55 μm,” Opt. Lett. 36, 1299–1301 (2011).

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

2010 (3)

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

R. M. Williams, A. Flesken-Nikitin, L. H. Ellenson, D. C. Connolly, T. C. Hamilton, A. Y. Nikitin, and W. R. Zipfel, “Strategies for High-Resolution Imaging of Epithelial Ovarian Cancer by Laparoscopic Nonlinear Microscopy,” Transl. Oncol. 3(3), 181–194 (2010).
[Crossref] [PubMed]

M. L. Akins, K. Luby-Phelps, and M. Mahendroo, “Second harmonic generation imaging as a potential tool for staging pregnancy and predicting preterm birth,” J. Biomed. Opt. 15(2), 026020 (2010).
[Crossref] [PubMed]

2009 (2)

2008 (2)

C. B. Raub, J. Unruh, V. Suresh, T. Krasieva, T. Lindmo, E. Gratton, B. J. Tromberg, and S. C. George, “Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties,” Biophys. J. 94(6), 2361–2373 (2008).
[Crossref] [PubMed]

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[Crossref] [PubMed]

2007 (2)

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]

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref] [PubMed]

2006 (2)

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]

M. T. Myaing, D. J. MacDonald, and X. Li, “Fiber-optic scanning two-photon fluorescence endoscope,” Opt. Lett. 31(8), 1076–1078 (2006).
[Crossref] [PubMed]

2005 (1)

T. M. Lehmann, M. O. Güld, T. Deselaers, D. Keysers, H. Schubert, K. Spitzer, H. Ney, and B. B. Wein, “Automatic categorization of medical images for content-based retrieval and data mining,” Comput. Med. Imaging Graph. 29(2-3), 143–155 (2005).
[Crossref] [PubMed]

2003 (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).
[Crossref] [PubMed]

Akins, M. L.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. U.S.A. 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

M. L. Akins, K. Luby-Phelps, and M. Mahendroo, “Second harmonic generation imaging as a potential tool for staging pregnancy and predicting preterm birth,” J. Biomed. Opt. 15(2), 026020 (2010).
[Crossref] [PubMed]

Ambekar, R.

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]

R. Ambekar, M. Chittenden, I. Jasiuk, and K. C. Toussaint., “Quantitative second-harmonic generation microscopy for imaging porcine cortical bone: Comparison to SEM and its potential to investigate age-related changes,” Bone 50(3), 643–650 (2012).
[Crossref] [PubMed]

Argani, P.

S. M. Kakkad, M. Solaiyappan, P. Argani, S. Sukumar, L. K. Jacobs, D. Leibfritz, Z. M. Bhujwalla, and K. Glunde, “Collagen I fiber density increases in lymph node positive breast cancers: pilot study,” J. Biomed. Opt. 17(11), 116017 (2012).
[Crossref] [PubMed]

Beaurepaire, E.

Bhujwalla, Z. M.

S. M. Kakkad, M. Solaiyappan, P. Argani, S. Sukumar, L. K. Jacobs, D. Leibfritz, Z. M. Bhujwalla, and K. Glunde, “Collagen I fiber density increases in lymph node positive breast cancers: pilot study,” J. Biomed. Opt. 17(11), 116017 (2012).
[Crossref] [PubMed]

Bredfeldt, J. S.

J. S. Bredfeldt, Y. Liu, M. W. Conklin, P. J. Keely, T. R. Mackie, and K. W. Eliceiri, “Automated quantification of aligned collagen for human breast carcinoma prognosis,” J. Pathol. Inform. 5(1), 28 (2014).
[Crossref] [PubMed]

Brewer, M. A.

B. L. Wen, M. A. Brewer, O. Nadiarnykh, J. Hocker, V. Singh, T. R. Mackie, and P. J. Campagnola, “Texture analysis applied to second harmonic generation image data for ovarian cancer classification,” J. Biomed. Opt. 19(9), 096007 (2014).
[Crossref] [PubMed]

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

Campagnola, P. J.

B. L. Wen, M. A. Brewer, O. Nadiarnykh, J. Hocker, V. Singh, T. R. Mackie, and P. J. Campagnola, “Texture analysis applied to second harmonic generation image data for ovarian cancer classification,” J. Biomed. Opt. 19(9), 096007 (2014).
[Crossref] [PubMed]

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]

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[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]

Campbell, J. M.

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]

Chen, S.-J.

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 (2012).
[Crossref] [PubMed]

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 (2012).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Chen, Y.

Chen, Y.-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 (2012).
[Crossref] [PubMed]

Chittenden, M.

R. Ambekar, M. Chittenden, I. Jasiuk, and K. C. Toussaint., “Quantitative second-harmonic generation microscopy for imaging porcine cortical bone: Comparison to SEM and its potential to investigate age-related changes,” Bone 50(3), 643–650 (2012).
[Crossref] [PubMed]

Cobb, M. J.

Conklin, M. W.

J. S. Bredfeldt, Y. Liu, M. W. Conklin, P. J. Keely, T. R. Mackie, and K. W. Eliceiri, “Automated quantification of aligned collagen for human breast carcinoma prognosis,” J. Pathol. Inform. 5(1), 28 (2014).
[Crossref] [PubMed]

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

Connolly, D. C.

R. M. Williams, A. Flesken-Nikitin, L. H. Ellenson, D. C. Connolly, T. C. Hamilton, A. Y. Nikitin, and W. R. Zipfel, “Strategies for High-Resolution Imaging of Epithelial Ovarian Cancer by Laparoscopic Nonlinear Microscopy,” Transl. Oncol. 3(3), 181–194 (2010).
[Crossref] [PubMed]

Deselaers, T.

T. M. Lehmann, M. O. Güld, T. Deselaers, D. Keysers, H. Schubert, K. Spitzer, H. Ney, and B. B. Wein, “Automatic categorization of medical images for content-based retrieval and data mining,” Comput. Med. Imaging Graph. 29(2-3), 143–155 (2005).
[Crossref] [PubMed]

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 (2012).
[Crossref] [PubMed]

Eickhoff, J. C.

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

Eliceiri, K. W.

J. S. Bredfeldt, Y. Liu, M. W. Conklin, P. J. Keely, T. R. Mackie, and K. W. Eliceiri, “Automated quantification of aligned collagen for human breast carcinoma prognosis,” J. Pathol. Inform. 5(1), 28 (2014).
[Crossref] [PubMed]

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[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]

Ellenson, L. H.

R. M. Williams, A. Flesken-Nikitin, L. H. Ellenson, D. C. Connolly, T. C. Hamilton, A. Y. Nikitin, and W. R. Zipfel, “Strategies for High-Resolution Imaging of Epithelial Ovarian Cancer by Laparoscopic Nonlinear Microscopy,” Transl. Oncol. 3(3), 181–194 (2010).
[Crossref] [PubMed]

Flesken-Nikitin, A.

R. M. Williams, A. Flesken-Nikitin, L. H. Ellenson, D. C. Connolly, T. C. Hamilton, A. Y. Nikitin, and W. R. Zipfel, “Strategies for High-Resolution Imaging of Epithelial Ovarian Cancer by Laparoscopic Nonlinear Microscopy,” Transl. Oncol. 3(3), 181–194 (2010).
[Crossref] [PubMed]

Friedl, A.

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

George, S. C.

C. B. Raub, J. Unruh, V. Suresh, T. Krasieva, T. Lindmo, E. Gratton, B. J. Tromberg, and S. C. George, “Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties,” Biophys. J. 94(6), 2361–2373 (2008).
[Crossref] [PubMed]

Ghazaryan, A.

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 (2012).
[Crossref] [PubMed]

Glunde, K.

S. M. Kakkad, M. Solaiyappan, P. Argani, S. Sukumar, L. K. Jacobs, D. Leibfritz, Z. M. Bhujwalla, and K. Glunde, “Collagen I fiber density increases in lymph node positive breast cancers: pilot study,” J. Biomed. Opt. 17(11), 116017 (2012).
[Crossref] [PubMed]

Gratton, E.

C. B. Raub, J. Unruh, V. Suresh, T. Krasieva, T. Lindmo, E. Gratton, B. J. Tromberg, and S. C. George, “Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties,” Biophys. J. 94(6), 2361–2373 (2008).
[Crossref] [PubMed]

Güld, M. O.

T. M. Lehmann, M. O. Güld, T. Deselaers, D. Keysers, H. Schubert, K. Spitzer, H. Ney, and B. B. Wein, “Automatic categorization of medical images for content-based retrieval and data mining,” Comput. Med. Imaging Graph. 29(2-3), 143–155 (2005).
[Crossref] [PubMed]

Hall, G.

W. Liang, G. Hall, B. Messerschmidt, M.-J. Li, and X. D. Li, “Nonlinear optical endomicroscopy for label-free functional histology in vivo,” Light: Sci. Appl. 6, e17082 (2017).

Hamilton, T. C.

R. M. Williams, A. Flesken-Nikitin, L. H. Ellenson, D. C. Connolly, T. C. Hamilton, A. Y. Nikitin, and W. R. Zipfel, “Strategies for High-Resolution Imaging of Epithelial Ovarian Cancer by Laparoscopic Nonlinear Microscopy,” Transl. Oncol. 3(3), 181–194 (2010).
[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 (2012).
[Crossref] [PubMed]

Hernest, M.

Hocker, J.

B. L. Wen, M. A. Brewer, O. Nadiarnykh, J. Hocker, V. Singh, T. R. Mackie, and P. J. Campagnola, “Texture analysis applied to second harmonic generation image data for ovarian cancer classification,” J. Biomed. Opt. 19(9), 096007 (2014).
[Crossref] [PubMed]

Inman, D. R.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[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]

Jacobs, L. K.

S. M. Kakkad, M. Solaiyappan, P. Argani, S. Sukumar, L. K. Jacobs, D. Leibfritz, Z. M. Bhujwalla, and K. Glunde, “Collagen I fiber density increases in lymph node positive breast cancers: pilot study,” J. Biomed. Opt. 17(11), 116017 (2012).
[Crossref] [PubMed]

Jasiuk, I.

R. Ambekar, M. Chittenden, I. Jasiuk, and K. C. Toussaint., “Quantitative second-harmonic generation microscopy for imaging porcine cortical bone: Comparison to SEM and its potential to investigate age-related changes,” Bone 50(3), 643–650 (2012).
[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 (2012).
[Crossref] [PubMed]

Kakkad, S. M.

S. M. Kakkad, M. Solaiyappan, P. Argani, S. Sukumar, L. K. Jacobs, D. Leibfritz, Z. M. Bhujwalla, and K. Glunde, “Collagen I fiber density increases in lymph node positive breast cancers: pilot study,” J. Biomed. Opt. 17(11), 116017 (2012).
[Crossref] [PubMed]

Kalajzic, I.

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref] [PubMed]

Keely, P. J.

J. S. Bredfeldt, Y. Liu, M. W. Conklin, P. J. Keely, T. R. Mackie, and K. W. Eliceiri, “Automated quantification of aligned collagen for human breast carcinoma prognosis,” J. Pathol. Inform. 5(1), 28 (2014).
[Crossref] [PubMed]

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[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]

Keysers, D.

T. M. Lehmann, M. O. Güld, T. Deselaers, D. Keysers, H. Schubert, K. Spitzer, H. Ney, and B. B. Wein, “Automatic categorization of medical images for content-based retrieval and data mining,” Comput. Med. Imaging Graph. 29(2-3), 143–155 (2005).
[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 (2012).
[Crossref] [PubMed]

Knittel, J. G.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[Crossref] [PubMed]

Krasieva, T.

C. B. Raub, J. Unruh, V. Suresh, T. Krasieva, T. Lindmo, E. Gratton, B. J. Tromberg, and S. C. George, “Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties,” Biophys. J. 94(6), 2361–2373 (2008).
[Crossref] [PubMed]

LaComb, R. B.

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

Lau, T. Y.

Lehmann, T. M.

T. M. Lehmann, M. O. Güld, T. Deselaers, D. Keysers, H. Schubert, K. Spitzer, H. Ney, and B. B. Wein, “Automatic categorization of medical images for content-based retrieval and data mining,” Comput. Med. Imaging Graph. 29(2-3), 143–155 (2005).
[Crossref] [PubMed]

Leibfritz, D.

S. M. Kakkad, M. Solaiyappan, P. Argani, S. Sukumar, L. K. Jacobs, D. Leibfritz, Z. M. Bhujwalla, and K. Glunde, “Collagen I fiber density increases in lymph node positive breast cancers: pilot study,” J. Biomed. Opt. 17(11), 116017 (2012).
[Crossref] [PubMed]

Li, M. J.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. U.S.A. 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

Li, M.-J.

W. Liang, G. Hall, B. Messerschmidt, M.-J. Li, and X. D. Li, “Nonlinear optical endomicroscopy for label-free functional histology in vivo,” Light: Sci. Appl. 6, e17082 (2017).

K. Murari, Y. Zhang, S. Li, Y. Chen, M.-J. Li, and X. D. Li, “Compensation-free, all-fiber-optic, two-photon endomicroscopy at 1.55 μm,” Opt. Lett. 36, 1299–1301 (2011).

Li, S.

Li, X.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. U.S.A. 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

M. T. Myaing, D. J. MacDonald, and X. Li, “Fiber-optic scanning two-photon fluorescence endoscope,” Opt. Lett. 31(8), 1076–1078 (2006).
[Crossref] [PubMed]

Li, X. D.

Liang, W.

W. Liang, G. Hall, B. Messerschmidt, M.-J. Li, and X. D. Li, “Nonlinear optical endomicroscopy for label-free functional histology in vivo,” Light: Sci. Appl. 6, e17082 (2017).

Lindmo, T.

C. B. Raub, J. Unruh, V. Suresh, T. Krasieva, T. Lindmo, E. Gratton, B. J. Tromberg, and S. C. George, “Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties,” Biophys. J. 94(6), 2361–2373 (2008).
[Crossref] [PubMed]

Liu, Y.

J. S. Bredfeldt, Y. Liu, M. W. Conklin, P. J. Keely, T. R. Mackie, and K. W. Eliceiri, “Automated quantification of aligned collagen for human breast carcinoma prognosis,” J. Pathol. Inform. 5(1), 28 (2014).
[Crossref] [PubMed]

Loew, L. M.

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]

Luby-Phelps, K.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. U.S.A. 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

M. L. Akins, K. Luby-Phelps, and M. Mahendroo, “Second harmonic generation imaging as a potential tool for staging pregnancy and predicting preterm birth,” J. Biomed. Opt. 15(2), 026020 (2010).
[Crossref] [PubMed]

MacDonald, D. J.

Mackie, T. R.

J. S. Bredfeldt, Y. Liu, M. W. Conklin, P. J. Keely, T. R. Mackie, and K. W. Eliceiri, “Automated quantification of aligned collagen for human breast carcinoma prognosis,” J. Pathol. Inform. 5(1), 28 (2014).
[Crossref] [PubMed]

B. L. Wen, M. A. Brewer, O. Nadiarnykh, J. Hocker, V. Singh, T. R. Mackie, and P. J. Campagnola, “Texture analysis applied to second harmonic generation image data for ovarian cancer classification,” J. Biomed. Opt. 19(9), 096007 (2014).
[Crossref] [PubMed]

Mahendroo, M.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. U.S.A. 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

M. L. Akins, K. Luby-Phelps, and M. Mahendroo, “Second harmonic generation imaging as a potential tool for staging pregnancy and predicting preterm birth,” J. Biomed. Opt. 15(2), 026020 (2010).
[Crossref] [PubMed]

Martin, J. L.

Mehta, M. R.

Messerschmidt, B.

W. Liang, G. Hall, B. Messerschmidt, M.-J. Li, and X. D. Li, “Nonlinear optical endomicroscopy for label-free functional histology in vivo,” Light: Sci. Appl. 6, e17082 (2017).

Mohler, W. A.

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref] [PubMed]

Murari, K.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. U.S.A. 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

K. Murari, Y. Zhang, S. Li, Y. Chen, M.-J. Li, and X. D. Li, “Compensation-free, all-fiber-optic, two-photon endomicroscopy at 1.55 μm,” Opt. Lett. 36, 1299–1301 (2011).

Myaing, M. T.

Nadiarnykh, O.

B. L. Wen, M. A. Brewer, O. Nadiarnykh, J. Hocker, V. Singh, T. R. Mackie, and P. J. Campagnola, “Texture analysis applied to second harmonic generation image data for ovarian cancer classification,” J. Biomed. Opt. 19(9), 096007 (2014).
[Crossref] [PubMed]

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Ney, H.

T. M. Lehmann, M. O. Güld, T. Deselaers, D. Keysers, H. Schubert, K. Spitzer, H. Ney, and B. B. Wein, “Automatic categorization of medical images for content-based retrieval and data mining,” Comput. Med. Imaging Graph. 29(2-3), 143–155 (2005).
[Crossref] [PubMed]

Nikitin, A. Y.

R. M. Williams, A. Flesken-Nikitin, L. H. Ellenson, D. C. Connolly, T. C. Hamilton, A. Y. Nikitin, and W. R. Zipfel, “Strategies for High-Resolution Imaging of Epithelial Ovarian Cancer by Laparoscopic Nonlinear Microscopy,” Transl. Oncol. 3(3), 181–194 (2010).
[Crossref] [PubMed]

Pehlke, C. A.

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

Pena, A. M.

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).
[Crossref] [PubMed]

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref] [PubMed]

Provenzano, P. P.

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[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]

Rao, R. A.

Raub, C. B.

C. B. Raub, J. Unruh, V. Suresh, T. Krasieva, T. Lindmo, E. Gratton, B. J. Tromberg, and S. C. George, “Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties,” Biophys. J. 94(6), 2361–2373 (2008).
[Crossref] [PubMed]

Redford-Badwal, D.

O. Nadiarnykh, S. Plotnikov, W. A. Mohler, I. Kalajzic, D. Redford-Badwal, and P. J. Campagnola, “Second harmonic generation imaging microscopy studies of osteogenesis imperfecta,” J. Biomed. Opt. 12(5), 051805 (2007).
[Crossref] [PubMed]

Riching, K. M.

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

Rueden, C. T.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[Crossref] [PubMed]

Schanne-Klein, M. C.

Schubert, H.

T. M. Lehmann, M. O. Güld, T. Deselaers, D. Keysers, H. Schubert, K. Spitzer, H. Ney, and B. B. Wein, “Automatic categorization of medical images for content-based retrieval and data mining,” Comput. Med. Imaging Graph. 29(2-3), 143–155 (2005).
[Crossref] [PubMed]

Singh, V.

B. L. Wen, M. A. Brewer, O. Nadiarnykh, J. Hocker, V. Singh, T. R. Mackie, and P. J. Campagnola, “Texture analysis applied to second harmonic generation image data for ovarian cancer classification,” J. Biomed. Opt. 19(9), 096007 (2014).
[Crossref] [PubMed]

Solaiyappan, M.

S. M. Kakkad, M. Solaiyappan, P. Argani, S. Sukumar, L. K. Jacobs, D. Leibfritz, Z. M. Bhujwalla, and K. Glunde, “Collagen I fiber density increases in lymph node positive breast cancers: pilot study,” J. Biomed. Opt. 17(11), 116017 (2012).
[Crossref] [PubMed]

Spitzer, K.

T. M. Lehmann, M. O. Güld, T. Deselaers, D. Keysers, H. Schubert, K. Spitzer, H. Ney, and B. B. Wein, “Automatic categorization of medical images for content-based retrieval and data mining,” Comput. Med. Imaging Graph. 29(2-3), 143–155 (2005).
[Crossref] [PubMed]

Strupler, M.

Sukumar, S.

S. M. Kakkad, M. Solaiyappan, P. Argani, S. Sukumar, L. K. Jacobs, D. Leibfritz, Z. M. Bhujwalla, and K. Glunde, “Collagen I fiber density increases in lymph node positive breast cancers: pilot study,” J. Biomed. Opt. 17(11), 116017 (2012).
[Crossref] [PubMed]

Suresh, V.

C. B. Raub, J. Unruh, V. Suresh, T. Krasieva, T. Lindmo, E. Gratton, B. J. Tromberg, and S. C. George, “Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties,” Biophys. J. 94(6), 2361–2373 (2008).
[Crossref] [PubMed]

Tharaux, P. L.

Toussaint, K. C.

Tromberg, B. J.

C. B. Raub, J. Unruh, V. Suresh, T. Krasieva, T. Lindmo, E. Gratton, B. J. Tromberg, and S. C. George, “Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties,” Biophys. J. 94(6), 2361–2373 (2008).
[Crossref] [PubMed]

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 (2012).
[Crossref] [PubMed]

Unruh, J.

C. B. Raub, J. Unruh, V. Suresh, T. Krasieva, T. Lindmo, E. Gratton, B. J. Tromberg, and S. C. George, “Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties,” Biophys. J. 94(6), 2361–2373 (2008).
[Crossref] [PubMed]

Wein, B. B.

T. M. Lehmann, M. O. Güld, T. Deselaers, D. Keysers, H. Schubert, K. Spitzer, H. Ney, and B. B. Wein, “Automatic categorization of medical images for content-based retrieval and data mining,” Comput. Med. Imaging Graph. 29(2-3), 143–155 (2005).
[Crossref] [PubMed]

Wen, B. L.

B. L. Wen, M. A. Brewer, O. Nadiarnykh, J. Hocker, V. Singh, T. R. Mackie, and P. J. Campagnola, “Texture analysis applied to second harmonic generation image data for ovarian cancer classification,” J. Biomed. Opt. 19(9), 096007 (2014).
[Crossref] [PubMed]

White, J. G.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[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]

Williams, R. M.

R. M. Williams, A. Flesken-Nikitin, L. H. Ellenson, D. C. Connolly, T. C. Hamilton, A. Y. Nikitin, and W. R. Zipfel, “Strategies for High-Resolution Imaging of Epithelial Ovarian Cancer by Laparoscopic Nonlinear Microscopy,” Transl. Oncol. 3(3), 181–194 (2010).
[Crossref] [PubMed]

Wu, Y. C.

Xi, J.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. U.S.A. 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

Xi, J. F.

Yan, L.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[Crossref] [PubMed]

Zhang, Y.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. U.S.A. 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

K. Murari, Y. Zhang, S. Li, Y. Chen, M.-J. Li, and X. D. Li, “Compensation-free, all-fiber-optic, two-photon endomicroscopy at 1.55 μm,” Opt. Lett. 36, 1299–1301 (2011).

Zipfel, W. R.

R. M. Williams, A. Flesken-Nikitin, L. H. Ellenson, D. C. Connolly, T. C. Hamilton, A. Y. Nikitin, and W. R. Zipfel, “Strategies for High-Resolution Imaging of Epithelial Ovarian Cancer by Laparoscopic Nonlinear Microscopy,” Transl. Oncol. 3(3), 181–194 (2010).
[Crossref] [PubMed]

Am. J. Pathol. (1)

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

Biophys. J. (1)

C. B. Raub, J. Unruh, V. Suresh, T. Krasieva, T. Lindmo, E. Gratton, B. J. Tromberg, and S. C. George, “Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties,” Biophys. J. 94(6), 2361–2373 (2008).
[Crossref] [PubMed]

BMC Cancer (1)

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer 10(1), 94 (2010).
[Crossref] [PubMed]

BMC Med. (2)

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[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]

Bone (1)

R. Ambekar, M. Chittenden, I. Jasiuk, and K. C. Toussaint., “Quantitative second-harmonic generation microscopy for imaging porcine cortical bone: Comparison to SEM and its potential to investigate age-related changes,” Bone 50(3), 643–650 (2012).
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Comput. Med. Imaging Graph. (1)

T. M. Lehmann, M. O. Güld, T. Deselaers, D. Keysers, H. Schubert, K. Spitzer, H. Ney, and B. B. Wein, “Automatic categorization of medical images for content-based retrieval and data mining,” Comput. Med. Imaging Graph. 29(2-3), 143–155 (2005).
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S. M. Kakkad, M. Solaiyappan, P. Argani, S. Sukumar, L. K. Jacobs, D. Leibfritz, Z. M. Bhujwalla, and K. Glunde, “Collagen I fiber density increases in lymph node positive breast cancers: pilot study,” J. Biomed. Opt. 17(11), 116017 (2012).
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J. Pathol. Inform. (1)

J. S. Bredfeldt, Y. Liu, M. W. Conklin, P. J. Keely, T. R. Mackie, and K. W. Eliceiri, “Automated quantification of aligned collagen for human breast carcinoma prognosis,” J. Pathol. Inform. 5(1), 28 (2014).
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Light: Sci. Appl. (1)

W. Liang, G. Hall, B. Messerschmidt, M.-J. Li, and X. D. Li, “Nonlinear optical endomicroscopy for label-free functional histology in vivo,” Light: Sci. Appl. 6, e17082 (2017).

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. 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)

Opt. Lett. (3)

Proc. Natl. Acad. Sci. U.S.A. (1)

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. U.S.A. 109(32), 12878–12883 (2012).
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K. V. Mardia and P. E. Jupp, “Summary Statistics,” in Directional Statistics (John Wiley & Sons, Inc., 2008), pp. 13–24.

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Figures (6)

Fig. 1
Fig. 1 Digital phantoms of fibers ranging from high (a) to intermediate (b) and random alignment (c). The first column shows the spatial images  I(x,y) whereas the second column shows the corresponding FT magnitude image | I ^ (u,v)|. The third and fourth columns show the angular content distributions of | I ^ (u,v)| in a linear and polar manner, respectively. The computed R’s are shown for each case on the right.
Fig. 2
Fig. 2 Phantom generation for validation study. (a) Example of multi-fiber architecture on a black background. (b) Cross-sectional intensity profiles of fibers illustrating the influence of the contrast parameter c. (c) Illustration of the fibers in (b) in 2D images with a black background.
Fig. 3
Fig. 3 Distribution of the actual and computed angular anisotropy value R. Plotted in the figure are the mean value and standard deviation of   R computed versus corresponding R actual extracted from multiple digital phantoms. The standard deviation is represented by the error bars.
Fig. 4
Fig. 4 Robustness evaluation of the algorithm against various morphological parameters. The average and standard deviation (represented by the error bars) of R computed values are plotted versus R actual for different fiber morphological parameter values (ranges), including: (a) fiber diameter, (b) fiber contrast, (c) fiber density, and (d) fiber lengths.
Fig. 5
Fig. 5 Pronounced effect of white noise on the absolute R value for a perfectly aligned distribution. It is noted that white noise has no effect on the absolute R value for cases of completely random fiber orientation.
Fig. 6
Fig. 6 Application of the proposed algorithm to SHG images acquired from various types of biological tissues. (a) Highly aligned collagen fibers from mouse tail tendon. (b) Moderately-aligned cervical collagen fibers of normal pregnant mice at gestation day 6. (c) More randomized cervical collagen fibers of normal pregnant mice at gestation day 18. All images shown here were acquired using the nonlinear endomicroscope we recently developed [23]. The excitation conditions were ~10 mW for mouse tail tendon (a), and of ~40 mW for cervical tissue sections (b-c) at 890 nm. Ten raw frames were averaged for (a) while twenty for (b-c), corresponding to an effective frame acquisition time of ~3.8 s (a) and ~7.6 s (b-c), respectively. The computed R’s are shown at the upper-left corner for each image. Scale bars: 20 µm.

Equations (8)

Equations on this page are rendered with MathJax. Learn more.

I ^ ( u,v )=FT{ I(x,y) }= x= + y= + I( x,y ) e j2π( ux+vy ) dxdy.
A( θ )= ρ= + I ^ ( ρcosθ,ρsinθ )dρ.
R=| R |= | n=1 N a A( θ n ) ρ ^ 2 θ n | m=1 N a A( θ m )
I fib ( x,y )=exp[ x 2 2c ( D/2 ) 2 ]rect(x/D)rect(y/L)
I phantom ( x,y )= n=1 N f I fib (x x n ,y y n )×Rot( θ n )
R actual =| 1 N f n=1 N f ρ ^ 2 θ n   |
A( θ )=δ( θ θ 0 )+b
R computed =| 1 Nb+1 n=1 N A( θ n ) ρ ^ 2 θ n |

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