Abstract

Second-harmonic generation (SHG) double Stokes-Mueller polarimetric microscopy is applied to study the alteration of collagen ultrastructure in a tissue microarray containing three pathological human breast cancer types with differently overexpressed estrogen receptor (ER), progesterone receptor (PgR), and human epidermal growth factor receptor 2 (HER2). Kleinman symmetry is experimentally validated in breast tissue for 1028 nm laser wavelength and it has been shown that measurements with only linearly polarized incoming and outgoing states can determine molecular nonlinear susceptibility tensor component ratio, average in-plane orientation of collagen fibers and degree of linear polarization of SHG. Increase in the susceptibility ratio for ER, PgR, HER2 positive cases, reveals ultrastructural changes in the collagen fibers while the susceptibility ratio increase and decrease in degree of linear polarization for ER and PgR positive cases indicate alteration of the ultrastructure and increased disorder of the collagen fibers within each focal volume. The study demonstrates a potential use of polarimetric SHG microscopy for collagen characterization and cancer diagnostics.

© 2016 Optical Society of America

Full Article  |  PDF Article
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    [Crossref] [PubMed]

2016 (2)

2015 (4)

M. Samim, S. Krouglov, and V. Barzda, “Double Stokes Mueller polarimetry of second-harmonic generation in ordered molecular structures,” J. Opt. Soc. Am. B 32(3), 451–461 (2015).
[Crossref]

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]

A. Brabrand, II. Kariuki, M. J. Engstrom, O. A. Haugen, L. A. Dyrnes, B. O. Asvold, M. B. Lilledahl, and A. M. Bofin, “Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness?” APMIS 123(1)1–8 (2015).
[Crossref]

C. Brisken, K. Hess, and R. Jeitziner, “Progesterone and overlooked endocrine pathways in breast cancer pathogenesis,” Endocrinology 156(10), 3442–3450 (2015).
[Crossref] [PubMed]

2014 (2)

2013 (3)

C. Leys, C. Ley, O. Klein, P. Bernard, and L. Licata, “Detecting outliers: Do not use standard deviation around the mean, use absolute deviation around the median,” J. Exp. Soc. Psychol. 49(4), 764–766 (2013).
[Crossref]

L. B. Mostaco-Guidolin, A. C. 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, 2190 (2013).
[Crossref] [PubMed]

K. Burke, P. Tang, and E. Brown, “Second harmonic generation reveals matrix alterations during breast tumor progression,” J. Biomed. Opt. 18(3), 031106 (2013).
[Crossref]

2012 (3)

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]

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

R. Ambekar, T.-Y. Lau, M. Walsh, R. Bhargava, and K. C. Toussaint, “Quantifying collagen structure in breast biopsies using second-harmonic generation imaging,” Biomed. Opt. Express 3(9), 2021–2035 (2012).
[Crossref] [PubMed]

2011 (3)

V. Ajeti, O. N. Suzanne, M. Ponik, P. J. Keely, K. W. Eliceiri, and P. J. Campagnola, “Structural changes in mixed Col I/Col V collagen gels probed by SHG microscopy: implications for probing stromal alterations in human breast cancer,” Biomed. Opt. Express,  4(8), 2307–2316 (2011).
[Crossref]

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]

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

2010 (1)

A. Tuer, D. Tokarz, N. Prent, R. Cisek, J. Alami, D. J. Dumont, L. Bakueva, J. Rowlands, and V. Barzda, “Nonlinear multicontrast microscopy of hematoxylin-and-eosin-stained histological sections,” J. Biomed. Opt. 15(2), 026018 (2010)
[Crossref] [PubMed]

2008 (2)

B. Saikia, K. Gupta, and U. N. Saikia, “The modern histopathologist: in the changing face of time,” Diagnostic Pathology 3, 25–29 (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 Medicine 6(1), 11–16 (2008).
[Crossref] [PubMed]

2007 (1)

A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt. 12(4), 044002 (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 Medicine 4(1), 38–54 (2006).
[Crossref] [PubMed]

A. Major, R. Cisek, and V. Barzda, “Femtosecond Yb:KGd(WO4)2 laser oscillator pumped by a high power fiber-coupled diode laser module,” Opt. Express 14(25), 12163–12168 (2006).
[Crossref] [PubMed]

2004 (1)

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of chi(2)/chi(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophy. J. 86(6), 3914–3922 (2004).
[Crossref]

2002 (1)

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(2), 3330–3342 (2002).
[Crossref] [PubMed]

2001 (1)

M. Hidalgo and S. G. Eckhardt, “Development of matrix metalloproteinase inhibitors in cancer therapy,” J. Natl. Cancer Inst. 93(3), 178–193 (2001).
[Crossref] [PubMed]

1996 (1)

T.F. Coleman and Y. Li, “An Interior, Trust Region Approach for Nonlinear Minimization Subject to Bounds,” SIAM Journal on Optimization 6(2), 418–445 (1996).
[Crossref]

1994 (1)

Y. Shi, W. M. McClain, and R. A. Harris, “Generalized Stokes-Mueller formalism for two-photon absorption, frequency doubling, and hyper-Raman scattering,” Phys. Rev. A.,  49(3), 1999–2015 (1994).
[Crossref] [PubMed]

1988 (1)

C. Luparello, C. P. Rizzo, R. Schillaci, and I. Pucci-Minafra, “Fractionation of type V collagen from carcinomatous and dysplasic breast in the presence of alkaline potassium chloride,” Anal. Biochem. 169(1), 26–32 (1988).
[Crossref] [PubMed]

Ajeti, V.

Akens, M. K.

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

Alami, J.

A. Tuer, D. Tokarz, N. Prent, R. Cisek, J. Alami, D. J. Dumont, L. Bakueva, J. Rowlands, and V. Barzda, “Nonlinear multicontrast microscopy of hematoxylin-and-eosin-stained histological sections,” J. Biomed. Opt. 15(2), 026018 (2010)
[Crossref] [PubMed]

Ambekar, R.

Asa, S. L.

Asvold, B. O.

A. Brabrand, II. Kariuki, M. J. Engstrom, O. A. Haugen, L. A. Dyrnes, B. O. Asvold, M. B. Lilledahl, and A. M. Bofin, “Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness?” APMIS 123(1)1–8 (2015).
[Crossref]

Bakueva, L.

A. Tuer, D. Tokarz, N. Prent, R. Cisek, J. Alami, D. J. Dumont, L. Bakueva, J. Rowlands, and V. Barzda, “Nonlinear multicontrast microscopy of hematoxylin-and-eosin-stained histological sections,” J. Biomed. Opt. 15(2), 026018 (2010)
[Crossref] [PubMed]

Barzda, V.

M. Samim, S. Krouglov, and V. Barzda, “Nonlinear Stokes-Mueller polarimetry,” Phys. Rev. A 93(1), 013847 (2016).
[Crossref]

L. Kontenis, M. Samim, A. Karunendiran, S. Krouglov, B. Stewart, and V. Barzda, “Second harmonic generation double Stokes Mueller polarimetric microscopy of myofilaments,” Biomed. Opt. Express 7(2), 559–570 (2016).
[Crossref] [PubMed]

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]

M. Samim, S. Krouglov, and V. Barzda, “Double Stokes Mueller polarimetry of second-harmonic generation in ordered molecular structures,” J. Opt. Soc. Am. B 32(3), 451–461 (2015).
[Crossref]

A. Golaraei, R. Cisek, S. Krouglov, R. Navab, C. Niu, S. Sakashita, K. Yasufuku, M.-S. Tsao, B. C. Wilson, and V. Barzda, “Characterization of collagen in non-small cell lung carcinoma with second harmonic polarization microscopy,” Biomed. Opt. Express 5(10), 3562–3567 (2014).
[Crossref] [PubMed]

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

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

A. Tuer, D. Tokarz, N. Prent, R. Cisek, J. Alami, D. J. Dumont, L. Bakueva, J. Rowlands, and V. Barzda, “Nonlinear multicontrast microscopy of hematoxylin-and-eosin-stained histological sections,” J. Biomed. Opt. 15(2), 026018 (2010)
[Crossref] [PubMed]

A. Major, R. Cisek, and V. Barzda, “Femtosecond Yb:KGd(WO4)2 laser oscillator pumped by a high power fiber-coupled diode laser module,” Opt. Express 14(25), 12163–12168 (2006).
[Crossref] [PubMed]

Bernard, P.

C. Leys, C. Ley, O. Klein, P. Bernard, and L. Licata, “Detecting outliers: Do not use standard deviation around the mean, use absolute deviation around the median,” J. Exp. Soc. Psychol. 49(4), 764–766 (2013).
[Crossref]

Bhargava, R.

Bhatia, A. B.

M. Born, E. Wolf, and A. B. Bhatia, Principles of Optics: Electromagnetic Theory of Propagation, Interference and Diffraction of Light, 7th ed. (Cambridge University Press, 1999).
[Crossref]

Bofin, A. M.

A. Brabrand, II. Kariuki, M. J. Engstrom, O. A. Haugen, L. A. Dyrnes, B. O. Asvold, M. B. Lilledahl, and A. M. Bofin, “Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness?” APMIS 123(1)1–8 (2015).
[Crossref]

Born, M.

M. Born, E. Wolf, and A. B. Bhatia, Principles of Optics: Electromagnetic Theory of Propagation, Interference and Diffraction of Light, 7th ed. (Cambridge University Press, 1999).
[Crossref]

Brabrand, A.

A. Brabrand, II. Kariuki, M. J. Engstrom, O. A. Haugen, L. A. Dyrnes, B. O. Asvold, M. B. Lilledahl, and A. M. Bofin, “Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness?” APMIS 123(1)1–8 (2015).
[Crossref]

Brisken, C.

C. Brisken, K. Hess, and R. Jeitziner, “Progesterone and overlooked endocrine pathways in breast cancer pathogenesis,” Endocrinology 156(10), 3442–3450 (2015).
[Crossref] [PubMed]

Brown, E.

K. Burke, P. Tang, and E. Brown, “Second harmonic generation reveals matrix alterations during breast tumor progression,” J. Biomed. Opt. 18(3), 031106 (2013).
[Crossref]

Burke, K.

K. Burke, P. Tang, and E. Brown, “Second harmonic generation reveals matrix alterations during breast tumor progression,” J. Biomed. Opt. 18(3), 031106 (2013).
[Crossref]

Campagnola, P. J.

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 Medicine 4(1), 38–54 (2006).
[Crossref] [PubMed]

Celliers, P. M.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(2), 3330–3342 (2002).
[Crossref] [PubMed]

Chen, S. Y.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of chi(2)/chi(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophy. J. 86(6), 3914–3922 (2004).
[Crossref]

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. C.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of chi(2)/chi(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophy. J. 86(6), 3914–3922 (2004).
[Crossref]

Chern, G. W.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of chi(2)/chi(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophy. J. 86(6), 3914–3922 (2004).
[Crossref]

Chipman, R. A.

R. A. Chipman, “Polarimetry,” in Handbook of Optics, Vol I, M. Bass, C. DeCusatis, J. Enoch, V. Lakshminarayanan, G. Li, C. MacDonald, V. Mahajan, and E. Van Stryland, eds., 3rd ed. (McGraw Hill1995).

Chu, S. W.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of chi(2)/chi(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophy. J. 86(6), 3914–3922 (2004).
[Crossref]

Cisek, R.

Coleman, T.F.

T.F. Coleman and Y. Li, “An Interior, Trust Region Approach for Nonlinear Minimization Subject to Bounds,” SIAM Journal on Optimization 6(2), 418–445 (1996).
[Crossref]

Conklin, M. W.

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]

de Lange Davies, C.

A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt. 12(4), 044002 (2007).
[Crossref] [PubMed]

Dumont, D. J.

A. Tuer, D. Tokarz, N. Prent, R. Cisek, J. Alami, D. J. Dumont, L. Bakueva, J. Rowlands, and V. Barzda, “Nonlinear multicontrast microscopy of hematoxylin-and-eosin-stained histological sections,” J. Biomed. Opt. 15(2), 026018 (2010)
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Dyrnes, L. A.

A. Brabrand, II. Kariuki, M. J. Engstrom, O. A. Haugen, L. A. Dyrnes, B. O. Asvold, M. B. Lilledahl, and A. M. Bofin, “Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness?” APMIS 123(1)1–8 (2015).
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Eckhardt, S. G.

M. Hidalgo and S. G. Eckhardt, “Development of matrix metalloproteinase inhibitors in cancer therapy,” J. Natl. Cancer Inst. 93(3), 178–193 (2001).
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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.

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).
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V. Ajeti, O. N. Suzanne, M. Ponik, P. J. Keely, K. W. Eliceiri, and P. J. Campagnola, “Structural changes in mixed Col I/Col V collagen gels probed by SHG microscopy: implications for probing stromal alterations in human breast cancer,” Biomed. Opt. Express,  4(8), 2307–2316 (2011).
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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 Medicine 6(1), 11–16 (2008).
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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 Medicine 4(1), 38–54 (2006).
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Ellis, I. O.

S. R. Lakhani, I. O. Ellis, S. J. Schnitt, P. H. Tan, and M. J. van de Vijver, WHO Classification of Tumours of the Breast, World Health Organization classification of tumours, 4th ed. 2012, International Agency for Research on CancerFrance: Lyon.

Engstrom, M. J.

A. Brabrand, II. Kariuki, M. J. Engstrom, O. A. Haugen, L. A. Dyrnes, B. O. Asvold, M. B. Lilledahl, and A. M. Bofin, “Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness?” APMIS 123(1)1–8 (2015).
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A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt. 12(4), 044002 (2007).
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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).
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Golaraei, A.

Gupta, K.

B. Saikia, K. Gupta, and U. N. Saikia, “The modern histopathologist: in the changing face of time,” Diagnostic Pathology 3, 25–29 (2008).
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Harris, R. A.

Y. Shi, W. M. McClain, and R. A. Harris, “Generalized Stokes-Mueller formalism for two-photon absorption, frequency doubling, and hyper-Raman scattering,” Phys. Rev. A.,  49(3), 1999–2015 (1994).
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Haugen, O. A.

A. Brabrand, II. Kariuki, M. J. Engstrom, O. A. Haugen, L. A. Dyrnes, B. O. Asvold, M. B. Lilledahl, and A. M. Bofin, “Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness?” APMIS 123(1)1–8 (2015).
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Hess, K.

C. Brisken, K. Hess, and R. Jeitziner, “Progesterone and overlooked endocrine pathways in breast cancer pathogenesis,” Endocrinology 156(10), 3442–3450 (2015).
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Hewko, M.

L. B. Mostaco-Guidolin, A. C. 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, 2190 (2013).
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Hidalgo, M.

M. Hidalgo and S. G. Eckhardt, “Development of matrix metalloproteinase inhibitors in cancer therapy,” J. Natl. Cancer Inst. 93(3), 178–193 (2001).
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Hompland, T.

A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt. 12(4), 044002 (2007).
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Howell, D. C.

D. C. Howell, Statistical Methods for Psychology (Duxbury/Thomson Learning, 2002), Chap. 12.

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 Medicine 6(1), 11–16 (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 Medicine 4(1), 38–54 (2006).
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Jeitziner, R.

C. Brisken, K. Hess, and R. Jeitziner, “Progesterone and overlooked endocrine pathways in breast cancer pathogenesis,” Endocrinology 156(10), 3442–3450 (2015).
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Jemal, A.

R. Siegel, J. Ma, Z. Zou, and A. Jemal, “Cancer statistics 2014,” CA Cancer J. Clin. 64(1), 9–29 (2014).
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Kariuki, II.

A. Brabrand, II. Kariuki, M. J. Engstrom, O. A. Haugen, L. A. Dyrnes, B. O. Asvold, M. B. Lilledahl, and A. M. Bofin, “Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness?” APMIS 123(1)1–8 (2015).
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Karunendiran, A.

Keely, P. J.

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]

V. Ajeti, O. N. Suzanne, M. Ponik, P. J. Keely, K. W. Eliceiri, and P. J. Campagnola, “Structural changes in mixed Col I/Col V collagen gels probed by SHG microscopy: implications for probing stromal alterations in human breast cancer,” Biomed. Opt. Express,  4(8), 2307–2316 (2011).
[Crossref]

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 Medicine 6(1), 11–16 (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 Medicine 4(1), 38–54 (2006).
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Klein, O.

C. Leys, C. Ley, O. Klein, P. Bernard, and L. Licata, “Detecting outliers: Do not use standard deviation around the mean, use absolute deviation around the median,” J. Exp. Soc. Psychol. 49(4), 764–766 (2013).
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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 Medicine 6(1), 11–16 (2008).
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Ko, A. C.

L. B. Mostaco-Guidolin, A. C. 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, 2190 (2013).
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Kontenis, L.

Krouglov, S.

L. Kontenis, M. Samim, A. Karunendiran, S. Krouglov, B. Stewart, and V. Barzda, “Second harmonic generation double Stokes Mueller polarimetric microscopy of myofilaments,” Biomed. Opt. Express 7(2), 559–570 (2016).
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M. Samim, S. Krouglov, and V. Barzda, “Nonlinear Stokes-Mueller polarimetry,” Phys. Rev. A 93(1), 013847 (2016).
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M. Samim, S. Krouglov, and V. Barzda, “Double Stokes Mueller polarimetry of second-harmonic generation in ordered molecular structures,” J. Opt. Soc. Am. B 32(3), 451–461 (2015).
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A. Golaraei, R. Cisek, S. Krouglov, R. Navab, C. Niu, S. Sakashita, K. Yasufuku, M.-S. Tsao, B. C. Wilson, and V. Barzda, “Characterization of collagen in non-small cell lung carcinoma with second harmonic polarization microscopy,” Biomed. Opt. Express 5(10), 3562–3567 (2014).
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A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref] [PubMed]

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
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Lakhani, S. R.

S. R. Lakhani, I. O. Ellis, S. J. Schnitt, P. H. Tan, and M. J. van de Vijver, WHO Classification of Tumours of the Breast, World Health Organization classification of tumours, 4th ed. 2012, International Agency for Research on CancerFrance: Lyon.

Lau, T.-Y.

Ley, C.

C. Leys, C. Ley, O. Klein, P. Bernard, and L. Licata, “Detecting outliers: Do not use standard deviation around the mean, use absolute deviation around the median,” J. Exp. Soc. Psychol. 49(4), 764–766 (2013).
[Crossref]

Leys, C.

C. Leys, C. Ley, O. Klein, P. Bernard, and L. Licata, “Detecting outliers: Do not use standard deviation around the mean, use absolute deviation around the median,” J. Exp. Soc. Psychol. 49(4), 764–766 (2013).
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C. Leys, C. Ley, O. Klein, P. Bernard, and L. Licata, “Detecting outliers: Do not use standard deviation around the mean, use absolute deviation around the median,” J. Exp. Soc. Psychol. 49(4), 764–766 (2013).
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Lilledahl, M. B.

A. Brabrand, II. Kariuki, M. J. Engstrom, O. A. Haugen, L. A. Dyrnes, B. O. Asvold, M. B. Lilledahl, and A. M. Bofin, “Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness?” APMIS 123(1)1–8 (2015).
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Lin, B. L.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of chi(2)/chi(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophy. J. 86(6), 3914–3922 (2004).
[Crossref]

Lindgren, M.

A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt. 12(4), 044002 (2007).
[Crossref] [PubMed]

Luparello, C.

C. Luparello, C. P. Rizzo, R. Schillaci, and I. Pucci-Minafra, “Fractionation of type V collagen from carcinomatous and dysplasic breast in the presence of alkaline potassium chloride,” Anal. Biochem. 169(1), 26–32 (1988).
[Crossref] [PubMed]

Ma, J.

R. Siegel, J. Ma, Z. Zou, and A. Jemal, “Cancer statistics 2014,” CA Cancer J. Clin. 64(1), 9–29 (2014).
[Crossref] [PubMed]

Major, A.

L. B. Mostaco-Guidolin, A. C. 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, 2190 (2013).
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A. Major, R. Cisek, and V. Barzda, “Femtosecond Yb:KGd(WO4)2 laser oscillator pumped by a high power fiber-coupled diode laser module,” Opt. Express 14(25), 12163–12168 (2006).
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McClain, W. M.

Y. Shi, W. M. McClain, and R. A. Harris, “Generalized Stokes-Mueller formalism for two-photon absorption, frequency doubling, and hyper-Raman scattering,” Phys. Rev. A.,  49(3), 1999–2015 (1994).
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Mostaco-Guidolin, L. B.

L. B. Mostaco-Guidolin, A. C. 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, 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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Navab, R.

Niu, C.

Ortegren, J.

A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt. 12(4), 044002 (2007).
[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]

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]

Ponik, M.

Prent, N.

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

A. Tuer, D. Tokarz, N. Prent, R. Cisek, J. Alami, D. J. Dumont, L. Bakueva, J. Rowlands, and V. Barzda, “Nonlinear multicontrast microscopy of hematoxylin-and-eosin-stained histological sections,” J. Biomed. Opt. 15(2), 026018 (2010)
[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 Medicine 6(1), 11–16 (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 Medicine 4(1), 38–54 (2006).
[Crossref] [PubMed]

Pucci-Minafra, I.

C. Luparello, C. P. Rizzo, R. Schillaci, and I. Pucci-Minafra, “Fractionation of type V collagen from carcinomatous and dysplasic breast in the presence of alkaline potassium chloride,” Anal. Biochem. 169(1), 26–32 (1988).
[Crossref] [PubMed]

Reiser, K. M.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(2), 3330–3342 (2002).
[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]

Rizzo, C. P.

C. Luparello, C. P. Rizzo, R. Schillaci, and I. Pucci-Minafra, “Fractionation of type V collagen from carcinomatous and dysplasic breast in the presence of alkaline potassium chloride,” Anal. Biochem. 169(1), 26–32 (1988).
[Crossref] [PubMed]

Rowlands, J.

A. Tuer, D. Tokarz, N. Prent, R. Cisek, J. Alami, D. J. Dumont, L. Bakueva, J. Rowlands, and V. Barzda, “Nonlinear multicontrast microscopy of hematoxylin-and-eosin-stained histological sections,” J. Biomed. Opt. 15(2), 026018 (2010)
[Crossref] [PubMed]

Rubenchik, A. M.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(2), 3330–3342 (2002).
[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 Medicine 6(1), 11–16 (2008).
[Crossref] [PubMed]

Saikia, B.

B. Saikia, K. Gupta, and U. N. Saikia, “The modern histopathologist: in the changing face of time,” Diagnostic Pathology 3, 25–29 (2008).
[Crossref] [PubMed]

Saikia, U. N.

B. Saikia, K. Gupta, and U. N. Saikia, “The modern histopathologist: in the changing face of time,” Diagnostic Pathology 3, 25–29 (2008).
[Crossref] [PubMed]

Sakashita, S.

Samim, M.

Sandkuijl, D.

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

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
[Crossref] [PubMed]

Schillaci, R.

C. Luparello, C. P. Rizzo, R. Schillaci, and I. Pucci-Minafra, “Fractionation of type V collagen from carcinomatous and dysplasic breast in the presence of alkaline potassium chloride,” Anal. Biochem. 169(1), 26–32 (1988).
[Crossref] [PubMed]

Schnitt, S. J.

S. R. Lakhani, I. O. Ellis, S. J. Schnitt, P. H. Tan, and M. J. van de Vijver, WHO Classification of Tumours of the Breast, World Health Organization classification of tumours, 4th ed. 2012, International Agency for Research on CancerFrance: Lyon.

Shi, Y.

Y. Shi, W. M. McClain, and R. A. Harris, “Generalized Stokes-Mueller formalism for two-photon absorption, frequency doubling, and hyper-Raman scattering,” Phys. Rev. A.,  49(3), 1999–2015 (1994).
[Crossref] [PubMed]

Shiomi, M.

L. B. Mostaco-Guidolin, A. C. 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, 2190 (2013).
[Crossref] [PubMed]

Siegel, R.

R. Siegel, J. Ma, Z. Zou, and A. Jemal, “Cancer statistics 2014,” CA Cancer J. Clin. 64(1), 9–29 (2014).
[Crossref] [PubMed]

Sowa, M. G.

L. B. Mostaco-Guidolin, A. C. 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, 2190 (2013).
[Crossref] [PubMed]

Stewart, B.

Stoller, P.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(2), 3330–3342 (2002).
[Crossref] [PubMed]

Sun, C. K.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of chi(2)/chi(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophy. J. 86(6), 3914–3922 (2004).
[Crossref]

Suzanne, O. N.

Tan, P. H.

S. R. Lakhani, I. O. Ellis, S. J. Schnitt, P. H. Tan, and M. J. van de Vijver, WHO Classification of Tumours of the Breast, World Health Organization classification of tumours, 4th ed. 2012, International Agency for Research on CancerFrance: Lyon.

Tang, P.

K. Burke, P. Tang, and E. Brown, “Second harmonic generation reveals matrix alterations during breast tumor progression,” J. Biomed. Opt. 18(3), 031106 (2013).
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Tian, G.

L. B. Mostaco-Guidolin, A. C. 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, 2190 (2013).
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Tokarz, D.

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).
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A. Tuer, D. Tokarz, N. Prent, R. Cisek, J. Alami, D. J. Dumont, L. Bakueva, J. Rowlands, and V. Barzda, “Nonlinear multicontrast microscopy of hematoxylin-and-eosin-stained histological sections,” J. Biomed. Opt. 15(2), 026018 (2010)
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Toussaint, K. C.

Tsai, T. H.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of chi(2)/chi(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophy. J. 86(6), 3914–3922 (2004).
[Crossref]

Tsao, M.-S.

Tuer, A.

A. Tuer, D. Tokarz, N. Prent, R. Cisek, J. Alami, D. J. Dumont, L. Bakueva, J. Rowlands, and V. Barzda, “Nonlinear multicontrast microscopy of hematoxylin-and-eosin-stained histological sections,” J. Biomed. Opt. 15(2), 026018 (2010)
[Crossref] [PubMed]

Tuer, A. E.

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
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A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
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van de Vijver, M. J.

S. R. Lakhani, I. O. Ellis, S. J. Schnitt, P. H. Tan, and M. J. van de Vijver, WHO Classification of Tumours of the Breast, World Health Organization classification of tumours, 4th ed. 2012, International Agency for Research on CancerFrance: Lyon.

Walsh, M.

Wang, F.

L. B. Mostaco-Guidolin, A. C. 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, 2190 (2013).
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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 Medicine 6(1), 11–16 (2008).
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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 Medicine 4(1), 38–54 (2006).
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Whyne, C. M.

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

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).
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A. Golaraei, R. Cisek, S. Krouglov, R. Navab, C. Niu, S. Sakashita, K. Yasufuku, M.-S. Tsao, B. C. Wilson, and V. Barzda, “Characterization of collagen in non-small cell lung carcinoma with second harmonic polarization microscopy,” Biomed. Opt. Express 5(10), 3562–3567 (2014).
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A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref] [PubMed]

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
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Wolf, E.

M. Born, E. Wolf, and A. B. Bhatia, Principles of Optics: Electromagnetic Theory of Propagation, Interference and Diffraction of Light, 7th ed. (Cambridge University Press, 1999).
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Xiang, B.

L. B. Mostaco-Guidolin, A. C. 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, 2190 (2013).
[Crossref] [PubMed]

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 Medicine 6(1), 11–16 (2008).
[Crossref] [PubMed]

Yasufuku, K.

A. Golaraei, R. Cisek, S. Krouglov, R. Navab, C. Niu, S. Sakashita, K. Yasufuku, M.-S. Tsao, B. C. Wilson, and V. Barzda, “Characterization of collagen in non-small cell lung carcinoma with second harmonic polarization microscopy,” Biomed. Opt. Express 5(10), 3562–3567 (2014).
[Crossref] [PubMed]

A. E. Tuer, S. Krouglov, N. Prent, R. Cisek, D. Sandkuijl, K. Yasufuku, B. C. Wilson, and V. Barzda, “Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy,” J. Phys. Chem. B 115(44), 12759–12769 (2011).
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Zou, Z.

R. Siegel, J. Ma, Z. Zou, and A. Jemal, “Cancer statistics 2014,” CA Cancer J. Clin. 64(1), 9–29 (2014).
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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).
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Anal. Biochem. (1)

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APMIS (1)

A. Brabrand, II. Kariuki, M. J. Engstrom, O. A. Haugen, L. A. Dyrnes, B. O. Asvold, M. B. Lilledahl, and A. M. Bofin, “Alterations in collagen fibre patterns in breast cancer. A premise for tumour invasiveness?” APMIS 123(1)1–8 (2015).
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Biomed. Opt. Express (5)

Biophy. J. (1)

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of chi(2)/chi(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophy. J. 86(6), 3914–3922 (2004).
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Biophys. J. (2)

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
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P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J. 82(2), 3330–3342 (2002).
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BMC Medicine (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 Medicine 4(1), 38–54 (2006).
[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 Medicine 6(1), 11–16 (2008).
[Crossref] [PubMed]

CA Cancer J. Clin. (1)

R. Siegel, J. Ma, Z. Zou, and A. Jemal, “Cancer statistics 2014,” CA Cancer J. Clin. 64(1), 9–29 (2014).
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Diagnostic Pathology (1)

B. Saikia, K. Gupta, and U. N. Saikia, “The modern histopathologist: in the changing face of time,” Diagnostic Pathology 3, 25–29 (2008).
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Endocrinology (1)

C. Brisken, K. Hess, and R. Jeitziner, “Progesterone and overlooked endocrine pathways in breast cancer pathogenesis,” Endocrinology 156(10), 3442–3450 (2015).
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J. Biomed. Opt. (3)

A. Tuer, D. Tokarz, N. Prent, R. Cisek, J. Alami, D. J. Dumont, L. Bakueva, J. Rowlands, and V. Barzda, “Nonlinear multicontrast microscopy of hematoxylin-and-eosin-stained histological sections,” J. Biomed. Opt. 15(2), 026018 (2010)
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K. Burke, P. Tang, and E. Brown, “Second harmonic generation reveals matrix alterations during breast tumor progression,” J. Biomed. Opt. 18(3), 031106 (2013).
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A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt. 12(4), 044002 (2007).
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J. Exp. Soc. Psychol. (1)

C. Leys, C. Ley, O. Klein, P. Bernard, and L. Licata, “Detecting outliers: Do not use standard deviation around the mean, use absolute deviation around the median,” J. Exp. Soc. Psychol. 49(4), 764–766 (2013).
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M. Hidalgo and S. G. Eckhardt, “Development of matrix metalloproteinase inhibitors in cancer therapy,” J. Natl. Cancer Inst. 93(3), 178–193 (2001).
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Nat. Protoc. (1)

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Opt. Express (1)

Phys. Rev. A (1)

M. Samim, S. Krouglov, and V. Barzda, “Nonlinear Stokes-Mueller polarimetry,” Phys. Rev. A 93(1), 013847 (2016).
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Phys. Rev. A. (1)

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Figures (6)

Fig. 1
Fig. 1 DSMP microscope setup. PSG and PSA are polarization state generator and analyzer respectively. collagen fibers are shown in the laboratory coordinate system (XYZ) and molecular coordinate system (xyz) where angle δ is defined as the angle between average fiber axis, z and Z-axis of the laboratory-frame of reference.
Fig. 2
Fig. 2 Measured SHG Stokes matrix elements of normal and malignant breast tissue samples. Bright-field microscopy images of scanned area are presented for the H&E stained a) normal and c) malignant (double positive) breast tissues. Scale bar shown in panel (a) is 25 μm. Measured SHG Stokes matrix elements of b) normal and d) malignant breast tissue are shown. Each row represents SHG Stokes vector components γ with γ = 0, 1, 2, 3 for each of the nine incoming polarization states indicated on the top of the matrix. Laboratory axes and a 20-μm scale bar are shown in panel (b).
Fig. 3
Fig. 3 Degree of total (DP), linear (DLP), and circular (DCP) polarization of outgoing SHG from breast tissue for the nine different incoming polarization states. The a) normal and b) malignant (double positive) breast tissue were studied. The images are calculated from the data shown in Fig. 2. Only pixels with signal-to-noise>4 are shown. Laboratory axes and a 20-μm scale bar are shown in panel (a).
Fig. 4
Fig. 4 Double Mueller matrix elements of a) normal and b) malignant (double positive) breast tissue. Laboratory axes and a 20-μm scale bar are shown in panel (a).
Fig. 5
Fig. 5 Laboratory-frame second-order susceptibility values of breast tissue for a) normal and b) malignant (double positive) breast tissue. The number below each image shows the normalized (to χ Z Z Z ( 2 )) average value of the non-zero pixels. Laboratory axes and a 20-μm scale bar are shown in panel (a).
Fig. 6
Fig. 6 PIPO SHG analysis of normal and malignant breast tissue samples. Column (a) shows bright-field microscopy images of the H&E stained tissues with square indicating the scanned area of 110 μm×110 μm used for the SHG data analysis shown in columns (b) to (e). Column (b) visualizes the normalized SHG intensity images (summation of all the polarization states) of the corresponding regions outlined by a black box in H&E images. Column (c) displays the R map where the blue represents an R value of 1.5 and the red represents a R value of 3. The colorbar also contains the R occurrence pixel histogram of the corresponding images. Column (d) shows the orientation map of the cylindrical axis, δ, for each fitted image pixel. Column (e) displays the DLP map where the color bar ranges from 0 to 1 and also contains corresponding DLP occurrence pixel histograms. Laboratory axes and a 25-μm scale bar are shown in the last panel of column (b).

Tables (1)

Tables Icon

Table 1 Statistical analysis for the R, δ and DLP values for all patients.a,b

Equations (5)

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s ( 2 ω ) = ( 2 ) S ( ω )
Q 1 2 3 4 5 6 7 8 9 HLP VLP + 45 45 RCP LCP 22.5 REP LEP Γ Ω ( 0 0 ) ( π / 2 0 ) ( π / 4 0 ) ( π / 4 0 ) ( 0 π / 4 ) ( 0 π / 4 ) ( π / 8 0 ) ( π / 2 π / 8 ) ( π / 4 π / 8 )
γ , i ( 2 ) = s γ , Q S Q , i 1
DP = s ˜ 1 2 + s ˜ 2 2 + s ˜ 3 2 s ˜ 0 DLP = s ˜ 1 2 + s ˜ 2 2 s ˜ 0 DCP = s ˜ 3 2 s ˜ 0
I SHG | sin ( ϕ δ ) sin ( 2 θ 2 δ ) + cos ( ϕ δ ) sin 2 ( θ δ ) + χ z z z ( 2 ) χ z x x ( 2 ) cos ( ϕ δ ) cos 2 ( θ δ ) | 2

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