Abstract

Quantitative second-harmonic generation imaging is employed to assess stromal collagen in normal, hyperplastic, dysplastic, and malignant breast tissues. The cellular scale organization is quantified using Fourier transform-second harmonic generation imaging (FT-SHG), while the molecular scale organization is quantified using polarization-resolved second-harmonic generation measurements (P-SHG). In the case of FT-SHG, we apply a parameter that quantifies the regularity in collagen fiber orientation and find that malignant tissue contains locally aligned fibers compared to other tissue conditions. Alternatively, using P-SHG we calculate the ratio of tensor elements (d15/d31, d22/d31, and d33/d31) of the second-order susceptibility χ2 for collagen fibers in breast biopsies. In particular, d15/d31 shows potential differences across the tissue pathology. We also find that trigonal symmetry (3m) is a more appropriate model to describe collagen fibers in malignant tissues as opposed to the conventionally used hexagonal symmetry (C6). This novel method of targeting collagen fibers using a combination of two quantitative SHG techniques, FT-SHG and P-SHG, holds promise for breast tissue analysis and applications to characterizing cancer in a manner that is compatible with clinical practice.

© 2012 OSA

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  1. A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, and D. Forman, “Global cancer statistics,” CA Cancer J. Clin.61(2), 69–90 (2011).
    [CrossRef] [PubMed]
  2. “Cancer Facts & Figures—2012American Cancer Society, 2012).
  3. B. N. Datta, Textbook of Pathology (Jaypee Brothers Medical, 2008).
  4. S. Srivastava, Molecular Pathology of Early Cancer (IOS, 1998).
  5. L. A. Liotta, C. N. Rao, and S. H. Barsky, “Tumor invasion and the extracellular matrix,” Lab. Invest.49(6), 636–649 (1983).
    [PubMed]
  6. D. Radisky, J. Muschler, and M. J. Bissell, “Order and disorder: the role of extracellular matrix in epithelial cancer,” Cancer Invest.20(1), 139–153 (2002).
    [CrossRef] [PubMed]
  7. J. E. Ferguson, A. M. Schor, A. Howell, and M. W. J. Ferguson, “Changes in the extracellular matrix of the normal human breast during the menstrual cycle,” Cell Tissue Res.268(1), 167–177 (1992).
    [CrossRef] [PubMed]
  8. I. Stamenkovic, “Extracellular matrix remodelling: the role of matrix metalloproteinases,” J. Pathol.200(4), 448–464 (2003).
    [CrossRef] [PubMed]
  9. O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
    [CrossRef] [PubMed]
  10. S. E. Holton, M. J. Walsh, A. Kajdacsy-Balla, and R. Bhargava, “Label-free characterization of cancer-activated fibroblasts using infrared spectroscopic imaging,” Biophys. J.101(6), 1513–1521 (2011).
    [CrossRef] [PubMed]
  11. S. E. Holton, M. J. Walsh, and R. Bhargava, “Subcellular localization of early biochemical transformations in cancer-activated fibroblasts using infrared spectroscopic imaging,” Analyst (Lond.)136(14), 2953–2958 (2011).
    [CrossRef] [PubMed]
  12. J. T. Erler and V. M. Weaver, “Three-dimensional context regulation of metastasis,” Clin. Exp. Metastasis26(1), 35–49 (2009).
    [CrossRef] [PubMed]
  13. J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
    [CrossRef] [PubMed]
  14. D. Barkan, J. E. Green, and A. F. Chambers, “Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth,” Eur. J. Cancer46(7), 1181–1188 (2010).
    [CrossRef] [PubMed]
  15. 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]
  16. 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]
  17. C. Thrasivoulou, G. Virich, T. Krenacs, I. Korom, and D. L. Becker, “Optical delineation of human malignant melanoma using second harmonic imaging of collagen,” Biomed. Opt. Express2(5), 1282–1295 (2011).
    [CrossRef] [PubMed]
  18. W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A.100(12), 7075–7080 (2003).
    [CrossRef] [PubMed]
  19. 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]
  20. A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
    [CrossRef] [PubMed]
  21. I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
    [CrossRef] [PubMed]
  22. G. Cox, E. Kable, A. Jones, I. K. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol.141(1), 53–62 (2003).
    [CrossRef] [PubMed]
  23. W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).
  24. F. Tiaho, G. Recher, and D. Rouède, “Estimation of helical angles of myosin and collagen by second harmonic generation imaging microscopy,” Opt. Express15(19), 12286–12295 (2007).
    [CrossRef] [PubMed]
  25. R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J.88(2), 1377–1386 (2005).
    [CrossRef] [PubMed]
  26. 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,” Bone50(3), 643–650 (2012).
    [CrossRef] [PubMed]
  27. R. A. Rao, M. R. Mehta, S. Leithem, and K. C. Toussaint., “Quantitative analysis of forward and backward second-harmonic images of collagen fibers using Fourier transform second-harmonic-generation microscopy,” Opt. Lett.34(24), 3779–3781 (2009).
    [CrossRef] [PubMed]
  28. R. A. Rao, M. R. Mehta, and K. C. Toussaint., “Fourier transform-second-harmonic generation imaging of biological tissues,” Opt. Express17(17), 14534–14542 (2009).
    [CrossRef] [PubMed]
  29. M. Sivaguru, S. Durgam, R. Ambekar, D. Luedtke, G. Fried, A. Stewart, and K. C. Toussaint., “Quantitative analysis of collagen fiber organization in injured tendons using Fourier transform-second harmonic generation imaging,” Opt. Express18(24), 24983–24993 (2010).
    [CrossRef] [PubMed]
  30. P. J. Su, W. L. Chen, J. B. Hong, T. H. Li, R. J. Wu, C. K. Chou, S. J. Chen, C. Hu, S. J. Lin, and C. Y. Dong, “Discrimination of collagen in normal and pathological skin dermis through second-order susceptibility microscopy,” Opt. Express17(13), 11161–11171 (2009).
    [CrossRef] [PubMed]
  31. C. Odin, T. Guilbert, A. Alkilani, O. P. Boryskina, V. Fleury, and Y. Le Grand, “Collagen and myosin characterization by orientation field second harmonic microscopy,” Opt. Express16(20), 16151–16165 (2008).
    [CrossRef] [PubMed]
  32. S. Psilodimitrakopoulos, D. Artigas, G. Soria, I. Amat-Roldan, A. M. Planas, and P. Loza-Alvarez, “Quantitative discrimination between endogenous SHG sources in mammalian tissue, based on their polarization response,” Opt. Express17(12), 10168–10176 (2009).
    [CrossRef] [PubMed]
  33. S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt.14(1), 014001–014011 (2009).
    [CrossRef] [PubMed]
  34. P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
    [CrossRef] [PubMed]
  35. X. Han, R. M. Burke, M. L. Zettel, P. Tang, and E. B. Brown, “Second harmonic properties of tumor collagen: determining the structural relationship between reactive stroma and healthy stroma,” Opt. Express16(3), 1846–1859 (2008).
    [CrossRef] [PubMed]
  36. T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt.13(5), 054050 (2008).
    [CrossRef] [PubMed]
  37. B. E. A. Saleh and M. C. Teich, Fundamentals of Photonics (Wiley Interscience, 2007).
  38. P. N. Butcher and D. Cotter, The Elements of Nonlinear Optics (Cambridge University Press, 2003).
  39. B. Y. Jiang and S. W. Chu, “Trigonal symmetry of type I collagen probed by SHG polarization anisotropy,” in Conference on Lasers and Electro-Optics/Quantum Electronics and Laser Science Conference and Photonic Applications Systems Technologies, OSA Technical Digest (CD) (Optical Society of America, 2008), paper JWA30.
  40. J. T. Kwak, R. Reddy, S. Sinha, and R. Bhargava, “Analysis of variance in spectroscopic imaging data from human tissues,” Anal. Chem.84(2), 1063–1069 (2012).
    [CrossRef] [PubMed]
  41. I. W. Levin and R. Bhargava, “Fourier transform infrared vibrational spectroscopic imaging: integrating microscopy and molecular recognition,” in Annual Review of Physical Chemistry (Annual Reviews, Palo Alto, 2005), Vol. 56, pp. 429–474.
  42. D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol.23(4), 469–474 (2005).
    [CrossRef] [PubMed]
  43. S. Brasselet, D. Aït-Belkacem, A. Gasecka, F. Munhoz, S. Brustlein, and S. Brasselet, “Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging,” Opt. Express18(14), 14859–14870 (2010).
    [CrossRef] [PubMed]
  44. I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Polarization-resolved Second Harmonic microscopy in anisotropic thick tissues,” Opt. Express18(18), 19339–19352 (2010).
    [CrossRef] [PubMed]
  45. O. De Wever and M. Mareel, “Role of tissue stroma in cancer cell invasion,” J. Pathol.200(4), 429–447 (2003).
    [CrossRef] [PubMed]
  46. E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
    [CrossRef] [PubMed]
  47. S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
    [CrossRef] [PubMed]
  48. 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]

2012

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,” Bone50(3), 643–650 (2012).
[CrossRef] [PubMed]

J. T. Kwak, R. Reddy, S. Sinha, and R. Bhargava, “Analysis of variance in spectroscopic imaging data from human tissues,” Anal. Chem.84(2), 1063–1069 (2012).
[CrossRef] [PubMed]

2011

A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, and D. Forman, “Global cancer statistics,” CA Cancer J. Clin.61(2), 69–90 (2011).
[CrossRef] [PubMed]

S. E. Holton, M. J. Walsh, A. Kajdacsy-Balla, and R. Bhargava, “Label-free characterization of cancer-activated fibroblasts using infrared spectroscopic imaging,” Biophys. J.101(6), 1513–1521 (2011).
[CrossRef] [PubMed]

S. E. Holton, M. J. Walsh, and R. Bhargava, “Subcellular localization of early biochemical transformations in cancer-activated fibroblasts using infrared spectroscopic imaging,” Analyst (Lond.)136(14), 2953–2958 (2011).
[CrossRef] [PubMed]

C. Thrasivoulou, G. Virich, T. Krenacs, I. Korom, and D. L. Becker, “Optical delineation of human malignant melanoma using second harmonic imaging of collagen,” Biomed. Opt. Express2(5), 1282–1295 (2011).
[CrossRef] [PubMed]

2010

D. Barkan, J. E. Green, and A. F. Chambers, “Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth,” Eur. J. Cancer46(7), 1181–1188 (2010).
[CrossRef] [PubMed]

S. Brasselet, D. Aït-Belkacem, A. Gasecka, F. Munhoz, S. Brustlein, and S. Brasselet, “Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging,” Opt. Express18(14), 14859–14870 (2010).
[CrossRef] [PubMed]

I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Polarization-resolved Second Harmonic microscopy in anisotropic thick tissues,” Opt. Express18(18), 19339–19352 (2010).
[CrossRef] [PubMed]

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

M. Sivaguru, S. Durgam, R. Ambekar, D. Luedtke, G. Fried, A. Stewart, and K. C. Toussaint., “Quantitative analysis of collagen fiber organization in injured tendons using Fourier transform-second harmonic generation imaging,” Opt. Express18(24), 24983–24993 (2010).
[CrossRef] [PubMed]

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

2009

P. J. Su, W. L. Chen, J. B. Hong, T. H. Li, R. J. Wu, C. K. Chou, S. J. Chen, C. Hu, S. J. Lin, and C. Y. Dong, “Discrimination of collagen in normal and pathological skin dermis through second-order susceptibility microscopy,” Opt. Express17(13), 11161–11171 (2009).
[CrossRef] [PubMed]

R. A. Rao, M. R. Mehta, S. Leithem, and K. C. Toussaint., “Quantitative analysis of forward and backward second-harmonic images of collagen fibers using Fourier transform second-harmonic-generation microscopy,” Opt. Lett.34(24), 3779–3781 (2009).
[CrossRef] [PubMed]

R. A. Rao, M. R. Mehta, and K. C. Toussaint., “Fourier transform-second-harmonic generation imaging of biological tissues,” Opt. Express17(17), 14534–14542 (2009).
[CrossRef] [PubMed]

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

S. Psilodimitrakopoulos, D. Artigas, G. Soria, I. Amat-Roldan, A. M. Planas, and P. Loza-Alvarez, “Quantitative discrimination between endogenous SHG sources in mammalian tissue, based on their polarization response,” Opt. Express17(12), 10168–10176 (2009).
[CrossRef] [PubMed]

S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt.14(1), 014001–014011 (2009).
[CrossRef] [PubMed]

J. T. Erler and V. M. Weaver, “Three-dimensional context regulation of metastasis,” Clin. Exp. Metastasis26(1), 35–49 (2009).
[CrossRef] [PubMed]

2008

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

X. Han, R. M. Burke, M. L. Zettel, P. Tang, and E. B. Brown, “Second harmonic properties of tumor collagen: determining the structural relationship between reactive stroma and healthy stroma,” Opt. Express16(3), 1846–1859 (2008).
[CrossRef] [PubMed]

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt.13(5), 054050 (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]

C. Odin, T. Guilbert, A. Alkilani, O. P. Boryskina, V. Fleury, and Y. Le Grand, “Collagen and myosin characterization by orientation field second harmonic microscopy,” Opt. Express16(20), 16151–16165 (2008).
[CrossRef] [PubMed]

2007

2006

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

2005

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

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol.23(4), 469–474 (2005).
[CrossRef] [PubMed]

2003

O. De Wever and M. Mareel, “Role of tissue stroma in cancer cell invasion,” J. Pathol.200(4), 429–447 (2003).
[CrossRef] [PubMed]

G. Cox, E. Kable, A. Jones, I. K. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol.141(1), 53–62 (2003).
[CrossRef] [PubMed]

I. Stamenkovic, “Extracellular matrix remodelling: the role of matrix metalloproteinases,” J. Pathol.200(4), 448–464 (2003).
[CrossRef] [PubMed]

O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A.100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

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

2002

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

D. Radisky, J. Muschler, and M. J. Bissell, “Order and disorder: the role of extracellular matrix in epithelial cancer,” Cancer Invest.20(1), 139–153 (2002).
[CrossRef] [PubMed]

2001

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]

1992

J. E. Ferguson, A. M. Schor, A. Howell, and M. W. J. Ferguson, “Changes in the extracellular matrix of the normal human breast during the menstrual cycle,” Cell Tissue Res.268(1), 167–177 (1992).
[CrossRef] [PubMed]

1986

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
[CrossRef] [PubMed]

1983

L. A. Liotta, C. N. Rao, and S. H. Barsky, “Tumor invasion and the extracellular matrix,” Lab. Invest.49(6), 636–649 (1983).
[PubMed]

Aït-Belkacem, D.

Alkilani, A.

Amat-Roldan, I.

S. Psilodimitrakopoulos, D. Artigas, G. Soria, I. Amat-Roldan, A. M. Planas, and P. Loza-Alvarez, “Quantitative discrimination between endogenous SHG sources in mammalian tissue, based on their polarization response,” Opt. Express17(12), 10168–10176 (2009).
[CrossRef] [PubMed]

S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt.14(1), 014001–014011 (2009).
[CrossRef] [PubMed]

Ambekar, R.

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,” Bone50(3), 643–650 (2012).
[CrossRef] [PubMed]

M. Sivaguru, S. Durgam, R. Ambekar, D. Luedtke, G. Fried, A. Stewart, and K. C. Toussaint., “Quantitative analysis of collagen fiber organization in injured tendons using Fourier transform-second harmonic generation imaging,” Opt. Express18(24), 24983–24993 (2010).
[CrossRef] [PubMed]

Artigas, D.

S. Psilodimitrakopoulos, D. Artigas, G. Soria, I. Amat-Roldan, A. M. Planas, and P. Loza-Alvarez, “Quantitative discrimination between endogenous SHG sources in mammalian tissue, based on their polarization response,” Opt. Express17(12), 10168–10176 (2009).
[CrossRef] [PubMed]

S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt.14(1), 014001–014011 (2009).
[CrossRef] [PubMed]

Barkan, D.

D. Barkan, J. E. Green, and A. F. Chambers, “Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth,” Eur. J. Cancer46(7), 1181–1188 (2010).
[CrossRef] [PubMed]

Barsky, S. H.

L. A. Liotta, C. N. Rao, and S. H. Barsky, “Tumor invasion and the extracellular matrix,” Lab. Invest.49(6), 636–649 (1983).
[PubMed]

Becker, D. L.

Berns, E. M.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

Bhargava, R.

J. T. Kwak, R. Reddy, S. Sinha, and R. Bhargava, “Analysis of variance in spectroscopic imaging data from human tissues,” Anal. Chem.84(2), 1063–1069 (2012).
[CrossRef] [PubMed]

S. E. Holton, M. J. Walsh, and R. Bhargava, “Subcellular localization of early biochemical transformations in cancer-activated fibroblasts using infrared spectroscopic imaging,” Analyst (Lond.)136(14), 2953–2958 (2011).
[CrossRef] [PubMed]

S. E. Holton, M. J. Walsh, A. Kajdacsy-Balla, and R. Bhargava, “Label-free characterization of cancer-activated fibroblasts using infrared spectroscopic imaging,” Biophys. J.101(6), 1513–1521 (2011).
[CrossRef] [PubMed]

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol.23(4), 469–474 (2005).
[CrossRef] [PubMed]

Bissell, M. J.

O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
[CrossRef] [PubMed]

D. Radisky, J. Muschler, and M. J. Bissell, “Order and disorder: the role of extracellular matrix in epithelial cancer,” Cancer Invest.20(1), 139–153 (2002).
[CrossRef] [PubMed]

Boryskina, O. P.

Brasselet, S.

Bray, F.

A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, and D. Forman, “Global cancer statistics,” CA Cancer J. Clin.61(2), 69–90 (2011).
[CrossRef] [PubMed]

Brown, E. B.

Brustlein, S.

Burke, R. M.

Campagnola, P. J.

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]

Center, M. M.

A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, and D. Forman, “Global cancer statistics,” CA Cancer J. Clin.61(2), 69–90 (2011).
[CrossRef] [PubMed]

Chambers, A. F.

D. Barkan, J. E. Green, and A. F. Chambers, “Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth,” Eur. J. Cancer46(7), 1181–1188 (2010).
[CrossRef] [PubMed]

Chang, S. J.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

Chen, S. J.

Chen, T. H.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

Chen, W. L.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

P. J. Su, W. L. Chen, J. B. Hong, T. H. Li, R. J. Wu, C. K. Chou, S. J. Chen, C. Hu, S. J. Lin, and C. Y. Dong, “Discrimination of collagen in normal and pathological skin dermis through second-order susceptibility microscopy,” Opt. Express17(13), 11161–11171 (2009).
[CrossRef] [PubMed]

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

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,” Bone50(3), 643–650 (2012).
[CrossRef] [PubMed]

Chou, C. K.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

P. J. Su, W. L. Chen, J. B. Hong, T. H. Li, R. J. Wu, C. K. Chou, S. J. Chen, C. Hu, S. J. Lin, and C. Y. Dong, “Discrimination of collagen in normal and pathological skin dermis through second-order susceptibility microscopy,” Opt. Express17(13), 11161–11171 (2009).
[CrossRef] [PubMed]

Christie, R.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A.100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Cox, G.

G. Cox, E. Kable, A. Jones, I. K. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol.141(1), 53–62 (2003).
[CrossRef] [PubMed]

de Lange Davies, C.

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt.13(5), 054050 (2008).
[CrossRef] [PubMed]

De Wever, O.

O. De Wever and M. Mareel, “Role of tissue stroma in cancer cell invasion,” J. Pathol.200(4), 429–447 (2003).
[CrossRef] [PubMed]

DeRidder, A. M.

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

Deutsch, M.

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
[CrossRef] [PubMed]

Dong, C. Y.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

P. J. Su, W. L. Chen, J. B. Hong, T. H. Li, R. J. Wu, C. K. Chou, S. J. Chen, C. Hu, S. J. Lin, and C. Y. Dong, “Discrimination of collagen in normal and pathological skin dermis through second-order susceptibility microscopy,” Opt. Express17(13), 11161–11171 (2009).
[CrossRef] [PubMed]

Durgam, S.

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).
[CrossRef] [PubMed]

Eliceiri, K. W.

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]

Erikson, A.

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt.13(5), 054050 (2008).
[CrossRef] [PubMed]

Erler, J. T.

J. T. Erler and V. M. Weaver, “Three-dimensional context regulation of metastasis,” Clin. Exp. Metastasis26(1), 35–49 (2009).
[CrossRef] [PubMed]

Ferguson, J. E.

J. E. Ferguson, A. M. Schor, A. Howell, and M. W. J. Ferguson, “Changes in the extracellular matrix of the normal human breast during the menstrual cycle,” Cell Tissue Res.268(1), 167–177 (1992).
[CrossRef] [PubMed]

Ferguson, M. W. J.

J. E. Ferguson, A. M. Schor, A. Howell, and M. W. J. Ferguson, “Changes in the extracellular matrix of the normal human breast during the menstrual cycle,” Cell Tissue Res.268(1), 167–177 (1992).
[CrossRef] [PubMed]

Ferlay, J.

A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, and D. Forman, “Global cancer statistics,” CA Cancer J. Clin.61(2), 69–90 (2011).
[CrossRef] [PubMed]

Fernandez, D. C.

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol.23(4), 469–474 (2005).
[CrossRef] [PubMed]

Fleury, V.

Foekens, J. A.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

Forman, D.

A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, and D. Forman, “Global cancer statistics,” CA Cancer J. Clin.61(2), 69–90 (2011).
[CrossRef] [PubMed]

Fraser, I. K.

G. Cox, E. Kable, A. Jones, I. K. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol.141(1), 53–62 (2003).
[CrossRef] [PubMed]

Freund, I.

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
[CrossRef] [PubMed]

Fried, G.

Fwu, P. T.

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

Gasecka, A.

Gorrell, M. D.

G. Cox, E. Kable, A. Jones, I. K. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol.141(1), 53–62 (2003).
[CrossRef] [PubMed]

Green, J. E.

D. Barkan, J. E. Green, and A. F. Chambers, “Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth,” Eur. J. Cancer46(7), 1181–1188 (2010).
[CrossRef] [PubMed]

Gudjonsson, T.

O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
[CrossRef] [PubMed]

Guilbert, T.

Gusachenko, I.

Han, S. J.

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

Han, X.

Helleman, J.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

Hewitt, S. M.

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol.23(4), 469–474 (2005).
[CrossRef] [PubMed]

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).
[CrossRef] [PubMed]

Ho, Y. Y.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

Holmbeck, K.

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

Holton, S. E.

S. E. Holton, M. J. Walsh, and R. Bhargava, “Subcellular localization of early biochemical transformations in cancer-activated fibroblasts using infrared spectroscopic imaging,” Analyst (Lond.)136(14), 2953–2958 (2011).
[CrossRef] [PubMed]

S. E. Holton, M. J. Walsh, A. Kajdacsy-Balla, and R. Bhargava, “Label-free characterization of cancer-activated fibroblasts using infrared spectroscopic imaging,” Biophys. J.101(6), 1513–1521 (2011).
[CrossRef] [PubMed]

Hompland, T.

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt.13(5), 054050 (2008).
[CrossRef] [PubMed]

Hong, J. B.

Howell, A.

J. E. Ferguson, A. M. Schor, A. Howell, and M. W. J. Ferguson, “Changes in the extracellular matrix of the normal human breast during the menstrual cycle,” Cell Tissue Res.268(1), 167–177 (1992).
[CrossRef] [PubMed]

Hu, C.

Huang, C. H.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

Huang, Y. Y.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

Hyman, B. T.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A.100(12), 7075–7080 (2003).
[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]

Jansen, M. P.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[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,” Bone50(3), 643–650 (2012).
[CrossRef] [PubMed]

Jemal, A.

A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, and D. Forman, “Global cancer statistics,” CA Cancer J. Clin.61(2), 69–90 (2011).
[CrossRef] [PubMed]

Jones, A.

G. Cox, E. Kable, A. Jones, I. K. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol.141(1), 53–62 (2003).
[CrossRef] [PubMed]

Kable, E.

G. Cox, E. Kable, A. Jones, I. K. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol.141(1), 53–62 (2003).
[CrossRef] [PubMed]

Kajdacsy-Balla, A.

S. E. Holton, M. J. Walsh, A. Kajdacsy-Balla, and R. Bhargava, “Label-free characterization of cancer-activated fibroblasts using infrared spectroscopic imaging,” Biophys. J.101(6), 1513–1521 (2011).
[CrossRef] [PubMed]

Keely, P. J.

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]

Kim, D.

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

Klijn, J. G. M.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[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]

Korom, I.

Krenacs, T.

Kuznetsova, N. V.

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

Kwak, J. T.

J. T. Kwak, R. Reddy, S. Sinha, and R. Bhargava, “Analysis of variance in spectroscopic imaging data from human tissues,” Anal. Chem.84(2), 1063–1069 (2012).
[CrossRef] [PubMed]

Latour, G.

Le Grand, Y.

Lee, H. S.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

Leikin, S.

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

Leithem, S.

Levin, I. W.

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol.23(4), 469–474 (2005).
[CrossRef] [PubMed]

Li, T. H.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

P. J. Su, W. L. Chen, J. B. Hong, T. H. Li, R. J. Wu, C. K. Chou, S. J. Chen, C. Hu, S. J. Lin, and C. Y. Dong, “Discrimination of collagen in normal and pathological skin dermis through second-order susceptibility microscopy,” Opt. Express17(13), 11161–11171 (2009).
[CrossRef] [PubMed]

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

Lin, S. J.

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

P. J. Su, W. L. Chen, J. B. Hong, T. H. Li, R. J. Wu, C. K. Chou, S. J. Chen, C. Hu, S. J. Lin, and C. Y. Dong, “Discrimination of collagen in normal and pathological skin dermis through second-order susceptibility microscopy,” Opt. Express17(13), 11161–11171 (2009).
[CrossRef] [PubMed]

Lindgren, M.

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt.13(5), 054050 (2008).
[CrossRef] [PubMed]

Lindmo, T.

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt.13(5), 054050 (2008).
[CrossRef] [PubMed]

Liotta, L. A.

L. A. Liotta, C. N. Rao, and S. H. Barsky, “Tumor invasion and the extracellular matrix,” Lab. Invest.49(6), 636–649 (1983).
[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]

Look, M. P.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

Losert, W.

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

Loza-Alvarez, P.

S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt.14(1), 014001–014011 (2009).
[CrossRef] [PubMed]

S. Psilodimitrakopoulos, D. Artigas, G. Soria, I. Amat-Roldan, A. M. Planas, and P. Loza-Alvarez, “Quantitative discrimination between endogenous SHG sources in mammalian tissue, based on their polarization response,” Opt. Express17(12), 10168–10176 (2009).
[CrossRef] [PubMed]

Luedtke, D.

Makareeva, E.

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

Manconi, F.

G. Cox, E. Kable, A. Jones, I. K. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol.141(1), 53–62 (2003).
[CrossRef] [PubMed]

Mareel, M.

O. De Wever and M. Mareel, “Role of tissue stroma in cancer cell invasion,” J. Pathol.200(4), 429–447 (2003).
[CrossRef] [PubMed]

Mehta, M. R.

Meijer-van Gelder, M. E.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

Munhoz, F.

Muschler, J.

D. Radisky, J. Muschler, and M. J. Bissell, “Order and disorder: the role of extracellular matrix in epithelial cancer,” Cancer Invest.20(1), 139–153 (2002).
[CrossRef] [PubMed]

Nagase, H.

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

Niebuhr, E.

O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
[CrossRef] [PubMed]

Nielsen, H. L.

O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
[CrossRef] [PubMed]

Nikitin, A. Y.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A.100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Odin, C.

Petersen, O. W.

O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
[CrossRef] [PubMed]

Phillips, C. L.

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

Planas, A. M.

Provenzano, P. P.

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]

Psilodimitrakopoulos, S.

S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt.14(1), 014001–014011 (2009).
[CrossRef] [PubMed]

S. Psilodimitrakopoulos, D. Artigas, G. Soria, I. Amat-Roldan, A. M. Planas, and P. Loza-Alvarez, “Quantitative discrimination between endogenous SHG sources in mammalian tissue, based on their polarization response,” Opt. Express17(12), 10168–10176 (2009).
[CrossRef] [PubMed]

Radisky, D.

D. Radisky, J. Muschler, and M. J. Bissell, “Order and disorder: the role of extracellular matrix in epithelial cancer,” Cancer Invest.20(1), 139–153 (2002).
[CrossRef] [PubMed]

Rank, F.

O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
[CrossRef] [PubMed]

Rao, C. N.

L. A. Liotta, C. N. Rao, and S. H. Barsky, “Tumor invasion and the extracellular matrix,” Lab. Invest.49(6), 636–649 (1983).
[PubMed]

Rao, R. A.

Recher, G.

Reddy, R.

J. T. Kwak, R. Reddy, S. Sinha, and R. Bhargava, “Analysis of variance in spectroscopic imaging data from human tissues,” Anal. Chem.84(2), 1063–1069 (2012).
[CrossRef] [PubMed]

Rønnov-Jessen, L.

O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
[CrossRef] [PubMed]

Rouède, D.

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]

Ruigrok-Ritstier, K.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

Sackett, D. L.

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

Santos, S. I. C. O.

S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt.14(1), 014001–014011 (2009).
[CrossRef] [PubMed]

Schanne-Klein, M. C.

Schor, A. M.

J. E. Ferguson, A. M. Schor, A. Howell, and M. W. J. Ferguson, “Changes in the extracellular matrix of the normal human breast during the menstrual cycle,” Cell Tissue Res.268(1), 167–177 (1992).
[CrossRef] [PubMed]

Sieuwerts, A. M.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

Sinha, S.

J. T. Kwak, R. Reddy, S. Sinha, and R. Bhargava, “Analysis of variance in spectroscopic imaging data from human tissues,” Anal. Chem.84(2), 1063–1069 (2012).
[CrossRef] [PubMed]

Sivaguru, M.

Sleijfer, S.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

So, P. T. C.

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

Soria, G.

Sprecher, A.

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
[CrossRef] [PubMed]

Stamenkovic, I.

I. Stamenkovic, “Extracellular matrix remodelling: the role of matrix metalloproteinases,” J. Pathol.200(4), 448–464 (2003).
[CrossRef] [PubMed]

Stewart, A.

Su, P. J.

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

P. J. Su, W. L. Chen, J. B. Hong, T. H. Li, R. J. Wu, C. K. Chou, S. J. Chen, C. Hu, S. J. Lin, and C. Y. Dong, “Discrimination of collagen in normal and pathological skin dermis through second-order susceptibility microscopy,” Opt. Express17(13), 11161–11171 (2009).
[CrossRef] [PubMed]

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

Sutter, M. B.

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

Tang, P.

Thayil, A. K. N.

S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt.14(1), 014001–014011 (2009).
[CrossRef] [PubMed]

Thrasivoulou, C.

Tiaho, F.

Toussaint, K. C.

Tromberg, B. J.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

van Staveren, I. L.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

Vera, J. C.

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

Villadsen, R.

O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
[CrossRef] [PubMed]

Virich, G.

Visse, R.

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

Walsh, M. J.

S. E. Holton, M. J. Walsh, A. Kajdacsy-Balla, and R. Bhargava, “Label-free characterization of cancer-activated fibroblasts using infrared spectroscopic imaging,” Biophys. J.101(6), 1513–1521 (2011).
[CrossRef] [PubMed]

S. E. Holton, M. J. Walsh, and R. Bhargava, “Subcellular localization of early biochemical transformations in cancer-activated fibroblasts using infrared spectroscopic imaging,” Analyst (Lond.)136(14), 2953–2958 (2011).
[CrossRef] [PubMed]

Ward, E.

A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, and D. Forman, “Global cancer statistics,” CA Cancer J. Clin.61(2), 69–90 (2011).
[CrossRef] [PubMed]

Weaver, V. M.

J. T. Erler and V. M. Weaver, “Three-dimensional context regulation of metastasis,” Clin. Exp. Metastasis26(1), 35–49 (2009).
[CrossRef] [PubMed]

Webb, W. W.

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

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A.100(12), 7075–7080 (2003).
[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, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J.88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A.100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Wu, R. J.

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]

Yeh, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

Zettel, M. L.

Zipfel, W. R.

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

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A.100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Zoumi, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

Am. J. Pathol.

O. W. Petersen, H. L. Nielsen, T. Gudjonsson, R. Villadsen, F. Rank, E. Niebuhr, M. J. Bissell, and L. Rønnov-Jessen, “Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma,” Am. J. Pathol.162(2), 391–402 (2003).
[CrossRef] [PubMed]

Anal. Chem.

J. T. Kwak, R. Reddy, S. Sinha, and R. Bhargava, “Analysis of variance in spectroscopic imaging data from human tissues,” Anal. Chem.84(2), 1063–1069 (2012).
[CrossRef] [PubMed]

Analyst (Lond.)

S. E. Holton, M. J. Walsh, and R. Bhargava, “Subcellular localization of early biochemical transformations in cancer-activated fibroblasts using infrared spectroscopic imaging,” Analyst (Lond.)136(14), 2953–2958 (2011).
[CrossRef] [PubMed]

Appl. Phys. Lett.

W. L. Chen, T. H. Li, P. J. Su, C. K. Chou, P. T. Fwu, S. J. Lin, D. Kim, P. T. C. So, and C. Y. Dong, “Second harmonic generation chi tensor microscopy for tissue imaging,” Appl. Phys. Lett.94, 3 (2009).

Biomaterials

P. J. Su, W. L. Chen, T. H. Li, C. K. Chou, T. H. Chen, Y. Y. Ho, C. H. Huang, S. J. Chang, Y. Y. Huang, H. S. Lee, and C. Y. Dong, “The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue,” Biomaterials31(36), 9415–9421 (2010).
[CrossRef] [PubMed]

Biomed. Opt. Express

Biophys. J.

S. E. Holton, M. J. Walsh, A. Kajdacsy-Balla, and R. Bhargava, “Label-free characterization of cancer-activated fibroblasts using infrared spectroscopic imaging,” Biophys. J.101(6), 1513–1521 (2011).
[CrossRef] [PubMed]

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

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J.50(4), 693–712 (1986).
[CrossRef] [PubMed]

BMC Med.

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]

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]

Bone

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,” Bone50(3), 643–650 (2012).
[CrossRef] [PubMed]

CA Cancer J. Clin.

A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, and D. Forman, “Global cancer statistics,” CA Cancer J. Clin.61(2), 69–90 (2011).
[CrossRef] [PubMed]

Cancer Invest.

D. Radisky, J. Muschler, and M. J. Bissell, “Order and disorder: the role of extracellular matrix in epithelial cancer,” Cancer Invest.20(1), 139–153 (2002).
[CrossRef] [PubMed]

Cancer Res.

E. Makareeva, S. J. Han, J. C. Vera, D. L. Sackett, K. Holmbeck, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion,” Cancer Res.70(11), 4366–4374 (2010).
[CrossRef] [PubMed]

Cell Tissue Res.

J. E. Ferguson, A. M. Schor, A. Howell, and M. W. J. Ferguson, “Changes in the extracellular matrix of the normal human breast during the menstrual cycle,” Cell Tissue Res.268(1), 167–177 (1992).
[CrossRef] [PubMed]

Clin. Cancer Res.

J. Helleman, M. P. Jansen, K. Ruigrok-Ritstier, I. L. van Staveren, M. P. Look, M. E. Meijer-van Gelder, A. M. Sieuwerts, J. G. M. Klijn, S. Sleijfer, J. A. Foekens, and E. M. Berns, “Association of an extracellular matrix gene cluster with breast cancer prognosis and endocrine therapy response,” Clin. Cancer Res.14(17), 5555–5564 (2008).
[CrossRef] [PubMed]

Clin. Exp. Metastasis

J. T. Erler and V. M. Weaver, “Three-dimensional context regulation of metastasis,” Clin. Exp. Metastasis26(1), 35–49 (2009).
[CrossRef] [PubMed]

Eur. J. Cancer

D. Barkan, J. E. Green, and A. F. Chambers, “Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth,” Eur. J. Cancer46(7), 1181–1188 (2010).
[CrossRef] [PubMed]

J. Biol. Chem.

S. J. Han, E. Makareeva, N. V. Kuznetsova, A. M. DeRidder, M. B. Sutter, W. Losert, C. L. Phillips, R. Visse, H. Nagase, and S. Leikin, “Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases,” J. Biol. Chem.285(29), 22276–22281 (2010).
[CrossRef] [PubMed]

J. Biomed. Opt.

T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lange Davies, “Second-harmonic generation in collagen as a potential cancer diagnostic parameter,” J. Biomed. Opt.13(5), 054050 (2008).
[CrossRef] [PubMed]

S. Psilodimitrakopoulos, S. I. C. O. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt.14(1), 014001–014011 (2009).
[CrossRef] [PubMed]

J. Natl. Cancer Inst.

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]

J. Pathol.

O. De Wever and M. Mareel, “Role of tissue stroma in cancer cell invasion,” J. Pathol.200(4), 429–447 (2003).
[CrossRef] [PubMed]

I. Stamenkovic, “Extracellular matrix remodelling: the role of matrix metalloproteinases,” J. Pathol.200(4), 448–464 (2003).
[CrossRef] [PubMed]

J. Struct. Biol.

G. Cox, E. Kable, A. Jones, I. K. Fraser, F. Manconi, and M. D. Gorrell, “3-dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol.141(1), 53–62 (2003).
[CrossRef] [PubMed]

Lab. Invest.

L. A. Liotta, C. N. Rao, and S. H. Barsky, “Tumor invasion and the extracellular matrix,” Lab. Invest.49(6), 636–649 (1983).
[PubMed]

Nat. Biotechnol.

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]

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol.23(4), 469–474 (2005).
[CrossRef] [PubMed]

Opt. Express

S. Brasselet, D. Aït-Belkacem, A. Gasecka, F. Munhoz, S. Brustlein, and S. Brasselet, “Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging,” Opt. Express18(14), 14859–14870 (2010).
[CrossRef] [PubMed]

I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Polarization-resolved Second Harmonic microscopy in anisotropic thick tissues,” Opt. Express18(18), 19339–19352 (2010).
[CrossRef] [PubMed]

F. Tiaho, G. Recher, and D. Rouède, “Estimation of helical angles of myosin and collagen by second harmonic generation imaging microscopy,” Opt. Express15(19), 12286–12295 (2007).
[CrossRef] [PubMed]

X. Han, R. M. Burke, M. L. Zettel, P. Tang, and E. B. Brown, “Second harmonic properties of tumor collagen: determining the structural relationship between reactive stroma and healthy stroma,” Opt. Express16(3), 1846–1859 (2008).
[CrossRef] [PubMed]

R. A. Rao, M. R. Mehta, and K. C. Toussaint., “Fourier transform-second-harmonic generation imaging of biological tissues,” Opt. Express17(17), 14534–14542 (2009).
[CrossRef] [PubMed]

M. Sivaguru, S. Durgam, R. Ambekar, D. Luedtke, G. Fried, A. Stewart, and K. C. Toussaint., “Quantitative analysis of collagen fiber organization in injured tendons using Fourier transform-second harmonic generation imaging,” Opt. Express18(24), 24983–24993 (2010).
[CrossRef] [PubMed]

P. J. Su, W. L. Chen, J. B. Hong, T. H. Li, R. J. Wu, C. K. Chou, S. J. Chen, C. Hu, S. J. Lin, and C. Y. Dong, “Discrimination of collagen in normal and pathological skin dermis through second-order susceptibility microscopy,” Opt. Express17(13), 11161–11171 (2009).
[CrossRef] [PubMed]

C. Odin, T. Guilbert, A. Alkilani, O. P. Boryskina, V. Fleury, and Y. Le Grand, “Collagen and myosin characterization by orientation field second harmonic microscopy,” Opt. Express16(20), 16151–16165 (2008).
[CrossRef] [PubMed]

S. Psilodimitrakopoulos, D. Artigas, G. Soria, I. Amat-Roldan, A. M. Planas, and P. Loza-Alvarez, “Quantitative discrimination between endogenous SHG sources in mammalian tissue, based on their polarization response,” Opt. Express17(12), 10168–10176 (2009).
[CrossRef] [PubMed]

Opt. Lett.

Proc. Natl. Acad. Sci. U.S.A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A.100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Other

“Cancer Facts & Figures—2012American Cancer Society, 2012).

B. N. Datta, Textbook of Pathology (Jaypee Brothers Medical, 2008).

S. Srivastava, Molecular Pathology of Early Cancer (IOS, 1998).

I. W. Levin and R. Bhargava, “Fourier transform infrared vibrational spectroscopic imaging: integrating microscopy and molecular recognition,” in Annual Review of Physical Chemistry (Annual Reviews, Palo Alto, 2005), Vol. 56, pp. 429–474.

B. E. A. Saleh and M. C. Teich, Fundamentals of Photonics (Wiley Interscience, 2007).

P. N. Butcher and D. Cotter, The Elements of Nonlinear Optics (Cambridge University Press, 2003).

B. Y. Jiang and S. W. Chu, “Trigonal symmetry of type I collagen probed by SHG polarization anisotropy,” in Conference on Lasers and Electro-Optics/Quantum Electronics and Laser Science Conference and Photonic Applications Systems Technologies, OSA Technical Digest (CD) (Optical Society of America, 2008), paper JWA30.

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Figures (9)

Fig. 1
Fig. 1

Illustration of the geometric arrangement of a single collagen fiber relative to an applied electric field. The emitted SHG signal after spectral filtering is shown in blue. Details are provided in the text.

Fig. 2
Fig. 2

Simulated plots of normalized SHG intensity as a function of polarization angle (polarization spectrum) for collagen fibers possessing a) trigonal 3m and b) cylindrical C6 crystal class symmetry.

Fig. 3
Fig. 3

Experimental setup of the SHG microscope with forward and backward collection geometries. Details of the setup are provided in the text.

Fig. 4
Fig. 4

H&E stained and SHG images of three cores for normal, hyperplastic, dysplastic, and malignant breast tissues. Scale bar: 250 µm.

Fig. 5
Fig. 5

Bar plot of the number of dark regions for the four tissue conditions.

Fig. 6
Fig. 6

Bar plot of the parameter, A.I. ratio, for the four pathologic conditions.

Fig. 7
Fig. 7

Normalized SHG intensity as a function of polarization angle (or polarization spectrum) for a) normal, b) hyperplastic, c) dysplastic, and d) malignant breast tissue.

Fig. 8
Fig. 8

Bar plot of the tensor elements (d15/d31, d33/d31, d22/d31) for normal, hyperplastic, dysplastic, and malignant tissues.

Fig. 9
Fig. 9

Percentage of abnormal collagen fibers as a function of breast pathology.

Tables (1)

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Table 1 Comparison Tests between Breast Tissue Conditionsa

Equations (7)

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P= χ (1) E+ χ (2) E 2 + χ (3) E 3 +,
P i (2ω)=2 jk d ijk E j (ω) E k (ω) ,i,j,k=1,2,3,
[ P x (2ω) P y (2ω) P z (2ω) ]=2[ d 11 d 12 d 13 d 14 d 15 d 16 d 21 d 22 d 23 d 24 d 25 d 26 d 31 d 32 d 33 d 34 d 35 d 36 ] [ E x (ω) 2 E y (ω) 2 E z (ω) 2 2 E z (ω) E y (ω) 2 E x (ω) E z (ω) 2 E y (ω) E x (ω) ] .
[ 0 0 0 0 d 15 d 22 d 22 d 22 0 d 15 0 0 d 31 d 31 d 33 0 0 0 ] ,
P x (2ω)=2 d 15 E x ( ω ) E z ( ω )2 d 22 E y ( ω ) E x ( ω ) P y (2ω)= d 22 ( E x 2 ( ω )+ E y 2 ( ω ) )+2 d 15 E z ( ω ) E y ( ω ) P z (2ω)= d 31 ( E x 2 ( ω )+ E y 2 ( ω ) )+ d 33 E z 2 ( ω ) .
I(2ω)~ [ ( d 22 sin 2 α+ d 15 sin2α ) 2 + ( d 31 sin 2 α+ d 33 cos 2 α ) 2 ] .
I(2ω)~ [ ( d 22 d 31 sin 2 α+ d 15 d 31 sin2α ) 2 + ( sin 2 α+ d 33 d 31 cos 2 α ) 2 ] ,

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