Abstract

Preoperative neoadjuvant treatment in locally advanced breast cancer is recognized as an effective adjuvant therapy, as it improves treatment outcomes. However, the potential complications remain a threat, so there is an urgent clinical need to assess both the tumor response and changes in its microenvironment using non-invasive and precise identification techniques. Here, two-photon microscopy was employed to detect morphological alterations in breast cancer progression and recession throughout chemotherapy. The changes in structure were analyzed based on the autofluorescence and collagen of differing statuses. Parameters, including optical redox ratio, the ratio of second harmonic generation and auto-fluorescence signal, collagen density, and collagen shape orientation, were studied. Results indicate that these parameters are potential indicators for evaluating breast tumors and their microenvironment changes during progression and chemotherapy. Combined analyses of these parameters could provide a quantitative, novel method for monitoring tumor therapy.

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

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2017 (2)

T. M. Cannon, A. T. Shah, and M. C. Skala, “Autofluorescence imaging captures heterogeneous drug response differences between 2D and 3D breast cancer cultures,” Biomed. Opt. Express 8(3), 1911–1925 (2017).
[Crossref] [PubMed]

W. Liang, G. Hall, B. Messerschmidt, M.-J. Li, and X. Li, “Nonlinear optical endomicroscopy for label-free functional histology in vivo,” Light Sci. Appl. 6(11), e17082 (2017).
[Crossref]

2016 (6)

S. Chakraborty, F.-S. Nian, J.-W. Tsai, A. Karmenyan, and A. Chiou, “Quantification of the metabolic state in cell-model of Parkinson’s disease by fluorescence lifetime imaging microscopy,” Sci. Rep. 6(1), 19145 (2016).
[Crossref] [PubMed]

R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer statistics, 2016,” CA Cancer J. Clin. 66(1), 7–30 (2016).
[Crossref] [PubMed]

S. Aminololama-Shakeri, C. K. Abbey, P. Gazi, N. D. Prionas, A. Nosratieh, C.-S. Li, J. M. Boone, and K. K. Lindfors, “Differentiation of ductal carcinoma in-situ from benign micro-calcifications by dedicated breast computed tomography,” Eur. J. Radiol. 85(1), 297–303 (2016).
[Crossref] [PubMed]

Y. Zhu, X. Wang, J. Chen, J. Zhang, F. Meng, C. Deng, R. Cheng, J. Feijen, and Z. Zhong, “Bioresponsive and fluorescent hyaluronic acid-iodixanol nanogels for targeted X-ray computed tomography imaging and chemotherapy of breast tumors,” J. Control. Release 244(Pt B), 229–239 (2016).
[Crossref] [PubMed]

S. Ait-Mohand, V. Dumulon-Perreault, F. Benard, and B. Guerin, “Design optimization of a new 64Cu/NOTA truncated NPY analog with improved stability and Y1 affinity, the first step toward successful breast cancer PET Imaging,” J. Nucl. Med. 57(s2), 1076 (2016).

W. M. Allen, L. Chin, P. Wijesinghe, R. W. Kirk, B. Latham, D. D. Sampson, C. M. Saunders, and B. F. Kennedy, “Wide-field optical coherence micro-elastography for intraoperative assessment of human breast cancer margins,” Biomed. Opt. Express 7(10), 4139–4153 (2016).
[Crossref] [PubMed]

2015 (7)

K. Tilbury and P. J. Campagnola, “Applications of second-harmonic generation imaging microscopy in ovarian and breast cancer,” Perspect. Medicin. Chem. 7(1), 21–32 (2015).
[PubMed]

L. L. B. Ponto, Y. Menda, V. A. Magnotta, T. H. Yamada, N. L. Denburg, and S. K. Schultz, “Frontal hypometabolism in elderly breast cancer survivors determined by [(18)F]fluorodeoxyglucose (FDG) positron emission tomography (PET): a pilot study,” Int. J. Geriatr. Psychiatry 30(6), 587–594 (2015).
[Crossref] [PubMed]

G. J. Wengert, T. H. Helbich, W.-D. Vogl, P. Baltzer, G. Langs, M. Weber, W. Bogner, S. Gruber, S. Trattnig, and K. Pinker, “Introduction of an Automated User-Independent Quantitative Volumetric Magnetic Resonance Imaging Breast Density Measurement System Using the Dixon Sequence: Comparison With Mammographic Breast Density Assessment,” Invest. Radiol. 50(2), 73–80 (2015).
[Crossref] [PubMed]

C. E. DeSantis, F. Bray, J. Ferlay, J. Lortet-Tieulent, B. O. Anderson, and A. Jemal, “International variation in female breast cancer incidence and mortality rates,” Cancer Epidemiol. Biomarkers Prev. 24(10), 1495–1506 (2015).
[Crossref] [PubMed]

C. Jackisch, F. A. Scappaticci, D. Heinzmann, F. Bisordi, T. Schreitmüller, G. Minckwitz, and J. Cortés, “Neoadjuvant breast cancer treatment as a sensitive setting for trastuzumab biosimilar development and extrapolation,” Future Oncol. 11(1), 61–71 (2015).
[Crossref] [PubMed]

C. W. Huo, G. Chew, P. Hill, D. Huang, W. Ingman, L. Hodson, K. A. Brown, A. Magenau, A. H. Allam, E. McGhee, P. Timpson, M. A. Henderson, E. W. Thompson, and K. Britt, “High mammographic density is associated with an increase in stromal collagen and immune cells within the mammary epithelium,” Breast Cancer Res. 17(1), 79 (2015).
[Crossref] [PubMed]

K. A. Burke, R. P. Dawes, M. K. Cheema, A. Van Hove, D. S. Benoit, S. W. Perry, and E. Brown, “Second-harmonic generation scattering directionality predicts tumor cell motility in collagen gels,” J. Biomed. Opt. 20(5), 051024 (2015).
[Crossref] [PubMed]

2014 (7)

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative optical imaging of primary tumor organoid metabolism predicts drug response in breast cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

J. S. Bredfeldt, Y. Liu, C. A. Pehlke, M. W. Conklin, J. M. Szulczewski, D. R. Inman, P. J. Keely, R. D. Nowak, T. R. Mackie, and K. W. Eliceiri, “Computational segmentation of collagen fibers from second-harmonic generation images of breast cancer,” J. Biomed. Opt. 19(1), 016007 (2014).
[Crossref] [PubMed]

K. Cai, H. N. Xu, A. Singh, L. Moon, M. Haris, R. Reddy, and L. Z. Li, “Breast cancer redox heterogeneity detectable with chemical exchange saturation transfer (CEST) MRI,” Mol. Imaging Biol. 16(5), 670–679 (2014).
[Crossref] [PubMed]

G. Song, D. B. Darr, C. M. Santos, M. Ross, A. Valdivia, J. L. Jordan, B. R. Midkiff, S. Cohen, N. Nikolaishvili-Feinberg, C. R. Miller, T. K. Tarrant, A. B. Rogers, A. C. Dudley, C. M. Perou, and W. C. Zamboni, “Effects of tumor microenvironment heterogeneity on nanoparticle disposition and efficacy in breast cancer tumor models,” Clin. Cancer Res. 20(23), 6083–6095 (2014).
[Crossref] [PubMed]

C. F. Buchanan, E. E. Voigt, C. S. Szot, J. W. Freeman, P. P. Vlachos, and M. N. Rylander, “Three-dimensional microfluidic collagen hydrogels for investigating flow-mediated tumor-endothelial signaling and vascular organization,” Tissue Eng. Part C Methods 20(1), 64–75 (2014).
[Crossref] [PubMed]

L. Scolaro, R. A. McLaughlin, B. F. Kennedy, C. M. Saunders, and D. D. Sampson, “A review of optical coherence tomography in breast cancer,” Photonics Lasers Med. 3(3), 225–240 (2014).
[Crossref]

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

2013 (3)

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

J. S. Sung and D. D. Dershaw, “Breast magnetic resonance imaging for screening high-risk women,” Magn. Reson. Imaging Clin. N. Am. 21(3), 509–517 (2013).
[Crossref] [PubMed]

T. Mammoto, A. Jiang, E. Jiang, D. Panigrahy, M. W. Kieran, and A. Mammoto, “Role of collagen matrix in tumor angiogenesis and glioblastoma multiforme progression,” Am. J. Pathol. 183(4), 1293–1305 (2013).
[Crossref] [PubMed]

2012 (3)

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

S. W. Perry, R. M. Burke, and E. B. Brown, “Two-photon and second harmonic microscopy in clinical and translational cancer research,” Ann. Biomed. Eng. 40(2), 277–291 (2012).
[Crossref] [PubMed]

2011 (2)

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]

S. Wu, H. Li, H. Yang, X. Zhang, Z. Li, and S. Xu, “Quantitative analysis on collagen morphology in aging skin based on multiphoton microscopy,” J. Biomed. Opt. 16(4), 040502 (2011).
[Crossref] [PubMed]

2009 (1)

P. P. Provenzano, K. W. Eliceiri, and P. J. Keely, “Multiphoton microscopy and fluorescence lifetime imaging microscopy (FLIM) to monitor metastasis and the tumor microenvironment,” Clin. Exp. Metastasis 26(4), 357–370 (2009).
[Crossref] [PubMed]

2008 (2)

C. Liedtke, C. Mazouni, K. R. Hess, F. André, A. Tordai, J. A. Mejia, W. F. Symmans, A. M. Gonzalez-Angulo, B. Hennessy, M. Green, M. Cristofanilli, G. N. Hortobagyi, and L. Pusztai, “Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer,” J. Clin. Oncol. 26(8), 1275–1281 (2008).
[Crossref] [PubMed]

G. Falzon, S. Pearson, and R. Murison, “Analysis of collagen fibre shape changes in breast cancer,” Phys. Med. Biol. 53(23), 6641–6652 (2008).
[Crossref] [PubMed]

2007 (2)

W. F. Symmans, F. Peintinger, C. Hatzis, R. Rajan, H. Kuerer, V. Valero, L. Assad, A. Poniecka, B. Hennessy, M. Green, A. U. Buzdar, S. E. Singletary, G. N. Hortobagyi, and L. Pusztai, “Measurement of residual breast cancer burden to predict survival after neoadjuvant chemotherapy,” J. Clin. Oncol. 25(28), 4414–4422 (2007).
[Crossref] [PubMed]

J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit oesophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys. 9(7), 212 (2007).
[Crossref]

2006 (3)

C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
[Crossref] [PubMed]

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38–54 (2006).
[Crossref] [PubMed]

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2004 (1)

S. A. Boppart, W. Luo, D. L. Marks, and K. W. Singletary, “Optical coherence tomography: feasibility for basic research and image-guided surgery of breast cancer,” Breast Cancer Res. Treat. 84(2), 85–97 (2004).
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2003 (1)

A. Uppal and P. K. Gupta, “Measurement of NADH concentration in normal and malignant human tissues from breast and oral cavity,” Biotechnol. Appl. Biochem. 37(1), 45–50 (2003).
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2002 (2)

S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J. 82(5), 2811–2825 (2002).
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S. M. Chung, “Safety issues in magnetic resonance imaging,” J. Neuroophthalmol. 22(1), 35–39 (2002).
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1992 (1)

L. Lam, S.-W. Lee, and C. Y. Suen, “Thinning methodologies-a comprehensive survey,” IEEE Trans. Pattern Anal. Mach. Intell. 14(9), 869–885 (1992).
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1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
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1979 (2)

N. Otsu, “Threshold Selection Method from Gray-Level Histograms,” IEEE Trans. Syst. Man Cybern. 9(1), 62–66 (1979).
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B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

Abbey, C. K.

S. Aminololama-Shakeri, C. K. Abbey, P. Gazi, N. D. Prionas, A. Nosratieh, C.-S. Li, J. M. Boone, and K. K. Lindfors, “Differentiation of ductal carcinoma in-situ from benign micro-calcifications by dedicated breast computed tomography,” Eur. J. Radiol. 85(1), 297–303 (2016).
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Ait-Mohand, S.

S. Ait-Mohand, V. Dumulon-Perreault, F. Benard, and B. Guerin, “Design optimization of a new 64Cu/NOTA truncated NPY analog with improved stability and Y1 affinity, the first step toward successful breast cancer PET Imaging,” J. Nucl. Med. 57(s2), 1076 (2016).

Allam, A. H.

C. W. Huo, G. Chew, P. Hill, D. Huang, W. Ingman, L. Hodson, K. A. Brown, A. Magenau, A. H. Allam, E. McGhee, P. Timpson, M. A. Henderson, E. W. Thompson, and K. Britt, “High mammographic density is associated with an increase in stromal collagen and immune cells within the mammary epithelium,” Breast Cancer Res. 17(1), 79 (2015).
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Allen, W. M.

Ambekar, R.

Aminololama-Shakeri, S.

S. Aminololama-Shakeri, C. K. Abbey, P. Gazi, N. D. Prionas, A. Nosratieh, C.-S. Li, J. M. Boone, and K. K. Lindfors, “Differentiation of ductal carcinoma in-situ from benign micro-calcifications by dedicated breast computed tomography,” Eur. J. Radiol. 85(1), 297–303 (2016).
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Anderson, B. O.

C. E. DeSantis, F. Bray, J. Ferlay, J. Lortet-Tieulent, B. O. Anderson, and A. Jemal, “International variation in female breast cancer incidence and mortality rates,” Cancer Epidemiol. Biomarkers Prev. 24(10), 1495–1506 (2015).
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André, F.

C. Liedtke, C. Mazouni, K. R. Hess, F. André, A. Tordai, J. A. Mejia, W. F. Symmans, A. M. Gonzalez-Angulo, B. Hennessy, M. Green, M. Cristofanilli, G. N. Hortobagyi, and L. Pusztai, “Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer,” J. Clin. Oncol. 26(8), 1275–1281 (2008).
[Crossref] [PubMed]

Arteaga, C. L.

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative optical imaging of primary tumor organoid metabolism predicts drug response in breast cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Assad, L.

W. F. Symmans, F. Peintinger, C. Hatzis, R. Rajan, H. Kuerer, V. Valero, L. Assad, A. Poniecka, B. Hennessy, M. Green, A. U. Buzdar, S. E. Singletary, G. N. Hortobagyi, and L. Pusztai, “Measurement of residual breast cancer burden to predict survival after neoadjuvant chemotherapy,” J. Clin. Oncol. 25(28), 4414–4422 (2007).
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Aurisicchio, L.

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative optical imaging of primary tumor organoid metabolism predicts drug response in breast cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

Baltzer, P.

G. J. Wengert, T. H. Helbich, W.-D. Vogl, P. Baltzer, G. Langs, M. Weber, W. Bogner, S. Gruber, S. Trattnig, and K. Pinker, “Introduction of an Automated User-Independent Quantitative Volumetric Magnetic Resonance Imaging Breast Density Measurement System Using the Dixon Sequence: Comparison With Mammographic Breast Density Assessment,” Invest. Radiol. 50(2), 73–80 (2015).
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Benard, F.

S. Ait-Mohand, V. Dumulon-Perreault, F. Benard, and B. Guerin, “Design optimization of a new 64Cu/NOTA truncated NPY analog with improved stability and Y1 affinity, the first step toward successful breast cancer PET Imaging,” J. Nucl. Med. 57(s2), 1076 (2016).

Benoit, D. S.

K. A. Burke, R. P. Dawes, M. K. Cheema, A. Van Hove, D. S. Benoit, S. W. Perry, and E. Brown, “Second-harmonic generation scattering directionality predicts tumor cell motility in collagen gels,” J. Biomed. Opt. 20(5), 051024 (2015).
[Crossref] [PubMed]

Berton-Rigaud, D.

C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
[Crossref] [PubMed]

Bhargava, R.

Bisordi, F.

C. Jackisch, F. A. Scappaticci, D. Heinzmann, F. Bisordi, T. Schreitmüller, G. Minckwitz, and J. Cortés, “Neoadjuvant breast cancer treatment as a sensitive setting for trastuzumab biosimilar development and extrapolation,” Future Oncol. 11(1), 61–71 (2015).
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Bogner, W.

G. J. Wengert, T. H. Helbich, W.-D. Vogl, P. Baltzer, G. Langs, M. Weber, W. Bogner, S. Gruber, S. Trattnig, and K. Pinker, “Introduction of an Automated User-Independent Quantitative Volumetric Magnetic Resonance Imaging Breast Density Measurement System Using the Dixon Sequence: Comparison With Mammographic Breast Density Assessment,” Invest. Radiol. 50(2), 73–80 (2015).
[Crossref] [PubMed]

Boone, J. M.

S. Aminololama-Shakeri, C. K. Abbey, P. Gazi, N. D. Prionas, A. Nosratieh, C.-S. Li, J. M. Boone, and K. K. Lindfors, “Differentiation of ductal carcinoma in-situ from benign micro-calcifications by dedicated breast computed tomography,” Eur. J. Radiol. 85(1), 297–303 (2016).
[Crossref] [PubMed]

Boppart, S. A.

S. A. Boppart, W. Luo, D. L. Marks, and K. W. Singletary, “Optical coherence tomography: feasibility for basic research and image-guided surgery of breast cancer,” Breast Cancer Res. Treat. 84(2), 85–97 (2004).
[Crossref] [PubMed]

Bourbouloux, E.

C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
[Crossref] [PubMed]

Bouriel, C.

C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
[Crossref] [PubMed]

Bray, F.

C. E. DeSantis, F. Bray, J. Ferlay, J. Lortet-Tieulent, B. O. Anderson, and A. Jemal, “International variation in female breast cancer incidence and mortality rates,” Cancer Epidemiol. Biomarkers Prev. 24(10), 1495–1506 (2015).
[Crossref] [PubMed]

Bredfeldt, J. S.

J. S. Bredfeldt, Y. Liu, C. A. Pehlke, M. W. Conklin, J. M. Szulczewski, D. R. Inman, P. J. Keely, R. D. Nowak, T. R. Mackie, and K. W. Eliceiri, “Computational segmentation of collagen fibers from second-harmonic generation images of breast cancer,” J. Biomed. Opt. 19(1), 016007 (2014).
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J. S. Bredfeldt, Y. Liu, M. W. Conklin, P. J. Keely, T. R. Mackie, and K. W. Eliceiri, “Automated quantification of aligned collagen for human breast carcinoma prognosis,” J. Pathol. Inform. 5(1), 28 (2014).
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Bridji, B.

C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
[Crossref] [PubMed]

Britt, K.

C. W. Huo, G. Chew, P. Hill, D. Huang, W. Ingman, L. Hodson, K. A. Brown, A. Magenau, A. H. Allam, E. McGhee, P. Timpson, M. A. Henderson, E. W. Thompson, and K. Britt, “High mammographic density is associated with an increase in stromal collagen and immune cells within the mammary epithelium,” Breast Cancer Res. 17(1), 79 (2015).
[Crossref] [PubMed]

Brown, E.

K. A. Burke, R. P. Dawes, M. K. Cheema, A. Van Hove, D. S. Benoit, S. W. Perry, and E. Brown, “Second-harmonic generation scattering directionality predicts tumor cell motility in collagen gels,” J. Biomed. Opt. 20(5), 051024 (2015).
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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 (2012).
[Crossref] [PubMed]

Brown, E. B.

S. W. Perry, R. M. Burke, and E. B. Brown, “Two-photon and second harmonic microscopy in clinical and translational cancer research,” Ann. Biomed. Eng. 40(2), 277–291 (2012).
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Brown, K. A.

C. W. Huo, G. Chew, P. Hill, D. Huang, W. Ingman, L. Hodson, K. A. Brown, A. Magenau, A. H. Allam, E. McGhee, P. Timpson, M. A. Henderson, E. W. Thompson, and K. Britt, “High mammographic density is associated with an increase in stromal collagen and immune cells within the mammary epithelium,” Breast Cancer Res. 17(1), 79 (2015).
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Buchanan, C. F.

C. F. Buchanan, E. E. Voigt, C. S. Szot, J. W. Freeman, P. P. Vlachos, and M. N. Rylander, “Three-dimensional microfluidic collagen hydrogels for investigating flow-mediated tumor-endothelial signaling and vascular organization,” Tissue Eng. Part C Methods 20(1), 64–75 (2014).
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Bückle, R.

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 (2012).
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Burke, K. A.

K. A. Burke, R. P. Dawes, M. K. Cheema, A. Van Hove, D. S. Benoit, S. W. Perry, and E. Brown, “Second-harmonic generation scattering directionality predicts tumor cell motility in collagen gels,” J. Biomed. Opt. 20(5), 051024 (2015).
[Crossref] [PubMed]

Burke, R. M.

S. W. Perry, R. M. Burke, and E. B. Brown, “Two-photon and second harmonic microscopy in clinical and translational cancer research,” Ann. Biomed. Eng. 40(2), 277–291 (2012).
[Crossref] [PubMed]

Buzdar, A. U.

W. F. Symmans, F. Peintinger, C. Hatzis, R. Rajan, H. Kuerer, V. Valero, L. Assad, A. Poniecka, B. Hennessy, M. Green, A. U. Buzdar, S. E. Singletary, G. N. Hortobagyi, and L. Pusztai, “Measurement of residual breast cancer burden to predict survival after neoadjuvant chemotherapy,” J. Clin. Oncol. 25(28), 4414–4422 (2007).
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Cai, K.

K. Cai, H. N. Xu, A. Singh, L. Moon, M. Haris, R. Reddy, and L. Z. Li, “Breast cancer redox heterogeneity detectable with chemical exchange saturation transfer (CEST) MRI,” Mol. Imaging Biol. 16(5), 670–679 (2014).
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Campagnola, P. J.

K. Tilbury and P. J. Campagnola, “Applications of second-harmonic generation imaging microscopy in ovarian and breast cancer,” Perspect. Medicin. Chem. 7(1), 21–32 (2015).
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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), 38–54 (2006).
[Crossref] [PubMed]

Campion, L.

C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
[Crossref] [PubMed]

Campone, M.

C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
[Crossref] [PubMed]

Cannon, T. M.

Chakraborty, S.

S. Chakraborty, F.-S. Nian, J.-W. Tsai, A. Karmenyan, and A. Chiou, “Quantification of the metabolic state in cell-model of Parkinson’s disease by fluorescence lifetime imaging microscopy,” Sci. Rep. 6(1), 19145 (2016).
[Crossref] [PubMed]

Chance, B.

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

Chatal, J. F.

C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
[Crossref] [PubMed]

Cheema, M. K.

K. A. Burke, R. P. Dawes, M. K. Cheema, A. Van Hove, D. S. Benoit, S. W. Perry, and E. Brown, “Second-harmonic generation scattering directionality predicts tumor cell motility in collagen gels,” J. Biomed. Opt. 20(5), 051024 (2015).
[Crossref] [PubMed]

Chen, J.

Y. Zhu, X. Wang, J. Chen, J. Zhang, F. Meng, C. Deng, R. Cheng, J. Feijen, and Z. Zhong, “Bioresponsive and fluorescent hyaluronic acid-iodixanol nanogels for targeted X-ray computed tomography imaging and chemotherapy of breast tumors,” J. Control. Release 244(Pt B), 229–239 (2016).
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J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit oesophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys. 9(7), 212 (2007).
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Chen, R.

J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit oesophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys. 9(7), 212 (2007).
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Cheng, R.

Y. Zhu, X. Wang, J. Chen, J. Zhang, F. Meng, C. Deng, R. Cheng, J. Feijen, and Z. Zhong, “Bioresponsive and fluorescent hyaluronic acid-iodixanol nanogels for targeted X-ray computed tomography imaging and chemotherapy of breast tumors,” J. Control. Release 244(Pt B), 229–239 (2016).
[Crossref] [PubMed]

Chew, G.

C. W. Huo, G. Chew, P. Hill, D. Huang, W. Ingman, L. Hodson, K. A. Brown, A. Magenau, A. H. Allam, E. McGhee, P. Timpson, M. A. Henderson, E. W. Thompson, and K. Britt, “High mammographic density is associated with an increase in stromal collagen and immune cells within the mammary epithelium,” Breast Cancer Res. 17(1), 79 (2015).
[Crossref] [PubMed]

Chin, L.

Chiou, A.

S. Chakraborty, F.-S. Nian, J.-W. Tsai, A. Karmenyan, and A. Chiou, “Quantification of the metabolic state in cell-model of Parkinson’s disease by fluorescence lifetime imaging microscopy,” Sci. Rep. 6(1), 19145 (2016).
[Crossref] [PubMed]

Chung, S. M.

S. M. Chung, “Safety issues in magnetic resonance imaging,” J. Neuroophthalmol. 22(1), 35–39 (2002).
[Crossref] [PubMed]

Ciliberto, G.

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative optical imaging of primary tumor organoid metabolism predicts drug response in breast cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

Clouet, M.

C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
[Crossref] [PubMed]

Cohen, S.

G. Song, D. B. Darr, C. M. Santos, M. Ross, A. Valdivia, J. L. Jordan, B. R. Midkiff, S. Cohen, N. Nikolaishvili-Feinberg, C. R. Miller, T. K. Tarrant, A. B. Rogers, A. C. Dudley, C. M. Perou, and W. C. Zamboni, “Effects of tumor microenvironment heterogeneity on nanoparticle disposition and efficacy in breast cancer tumor models,” Clin. Cancer Res. 20(23), 6083–6095 (2014).
[Crossref] [PubMed]

Conklin, M. W.

J. S. Bredfeldt, Y. Liu, C. A. Pehlke, M. W. Conklin, J. M. Szulczewski, D. R. Inman, P. J. Keely, R. D. Nowak, T. R. Mackie, and K. W. Eliceiri, “Computational segmentation of collagen fibers from second-harmonic generation images of breast cancer,” J. Biomed. Opt. 19(1), 016007 (2014).
[Crossref] [PubMed]

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

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]

Cook, R. S.

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative optical imaging of primary tumor organoid metabolism predicts drug response in breast cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Cortés, J.

C. Jackisch, F. A. Scappaticci, D. Heinzmann, F. Bisordi, T. Schreitmüller, G. Minckwitz, and J. Cortés, “Neoadjuvant breast cancer treatment as a sensitive setting for trastuzumab biosimilar development and extrapolation,” Future Oncol. 11(1), 61–71 (2015).
[Crossref] [PubMed]

Cristofanilli, M.

C. Liedtke, C. Mazouni, K. R. Hess, F. André, A. Tordai, J. A. Mejia, W. F. Symmans, A. M. Gonzalez-Angulo, B. Hennessy, M. Green, M. Cristofanilli, G. N. Hortobagyi, and L. Pusztai, “Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer,” J. Clin. Oncol. 26(8), 1275–1281 (2008).
[Crossref] [PubMed]

Darr, D. B.

G. Song, D. B. Darr, C. M. Santos, M. Ross, A. Valdivia, J. L. Jordan, B. R. Midkiff, S. Cohen, N. Nikolaishvili-Feinberg, C. R. Miller, T. K. Tarrant, A. B. Rogers, A. C. Dudley, C. M. Perou, and W. C. Zamboni, “Effects of tumor microenvironment heterogeneity on nanoparticle disposition and efficacy in breast cancer tumor models,” Clin. Cancer Res. 20(23), 6083–6095 (2014).
[Crossref] [PubMed]

Dawes, R. P.

K. A. Burke, R. P. Dawes, M. K. Cheema, A. Van Hove, D. S. Benoit, S. W. Perry, and E. Brown, “Second-harmonic generation scattering directionality predicts tumor cell motility in collagen gels,” J. Biomed. Opt. 20(5), 051024 (2015).
[Crossref] [PubMed]

Delecroix, V.

C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
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Denburg, N. L.

L. L. B. Ponto, Y. Menda, V. A. Magnotta, T. H. Yamada, N. L. Denburg, and S. K. Schultz, “Frontal hypometabolism in elderly breast cancer survivors determined by [(18)F]fluorodeoxyglucose (FDG) positron emission tomography (PET): a pilot study,” Int. J. Geriatr. Psychiatry 30(6), 587–594 (2015).
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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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[Crossref] [PubMed]

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C. Rousseau, A. Devillers, C. Sagan, L. Ferrer, B. Bridji, L. Campion, M. Ricaud, E. Bourbouloux, I. Doutriaux, M. Clouet, D. Berton-Rigaud, C. Bouriel, V. Delecroix, E. Garin, S. Rouquette, I. Resche, P. Kerbrat, J. F. Chatal, and M. Campone, “Monitoring of early response to neoadjuvant chemotherapy in stage II and III breast cancer by [18F]fluorodeoxyglucose positron emission tomography,” J. Clin. Oncol. 24(34), 5366–5372 (2006).
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K. Cai, H. N. Xu, A. Singh, L. Moon, M. Haris, R. Reddy, and L. Z. Li, “Breast cancer redox heterogeneity detectable with chemical exchange saturation transfer (CEST) MRI,” Mol. Imaging Biol. 16(5), 670–679 (2014).
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Saunders, C. M.

Scappaticci, F. A.

C. Jackisch, F. A. Scappaticci, D. Heinzmann, F. Bisordi, T. Schreitmüller, G. Minckwitz, and J. Cortés, “Neoadjuvant breast cancer treatment as a sensitive setting for trastuzumab biosimilar development and extrapolation,” Future Oncol. 11(1), 61–71 (2015).
[Crossref] [PubMed]

Schoener, B.

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

Schreitmüller, T.

C. Jackisch, F. A. Scappaticci, D. Heinzmann, F. Bisordi, T. Schreitmüller, G. Minckwitz, and J. Cortés, “Neoadjuvant breast cancer treatment as a sensitive setting for trastuzumab biosimilar development and extrapolation,” Future Oncol. 11(1), 61–71 (2015).
[Crossref] [PubMed]

Schultz, S. K.

L. L. B. Ponto, Y. Menda, V. A. Magnotta, T. H. Yamada, N. L. Denburg, and S. K. Schultz, “Frontal hypometabolism in elderly breast cancer survivors determined by [(18)F]fluorodeoxyglucose (FDG) positron emission tomography (PET): a pilot study,” Int. J. Geriatr. Psychiatry 30(6), 587–594 (2015).
[Crossref] [PubMed]

Scolaro, L.

L. Scolaro, R. A. McLaughlin, B. F. Kennedy, C. M. Saunders, and D. D. Sampson, “A review of optical coherence tomography in breast cancer,” Photonics Lasers Med. 3(3), 225–240 (2014).
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Shah, A. T.

Siegel, R. L.

R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer statistics, 2016,” CA Cancer J. Clin. 66(1), 7–30 (2016).
[Crossref] [PubMed]

Singh, A.

K. Cai, H. N. Xu, A. Singh, L. Moon, M. Haris, R. Reddy, and L. Z. Li, “Breast cancer redox heterogeneity detectable with chemical exchange saturation transfer (CEST) MRI,” Mol. Imaging Biol. 16(5), 670–679 (2014).
[Crossref] [PubMed]

Singletary, K. W.

S. A. Boppart, W. Luo, D. L. Marks, and K. W. Singletary, “Optical coherence tomography: feasibility for basic research and image-guided surgery of breast cancer,” Breast Cancer Res. Treat. 84(2), 85–97 (2004).
[Crossref] [PubMed]

Singletary, S. E.

W. F. Symmans, F. Peintinger, C. Hatzis, R. Rajan, H. Kuerer, V. Valero, L. Assad, A. Poniecka, B. Hennessy, M. Green, A. U. Buzdar, S. E. Singletary, G. N. Hortobagyi, and L. Pusztai, “Measurement of residual breast cancer burden to predict survival after neoadjuvant chemotherapy,” J. Clin. Oncol. 25(28), 4414–4422 (2007).
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Skala, M. C.

T. M. Cannon, A. T. Shah, and M. C. Skala, “Autofluorescence imaging captures heterogeneous drug response differences between 2D and 3D breast cancer cultures,” Biomed. Opt. Express 8(3), 1911–1925 (2017).
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A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative optical imaging of primary tumor organoid metabolism predicts drug response in breast cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Song, G.

G. Song, D. B. Darr, C. M. Santos, M. Ross, A. Valdivia, J. L. Jordan, B. R. Midkiff, S. Cohen, N. Nikolaishvili-Feinberg, C. R. Miller, T. K. Tarrant, A. B. Rogers, A. C. Dudley, C. M. Perou, and W. C. Zamboni, “Effects of tumor microenvironment heterogeneity on nanoparticle disposition and efficacy in breast cancer tumor models,” Clin. Cancer Res. 20(23), 6083–6095 (2014).
[Crossref] [PubMed]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Suen, C. Y.

L. Lam, S.-W. Lee, and C. Y. Suen, “Thinning methodologies-a comprehensive survey,” IEEE Trans. Pattern Anal. Mach. Intell. 14(9), 869–885 (1992).
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Sung, J. S.

J. S. Sung and D. D. Dershaw, “Breast magnetic resonance imaging for screening high-risk women,” Magn. Reson. Imaging Clin. N. Am. 21(3), 509–517 (2013).
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Symmans, W. F.

C. Liedtke, C. Mazouni, K. R. Hess, F. André, A. Tordai, J. A. Mejia, W. F. Symmans, A. M. Gonzalez-Angulo, B. Hennessy, M. Green, M. Cristofanilli, G. N. Hortobagyi, and L. Pusztai, “Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer,” J. Clin. Oncol. 26(8), 1275–1281 (2008).
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W. F. Symmans, F. Peintinger, C. Hatzis, R. Rajan, H. Kuerer, V. Valero, L. Assad, A. Poniecka, B. Hennessy, M. Green, A. U. Buzdar, S. E. Singletary, G. N. Hortobagyi, and L. Pusztai, “Measurement of residual breast cancer burden to predict survival after neoadjuvant chemotherapy,” J. Clin. Oncol. 25(28), 4414–4422 (2007).
[Crossref] [PubMed]

Szot, C. S.

C. F. Buchanan, E. E. Voigt, C. S. Szot, J. W. Freeman, P. P. Vlachos, and M. N. Rylander, “Three-dimensional microfluidic collagen hydrogels for investigating flow-mediated tumor-endothelial signaling and vascular organization,” Tissue Eng. Part C Methods 20(1), 64–75 (2014).
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Szulczewski, J. M.

J. S. Bredfeldt, Y. Liu, C. A. Pehlke, M. W. Conklin, J. M. Szulczewski, D. R. Inman, P. J. Keely, R. D. Nowak, T. R. Mackie, and K. W. Eliceiri, “Computational segmentation of collagen fibers from second-harmonic generation images of breast cancer,” J. Biomed. Opt. 19(1), 016007 (2014).
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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 (2012).
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Tarrant, T. K.

G. Song, D. B. Darr, C. M. Santos, M. Ross, A. Valdivia, J. L. Jordan, B. R. Midkiff, S. Cohen, N. Nikolaishvili-Feinberg, C. R. Miller, T. K. Tarrant, A. B. Rogers, A. C. Dudley, C. M. Perou, and W. C. Zamboni, “Effects of tumor microenvironment heterogeneity on nanoparticle disposition and efficacy in breast cancer tumor models,” Clin. Cancer Res. 20(23), 6083–6095 (2014).
[Crossref] [PubMed]

Thompson, E. W.

C. W. Huo, G. Chew, P. Hill, D. Huang, W. Ingman, L. Hodson, K. A. Brown, A. Magenau, A. H. Allam, E. McGhee, P. Timpson, M. A. Henderson, E. W. Thompson, and K. Britt, “High mammographic density is associated with an increase in stromal collagen and immune cells within the mammary epithelium,” Breast Cancer Res. 17(1), 79 (2015).
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K. Tilbury and P. J. Campagnola, “Applications of second-harmonic generation imaging microscopy in ovarian and breast cancer,” Perspect. Medicin. Chem. 7(1), 21–32 (2015).
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C. W. Huo, G. Chew, P. Hill, D. Huang, W. Ingman, L. Hodson, K. A. Brown, A. Magenau, A. H. Allam, E. McGhee, P. Timpson, M. A. Henderson, E. W. Thompson, and K. Britt, “High mammographic density is associated with an increase in stromal collagen and immune cells within the mammary epithelium,” Breast Cancer Res. 17(1), 79 (2015).
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Tordai, A.

C. Liedtke, C. Mazouni, K. R. Hess, F. André, A. Tordai, J. A. Mejia, W. F. Symmans, A. M. Gonzalez-Angulo, B. Hennessy, M. Green, M. Cristofanilli, G. N. Hortobagyi, and L. Pusztai, “Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer,” J. Clin. Oncol. 26(8), 1275–1281 (2008).
[Crossref] [PubMed]

Toussaint, K. C.

Trattnig, S.

G. J. Wengert, T. H. Helbich, W.-D. Vogl, P. Baltzer, G. Langs, M. Weber, W. Bogner, S. Gruber, S. Trattnig, and K. Pinker, “Introduction of an Automated User-Independent Quantitative Volumetric Magnetic Resonance Imaging Breast Density Measurement System Using the Dixon Sequence: Comparison With Mammographic Breast Density Assessment,” Invest. Radiol. 50(2), 73–80 (2015).
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Tsai, J.-W.

S. Chakraborty, F.-S. Nian, J.-W. Tsai, A. Karmenyan, and A. Chiou, “Quantification of the metabolic state in cell-model of Parkinson’s disease by fluorescence lifetime imaging microscopy,” Sci. Rep. 6(1), 19145 (2016).
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Uppal, A.

A. Uppal and P. K. Gupta, “Measurement of NADH concentration in normal and malignant human tissues from breast and oral cavity,” Biotechnol. Appl. Biochem. 37(1), 45–50 (2003).
[Crossref] [PubMed]

Valdivia, A.

G. Song, D. B. Darr, C. M. Santos, M. Ross, A. Valdivia, J. L. Jordan, B. R. Midkiff, S. Cohen, N. Nikolaishvili-Feinberg, C. R. Miller, T. K. Tarrant, A. B. Rogers, A. C. Dudley, C. M. Perou, and W. C. Zamboni, “Effects of tumor microenvironment heterogeneity on nanoparticle disposition and efficacy in breast cancer tumor models,” Clin. Cancer Res. 20(23), 6083–6095 (2014).
[Crossref] [PubMed]

Valero, V.

W. F. Symmans, F. Peintinger, C. Hatzis, R. Rajan, H. Kuerer, V. Valero, L. Assad, A. Poniecka, B. Hennessy, M. Green, A. U. Buzdar, S. E. Singletary, G. N. Hortobagyi, and L. Pusztai, “Measurement of residual breast cancer burden to predict survival after neoadjuvant chemotherapy,” J. Clin. Oncol. 25(28), 4414–4422 (2007).
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Van Hove, A.

K. A. Burke, R. P. Dawes, M. K. Cheema, A. Van Hove, D. S. Benoit, S. W. Perry, and E. Brown, “Second-harmonic generation scattering directionality predicts tumor cell motility in collagen gels,” J. Biomed. Opt. 20(5), 051024 (2015).
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Vlachos, P. P.

C. F. Buchanan, E. E. Voigt, C. S. Szot, J. W. Freeman, P. P. Vlachos, and M. N. Rylander, “Three-dimensional microfluidic collagen hydrogels for investigating flow-mediated tumor-endothelial signaling and vascular organization,” Tissue Eng. Part C Methods 20(1), 64–75 (2014).
[Crossref] [PubMed]

Vogl, W.-D.

G. J. Wengert, T. H. Helbich, W.-D. Vogl, P. Baltzer, G. Langs, M. Weber, W. Bogner, S. Gruber, S. Trattnig, and K. Pinker, “Introduction of an Automated User-Independent Quantitative Volumetric Magnetic Resonance Imaging Breast Density Measurement System Using the Dixon Sequence: Comparison With Mammographic Breast Density Assessment,” Invest. Radiol. 50(2), 73–80 (2015).
[Crossref] [PubMed]

Voigt, E. E.

C. F. Buchanan, E. E. Voigt, C. S. Szot, J. W. Freeman, P. P. Vlachos, and M. N. Rylander, “Three-dimensional microfluidic collagen hydrogels for investigating flow-mediated tumor-endothelial signaling and vascular organization,” Tissue Eng. Part C Methods 20(1), 64–75 (2014).
[Crossref] [PubMed]

Walsh, A. J.

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative optical imaging of primary tumor organoid metabolism predicts drug response in breast cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Walsh, M.

Wang, X.

Y. Zhu, X. Wang, J. Chen, J. Zhang, F. Meng, C. Deng, R. Cheng, J. Feijen, and Z. Zhong, “Bioresponsive and fluorescent hyaluronic acid-iodixanol nanogels for targeted X-ray computed tomography imaging and chemotherapy of breast tumors,” J. Control. Release 244(Pt B), 229–239 (2016).
[Crossref] [PubMed]

Webb, W. W.

S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J. 82(5), 2811–2825 (2002).
[Crossref] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Weber, M.

G. J. Wengert, T. H. Helbich, W.-D. Vogl, P. Baltzer, G. Langs, M. Weber, W. Bogner, S. Gruber, S. Trattnig, and K. Pinker, “Introduction of an Automated User-Independent Quantitative Volumetric Magnetic Resonance Imaging Breast Density Measurement System Using the Dixon Sequence: Comparison With Mammographic Breast Density Assessment,” Invest. Radiol. 50(2), 73–80 (2015).
[Crossref] [PubMed]

Wengert, G. J.

G. J. Wengert, T. H. Helbich, W.-D. Vogl, P. Baltzer, G. Langs, M. Weber, W. Bogner, S. Gruber, S. Trattnig, and K. Pinker, “Introduction of an Automated User-Independent Quantitative Volumetric Magnetic Resonance Imaging Breast Density Measurement System Using the Dixon Sequence: Comparison With Mammographic Breast Density Assessment,” Invest. Radiol. 50(2), 73–80 (2015).
[Crossref] [PubMed]

White, J. G.

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38–54 (2006).
[Crossref] [PubMed]

Wijesinghe, P.

Wu, S.

S. Wu, H. Li, H. Yang, X. Zhang, Z. Li, and S. Xu, “Quantitative analysis on collagen morphology in aging skin based on multiphoton microscopy,” J. Biomed. Opt. 16(4), 040502 (2011).
[Crossref] [PubMed]

Xie, S.

J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit oesophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys. 9(7), 212 (2007).
[Crossref]

Xu, H. N.

K. Cai, H. N. Xu, A. Singh, L. Moon, M. Haris, R. Reddy, and L. Z. Li, “Breast cancer redox heterogeneity detectable with chemical exchange saturation transfer (CEST) MRI,” Mol. Imaging Biol. 16(5), 670–679 (2014).
[Crossref] [PubMed]

Xu, S.

S. Wu, H. Li, H. Yang, X. Zhang, Z. Li, and S. Xu, “Quantitative analysis on collagen morphology in aging skin based on multiphoton microscopy,” J. Biomed. Opt. 16(4), 040502 (2011).
[Crossref] [PubMed]

Yamada, T. H.

L. L. B. Ponto, Y. Menda, V. A. Magnotta, T. H. Yamada, N. L. Denburg, and S. K. Schultz, “Frontal hypometabolism in elderly breast cancer survivors determined by [(18)F]fluorodeoxyglucose (FDG) positron emission tomography (PET): a pilot study,” Int. J. Geriatr. Psychiatry 30(6), 587–594 (2015).
[Crossref] [PubMed]

Yang, H.

S. Wu, H. Li, H. Yang, X. Zhang, Z. Li, and S. Xu, “Quantitative analysis on collagen morphology in aging skin based on multiphoton microscopy,” J. Biomed. Opt. 16(4), 040502 (2011).
[Crossref] [PubMed]

Zamboni, W. C.

G. Song, D. B. Darr, C. M. Santos, M. Ross, A. Valdivia, J. L. Jordan, B. R. Midkiff, S. Cohen, N. Nikolaishvili-Feinberg, C. R. Miller, T. K. Tarrant, A. B. Rogers, A. C. Dudley, C. M. Perou, and W. C. Zamboni, “Effects of tumor microenvironment heterogeneity on nanoparticle disposition and efficacy in breast cancer tumor models,” Clin. Cancer Res. 20(23), 6083–6095 (2014).
[Crossref] [PubMed]

Zhang, J.

Y. Zhu, X. Wang, J. Chen, J. Zhang, F. Meng, C. Deng, R. Cheng, J. Feijen, and Z. Zhong, “Bioresponsive and fluorescent hyaluronic acid-iodixanol nanogels for targeted X-ray computed tomography imaging and chemotherapy of breast tumors,” J. Control. Release 244(Pt B), 229–239 (2016).
[Crossref] [PubMed]

Zhang, X.

S. Wu, H. Li, H. Yang, X. Zhang, Z. Li, and S. Xu, “Quantitative analysis on collagen morphology in aging skin based on multiphoton microscopy,” J. Biomed. Opt. 16(4), 040502 (2011).
[Crossref] [PubMed]

Zhong, Z.

Y. Zhu, X. Wang, J. Chen, J. Zhang, F. Meng, C. Deng, R. Cheng, J. Feijen, and Z. Zhong, “Bioresponsive and fluorescent hyaluronic acid-iodixanol nanogels for targeted X-ray computed tomography imaging and chemotherapy of breast tumors,” J. Control. Release 244(Pt B), 229–239 (2016).
[Crossref] [PubMed]

Zhu, Y.

Y. Zhu, X. Wang, J. Chen, J. Zhang, F. Meng, C. Deng, R. Cheng, J. Feijen, and Z. Zhong, “Bioresponsive and fluorescent hyaluronic acid-iodixanol nanogels for targeted X-ray computed tomography imaging and chemotherapy of breast tumors,” J. Control. Release 244(Pt B), 229–239 (2016).
[Crossref] [PubMed]

Zhuo, S.

J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit oesophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys. 9(7), 212 (2007).
[Crossref]

Zou, Q.

J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit oesophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys. 9(7), 212 (2007).
[Crossref]

Am. J. Pathol. (2)

T. Mammoto, A. Jiang, E. Jiang, D. Panigrahy, M. W. Kieran, and A. Mammoto, “Role of collagen matrix in tumor angiogenesis and glioblastoma multiforme progression,” Am. J. Pathol. 183(4), 1293–1305 (2013).
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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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Ann. Biomed. Eng. (1)

S. W. Perry, R. M. Burke, and E. B. Brown, “Two-photon and second harmonic microscopy in clinical and translational cancer research,” Ann. Biomed. Eng. 40(2), 277–291 (2012).
[Crossref] [PubMed]

Biomed. Opt. Express (3)

Biophys. J. (1)

S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J. 82(5), 2811–2825 (2002).
[Crossref] [PubMed]

Biotechnol. Appl. Biochem. (1)

A. Uppal and P. K. Gupta, “Measurement of NADH concentration in normal and malignant human tissues from breast and oral cavity,” Biotechnol. Appl. Biochem. 37(1), 45–50 (2003).
[Crossref] [PubMed]

BMC Med. (1)

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38–54 (2006).
[Crossref] [PubMed]

Breast Cancer Res. (1)

C. W. Huo, G. Chew, P. Hill, D. Huang, W. Ingman, L. Hodson, K. A. Brown, A. Magenau, A. H. Allam, E. McGhee, P. Timpson, M. A. Henderson, E. W. Thompson, and K. Britt, “High mammographic density is associated with an increase in stromal collagen and immune cells within the mammary epithelium,” Breast Cancer Res. 17(1), 79 (2015).
[Crossref] [PubMed]

Breast Cancer Res. Treat. (1)

S. A. Boppart, W. Luo, D. L. Marks, and K. W. Singletary, “Optical coherence tomography: feasibility for basic research and image-guided surgery of breast cancer,” Breast Cancer Res. Treat. 84(2), 85–97 (2004).
[Crossref] [PubMed]

CA Cancer J. Clin. (1)

R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer statistics, 2016,” CA Cancer J. Clin. 66(1), 7–30 (2016).
[Crossref] [PubMed]

Cancer Epidemiol. Biomarkers Prev. (1)

C. E. DeSantis, F. Bray, J. Ferlay, J. Lortet-Tieulent, B. O. Anderson, and A. Jemal, “International variation in female breast cancer incidence and mortality rates,” Cancer Epidemiol. Biomarkers Prev. 24(10), 1495–1506 (2015).
[Crossref] [PubMed]

Cancer Res. (2)

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative optical imaging of primary tumor organoid metabolism predicts drug response in breast cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Clin. Cancer Res. (1)

G. Song, D. B. Darr, C. M. Santos, M. Ross, A. Valdivia, J. L. Jordan, B. R. Midkiff, S. Cohen, N. Nikolaishvili-Feinberg, C. R. Miller, T. K. Tarrant, A. B. Rogers, A. C. Dudley, C. M. Perou, and W. C. Zamboni, “Effects of tumor microenvironment heterogeneity on nanoparticle disposition and efficacy in breast cancer tumor models,” Clin. Cancer Res. 20(23), 6083–6095 (2014).
[Crossref] [PubMed]

Clin. Exp. Metastasis (1)

P. P. Provenzano, K. W. Eliceiri, and P. J. Keely, “Multiphoton microscopy and fluorescence lifetime imaging microscopy (FLIM) to monitor metastasis and the tumor microenvironment,” Clin. Exp. Metastasis 26(4), 357–370 (2009).
[Crossref] [PubMed]

Eur. J. Radiol. (1)

S. Aminololama-Shakeri, C. K. Abbey, P. Gazi, N. D. Prionas, A. Nosratieh, C.-S. Li, J. M. Boone, and K. K. Lindfors, “Differentiation of ductal carcinoma in-situ from benign micro-calcifications by dedicated breast computed tomography,” Eur. J. Radiol. 85(1), 297–303 (2016).
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Future Oncol. (1)

C. Jackisch, F. A. Scappaticci, D. Heinzmann, F. Bisordi, T. Schreitmüller, G. Minckwitz, and J. Cortés, “Neoadjuvant breast cancer treatment as a sensitive setting for trastuzumab biosimilar development and extrapolation,” Future Oncol. 11(1), 61–71 (2015).
[Crossref] [PubMed]

IEEE Trans. Pattern Anal. Mach. Intell. (1)

L. Lam, S.-W. Lee, and C. Y. Suen, “Thinning methodologies-a comprehensive survey,” IEEE Trans. Pattern Anal. Mach. Intell. 14(9), 869–885 (1992).
[Crossref]

IEEE Trans. Syst. Man Cybern. (1)

N. Otsu, “Threshold Selection Method from Gray-Level Histograms,” IEEE Trans. Syst. Man Cybern. 9(1), 62–66 (1979).
[Crossref]

Int. J. Geriatr. Psychiatry (1)

L. L. B. Ponto, Y. Menda, V. A. Magnotta, T. H. Yamada, N. L. Denburg, and S. K. Schultz, “Frontal hypometabolism in elderly breast cancer survivors determined by [(18)F]fluorodeoxyglucose (FDG) positron emission tomography (PET): a pilot study,” Int. J. Geriatr. Psychiatry 30(6), 587–594 (2015).
[Crossref] [PubMed]

Invest. Radiol. (1)

G. J. Wengert, T. H. Helbich, W.-D. Vogl, P. Baltzer, G. Langs, M. Weber, W. Bogner, S. Gruber, S. Trattnig, and K. Pinker, “Introduction of an Automated User-Independent Quantitative Volumetric Magnetic Resonance Imaging Breast Density Measurement System Using the Dixon Sequence: Comparison With Mammographic Breast Density Assessment,” Invest. Radiol. 50(2), 73–80 (2015).
[Crossref] [PubMed]

J. Biol. Chem. (1)

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

J. Biomed. Opt. (4)

K. Burke, P. Tang, and E. Brown, “Second harmonic generation reveals matrix alterations during breast tumor progression,” J. Biomed. Opt. 18(3), 031106 (2012).
[Crossref] [PubMed]

S. Wu, H. Li, H. Yang, X. Zhang, Z. Li, and S. Xu, “Quantitative analysis on collagen morphology in aging skin based on multiphoton microscopy,” J. Biomed. Opt. 16(4), 040502 (2011).
[Crossref] [PubMed]

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Figures (4)

Fig. 1
Fig. 1 TPM images and histological images of the structures of breast tissues in four samples status. The first column (A1, B1, C1, and D1) was obtained by AF, which reflects endogenous fluorophore. The second column (A2, B2, C2, and D2) was obtained by the second harmonic generated, which reflects the collagen. The third column (A3, B3, C3, and D3) combines AF and SHG. The fourth column (A4, B4, C4, and D4) is the corresponding H&E stained images. (A1) -(A4) Normal breast, (B1) -(B4) Ductal carcinoma in situ, (C1) -(C4) Invasive ductal carcinoma, and (D1) -(D4) Invasive ductal carcinoma post-chemotherapy. The scale bar is 100 µm.

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Fig. 2
Fig. 2 Spectral information and the redox ratio in the breast tissues. (A) Lambda mode imaging of a breast tissue with 32 channels. The SHG channel is at 404 nm; the NADH channel is at 479 nm; the FAD channel is in the 543-nm channel. (B) The combined imaging of lambda mode. (C) The normalized intensity vs. the emission wavelength with collagen, NADH, and FAD highlighted respectively. (D) NADH and FAD intensities, as well as (E) the optical redox in three breast tissues status. The samples for statistics include seven normal intraductal breast, six ductal carcinoma in situ and four ductal carcinoma post-chemotherapy. The scale bar is 100 µm.

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Fig. 3
Fig. 3 The collagen intensity in different tissues status. (A)–(C) Images of collagen: (A) Normal stroma, (B) Invasive ductal carcinoma, (C) Post-chemotherapy. (D)-(F) AF images: (D) Normal stroma, (E) Invasive ductal carcinoma, (F) Post- chemotherapy. (G) The ratio of SHG/AF and the collagen density of the three status of breast tissues. The samples include seven normal stroma breast, six invasive ductal carcinoma and four post-chemotherapy. The scale bar is 100 µm.

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Fig. 4
Fig. 4 Collagen orientation information for the four breast tissues status extracted from the collagen center line. (A) A breast tissue SHG image. (B) The binary image of (A). (C) The filtered image. (D) The center line image. (E) The center line image of normal breast tissue. (F) The center line image of ductal carcinoma in situ. (G) The center line image of invasive ductal carcinoma. (H) The center line image of invasive ductal carcinoma post-chemotherapy. (I) The normal breast image rotated by 45 degrees. (J) The mean and SD values of fiber orientation with different rotation angles. (K) The standard deviation of fiber orientation in breast tissues with different status. The statistical samples include seven normal stroma breast tissues, six ductal carcinoma in situ samples, six invasive ductal carcinoma samples and four post-chemotherapy samples. The scale bar is 100 µm.

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Equations (4)

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k ( i , j ) = ( y 2 − y 1 ) / ( x 2 − x 1 ) , i f x 2 − x 1 ≠ 0
θ ( i , j ) = { a r c tan k ( i , j ) , i f k ≥ 0 π + a r c tan k ( i , j ) , i f k < 0 π / 2 , i f x 2 − x 1 = 0
R ( b ) = min [ d i s t . ∀ b ∈ B ( s , b ) ]
N o = π R a 2 / 2

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