Abstract

A number of histopathology studies have utilized the label free microscopy method of Second Harmonic Generation (SHG) to investigate collagen organization in disease onset and progression. Here we explored an alternative label free imaging approach, LC-PolScope that is based on liquid crystal based polarized light imaging. We demonstrated that this more accessible technology has the ability to visualize all fibers of interest and has a good to excellent correlation between SHG and LC-PolScope measurements in fibrillar collagen orientation and alignment. This study supports that LC-PolScope is a viable alternative to SHG for label free collagen organization measurements in thin histology sections.

© 2017 Optical Society of America

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    [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref]
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2016 (3)

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Comparison of Picrosirius Red Staining With Second Harmonic Generation Imaging for the Quantification of Clinically Relevant Collagen Fiber Features in Histopathology Samples,” J. Histochem. Cytochem. 64(9), 519–529 (2016).
[Crossref] [PubMed]

C. J. Hanley, F. Noble, M. Ward, M. Bullock, C. Drifka, M. Mellone, A. Manousopoulou, H. E. Johnston, A. Hayden, S. Thirdborough, Y. Liu, D. M. Smith, T. Mellows, W. J. Kao, S. D. Garbis, A. Mirnezami, T. J. Underwood, K. W. Eliceiri, and G. J. Thomas, “A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers,” Oncotarget 7(5), 6159–6174 (2016).
[Crossref] [PubMed]

N. L. Rosin, N. Agabalyan, K. Olsen, G. Martufi, V. Gabriel, J. Biernaskie, and E. S. Di Martino, “Collagen structural alterations contribute to stiffening of tissue after split-thickness skin grafting,” Wound Repair Regen. 24(2), 263–274 (2016).
[Crossref] [PubMed]

2015 (3)

P. Arun Gopinathan, G. Kokila, M. Jyothi, C. Ananjan, L. Pradeep, and S. Humaira Nazir, “Study of Collagen Birefringence in Different Grades of Oral Squamous Cell Carcinoma Using Picrosirius Red and Polarized Light Microscopy,” Scientifica (Cairo) 2015, 802980 (2015).
[Crossref] [PubMed]

B. K. Brisson, E. A. Mauldin, W. Lei, L. K. Vogel, A. M. Power, A. Lo, D. Dopkin, C. Khanna, R. G. Wells, E. Puré, and S. W. Volk, “Type III Collagen Directs Stromal Organization and Limits Metastasis in a Murine Model of Breast Cancer,” Am. J. Pathol. 185(5), 1471–1486 (2015).
[Crossref] [PubMed]

C. R. Drifka, J. Tod, A. G. Loeffler, Y. Liu, G. J. Thomas, K. W. Eliceiri, and W. J. Kao, “Periductal stromal collagen topology of pancreatic ductal adenocarcinoma differs from that of normal and chronic pancreatitis,” Mod. Pathol. 28(11), 1470–1480 (2015).
[Crossref] [PubMed]

2014 (3)

A. Keikhosravi, J. S. Bredfeldt, A. K. Sagar, and K. W. Eliceiri, “Second-harmonic generation imaging of cancer,” Methods Cell Biol. 123, 531–546 (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]

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 (1)

B. D. Quan and E. D. Sone, “Cryo-TEM analysis of collagen fibrillar structure,” Methods Enzymol. 532, 189–205 (2013).
[Crossref] [PubMed]

2012 (5)

M. Plodinec, M. Loparic, C. A. Monnier, E. C. Obermann, R. Zanetti-Dallenbach, P. Oertle, J. T. Hyotyla, U. Aebi, M. Bentires-Alj, R. Y. H. Lim, and C.-A. Schoenenberger, “The nanomechanical signature of breast cancer,” Nat. Nanotechnol. 7(11), 757–765 (2012).
[Crossref] [PubMed]

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

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an Open-Source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

P. P. Provenzano, C. Cuevas, A. E. Chang, V. K. Goel, D. D. Von Hoff, and S. R. Hingorani, “Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma,” Cancer Cell 21(3), 418–429 (2012).
[Crossref] [PubMed]

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

2011 (2)

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]

Z. Nong, C. O’Neil, M. Lei, R. Gros, A. Watson, A. Rizkalla, K. Mequanint, S. Li, M. J. Frontini, Q. Feng, and J. G. Pickering, “Type I Collagen Cleavage Is Essential for Effective Fibrotic Repair after Myocardial Infarction,” Am. J. Pathol. 179(5), 2189–2198 (2011).
[Crossref] [PubMed]

2010 (2)

S. Saalfeld, A. Cardona, V. Hartenstein, and P. Tomančák, “As-rigid-as-possible mosaicking and serial section registration of large ssTEM datasets,” Bioinformatics 26(12), i57–i63 (2010).
[Crossref] [PubMed]

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

2009 (1)

P. Berens, “CircStat: A MATLAB Toolbox for Circular Statistics,” J. Stat. Softw. 31(10), 21 (2009).
[Crossref]

2008 (1)

W. Sun, S. Chang, D. C. S. Tai, N. Tan, G. Xiao, H. Tang, and H. Yu, “Nonlinear optical microscopy: use of second harmonic generation and two-photon microscopy for automated quantitative liver fibrosis studies,” J. Biomed. Opt. 13(6), 064010 (2008).
[Crossref] [PubMed]

2007 (2)

T. T. Le, I. M. Langohr, M. J. Locker, M. Sturek, and J.-X. Cheng, “Label-free molecular imaging of atherosclerotic lesions using multimodal nonlinear optical microscopy,” J. Biomed. Opt. 12(5), 054007 (2007).
[Crossref] [PubMed]

M. B. Lilledahl, O. A. Haugen, C. de Lange Davies, and L. O. Svaasand, “Characterization of vulnerable plaques by multiphoton microscopy,” J. Biomed. Opt. 12(4), 044005 (2007).
[Crossref] [PubMed]

2006 (2)

I. Allon, M. Vered, A. Buchner, and D. Dayan, “Stromal differences in salivary gland tumors of a common histopathogenesis but with different biological behavior: a study with picrosirius red and polarizing microscopy,” Acta Histochem. 108(4), 259–264 (2006).
[Crossref] [PubMed]

M. Kobayashi, Y. Furuya, T. Okabayashi, and K. Araki, “Scanning electron microscopic study of the three-dimensional structure of the collagen sheath surrounding cancer cells after single high-dose irradiation,” Med. Mol. Morphol. 39(2), 106–112 (2006).
[Crossref] [PubMed]

2005 (1)

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting Second-Harmonic Generation Images of Collagen I Fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[Crossref] [PubMed]

2003 (3)

A. Hamlett, L. Ryan, P. Serrano-Trespalacios, and R. Wolfinger, “Mixed Models for Assessing Correlation in the Presence of Replication,” J. Air Waste Manag. Assoc. 53(4), 442–450 (2003).
[Crossref] [PubMed]

G. Ayala, J. A. Tuxhorn, T. M. Wheeler, A. Frolov, P. T. Scardino, M. Ohori, M. Wheeler, J. Spitler, and D. R. Rowley, “Reactive stroma as a predictor of biochemical-free recurrence in prostate cancer,” Clin. Cancer Res. 9(13), 4792–4801 (2003).
[PubMed]

M. Shribak and R. Oldenbourg, “Techniques for fast and sensitive measurements of two-dimensional birefringence distributions,” Appl. Opt. 42(16), 3009–3017 (2003).
[Crossref] [PubMed]

2002 (1)

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
[Crossref] [PubMed]

2000 (1)

B.-M. Kim, J. Eichler, K. M. Reiser, A. M. Rubenchik, and L. B. Da Silva, “Collagen structure and nonlinear susceptibility: Effects of heat, glycation, and enzymatic cleavage on second harmonic signal intensity,” Lasers Surg. Med. 27(4), 329–335 (2000).
[Crossref] [PubMed]

1996 (1)

R. Oldenbourg, “A new view on polarization microscopy,” Nature 381(6585), 811–812 (1996).
[Crossref] [PubMed]

1995 (1)

R. Oldenbourg and G. Mei, “New polarized light microscope with precision universal compensator,” J. Microsc. 180(2), 140–147 (1995).
[Crossref] [PubMed]

1994 (3)

D. V. Cicchetti, “Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology,” Psychol. Assess. 6(4), 284–290 (1994).
[Crossref]

P. Odetti, M. A. Pronzato, G. Noberasco, L. Cosso, N. Traverso, D. Cottalasso, and U. M. Marinari, “Relationships between glycation and oxidation related fluorescences in rat collagen during aging. An in vivo and in vitro study,” Lab. Invest. 70(1), 61–67 (1994).
[PubMed]

C. J. Cicchetti and J. A. Dubin, “A Microeconometric Analysis of Risk Aversion and the Decision to Self-Insure,” J. Polit. Econ. 102(1), 169–186 (1994).
[Crossref]

1988 (1)

S. Tanaka, G. Avigad, B. Brodsky, and E. F. Eikenberry, “Glycation induces expansion of the molecular packing of collagen,” J. Mol. Biol. 203(2), 495–505 (1988).
[Crossref] [PubMed]

1983 (1)

D. G. Altman and J. M. Bland, “Measurement in Medicine: The Analysis of Method Comparison Studies,” J. R. Stat. Soc. Ser. Stat. 32, 307–317 (1983).

1982 (1)

B. C. Vidal, M. L. Mello, and E. R. Pimentel, “Polarization microscopy and microspectrophotometry of Sirius Red, Picrosirius and Chlorantine Fast Red aggregates and of their complexes with collagen,” Histochem. J. 14(6), 857–878 (1982).
[Crossref] [PubMed]

1979 (1)

L. C. Junqueira, G. Bignolas, and R. R. Brentani, “Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections,” Histochem. J. 11(4), 447–455 (1979).
[Crossref] [PubMed]

1963 (1)

R. D. Allen, J. Brault, and R. D. Moore, “A new method of polarization microscopic analysis I. Scanning with a Birefringence Detection System,” J. Cell Biol. 18(2), 223–235 (1963).
[Crossref] [PubMed]

Aebi, U.

M. Plodinec, M. Loparic, C. A. Monnier, E. C. Obermann, R. Zanetti-Dallenbach, P. Oertle, J. T. Hyotyla, U. Aebi, M. Bentires-Alj, R. Y. H. Lim, and C.-A. Schoenenberger, “The nanomechanical signature of breast cancer,” Nat. Nanotechnol. 7(11), 757–765 (2012).
[Crossref] [PubMed]

Agabalyan, N.

N. L. Rosin, N. Agabalyan, K. Olsen, G. Martufi, V. Gabriel, J. Biernaskie, and E. S. Di Martino, “Collagen structural alterations contribute to stiffening of tissue after split-thickness skin grafting,” Wound Repair Regen. 24(2), 263–274 (2016).
[Crossref] [PubMed]

Allen, R. D.

R. D. Allen, J. Brault, and R. D. Moore, “A new method of polarization microscopic analysis I. Scanning with a Birefringence Detection System,” J. Cell Biol. 18(2), 223–235 (1963).
[Crossref] [PubMed]

Allon, I.

I. Allon, M. Vered, A. Buchner, and D. Dayan, “Stromal differences in salivary gland tumors of a common histopathogenesis but with different biological behavior: a study with picrosirius red and polarizing microscopy,” Acta Histochem. 108(4), 259–264 (2006).
[Crossref] [PubMed]

Altman, D. G.

D. G. Altman and J. M. Bland, “Measurement in Medicine: The Analysis of Method Comparison Studies,” J. R. Stat. Soc. Ser. Stat. 32, 307–317 (1983).

Ananjan, C.

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L. C. Junqueira, G. Bignolas, and R. R. Brentani, “Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections,” Histochem. J. 11(4), 447–455 (1979).
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S. Tanaka, G. Avigad, B. Brodsky, and E. F. Eikenberry, “Glycation induces expansion of the molecular packing of collagen,” J. Mol. Biol. 203(2), 495–505 (1988).
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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).
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I. Allon, M. Vered, A. Buchner, and D. Dayan, “Stromal differences in salivary gland tumors of a common histopathogenesis but with different biological behavior: a study with picrosirius red and polarizing microscopy,” Acta Histochem. 108(4), 259–264 (2006).
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Bullock, M.

C. J. Hanley, F. Noble, M. Ward, M. Bullock, C. Drifka, M. Mellone, A. Manousopoulou, H. E. Johnston, A. Hayden, S. Thirdborough, Y. Liu, D. M. Smith, T. Mellows, W. J. Kao, S. D. Garbis, A. Mirnezami, T. J. Underwood, K. W. Eliceiri, and G. J. Thomas, “A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers,” Oncotarget 7(5), 6159–6174 (2016).
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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).
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X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
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S. Saalfeld, A. Cardona, V. Hartenstein, and P. Tomančák, “As-rigid-as-possible mosaicking and serial section registration of large ssTEM datasets,” Bioinformatics 26(12), i57–i63 (2010).
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Chang, A. E.

P. P. Provenzano, C. Cuevas, A. E. Chang, V. K. Goel, D. D. Von Hoff, and S. R. Hingorani, “Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma,” Cancer Cell 21(3), 418–429 (2012).
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Chang, S.

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Chen, X.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, “Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure,” Nat. Protoc. 7(4), 654–669 (2012).
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C. J. Cicchetti and J. A. Dubin, “A Microeconometric Analysis of Risk Aversion and the Decision to Self-Insure,” J. Polit. Econ. 102(1), 169–186 (1994).
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[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).
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P. Odetti, M. A. Pronzato, G. Noberasco, L. Cosso, N. Traverso, D. Cottalasso, and U. M. Marinari, “Relationships between glycation and oxidation related fluorescences in rat collagen during aging. An in vivo and in vitro study,” Lab. Invest. 70(1), 61–67 (1994).
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Cottalasso, D.

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Cuevas, C.

P. P. Provenzano, C. Cuevas, A. E. Chang, V. K. Goel, D. D. Von Hoff, and S. R. Hingorani, “Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma,” Cancer Cell 21(3), 418–429 (2012).
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Da Silva, L. B.

B.-M. Kim, J. Eichler, K. M. Reiser, A. M. Rubenchik, and L. B. Da Silva, “Collagen structure and nonlinear susceptibility: Effects of heat, glycation, and enzymatic cleavage on second harmonic signal intensity,” Lasers Surg. Med. 27(4), 329–335 (2000).
[Crossref] [PubMed]

Dayan, D.

I. Allon, M. Vered, A. Buchner, and D. Dayan, “Stromal differences in salivary gland tumors of a common histopathogenesis but with different biological behavior: a study with picrosirius red and polarizing microscopy,” Acta Histochem. 108(4), 259–264 (2006).
[Crossref] [PubMed]

de Lange Davies, C.

M. B. Lilledahl, O. A. Haugen, C. de Lange Davies, and L. O. Svaasand, “Characterization of vulnerable plaques by multiphoton microscopy,” J. Biomed. Opt. 12(4), 044005 (2007).
[Crossref] [PubMed]

Di Martino, E. S.

N. L. Rosin, N. Agabalyan, K. Olsen, G. Martufi, V. Gabriel, J. Biernaskie, and E. S. Di Martino, “Collagen structural alterations contribute to stiffening of tissue after split-thickness skin grafting,” Wound Repair Regen. 24(2), 263–274 (2016).
[Crossref] [PubMed]

Dopkin, D.

B. K. Brisson, E. A. Mauldin, W. Lei, L. K. Vogel, A. M. Power, A. Lo, D. Dopkin, C. Khanna, R. G. Wells, E. Puré, and S. W. Volk, “Type III Collagen Directs Stromal Organization and Limits Metastasis in a Murine Model of Breast Cancer,” Am. J. Pathol. 185(5), 1471–1486 (2015).
[Crossref] [PubMed]

Drifka, C.

C. J. Hanley, F. Noble, M. Ward, M. Bullock, C. Drifka, M. Mellone, A. Manousopoulou, H. E. Johnston, A. Hayden, S. Thirdborough, Y. Liu, D. M. Smith, T. Mellows, W. J. Kao, S. D. Garbis, A. Mirnezami, T. J. Underwood, K. W. Eliceiri, and G. J. Thomas, “A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers,” Oncotarget 7(5), 6159–6174 (2016).
[Crossref] [PubMed]

Drifka, C. R.

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Comparison of Picrosirius Red Staining With Second Harmonic Generation Imaging for the Quantification of Clinically Relevant Collagen Fiber Features in Histopathology Samples,” J. Histochem. Cytochem. 64(9), 519–529 (2016).
[Crossref] [PubMed]

C. R. Drifka, J. Tod, A. G. Loeffler, Y. Liu, G. J. Thomas, K. W. Eliceiri, and W. J. Kao, “Periductal stromal collagen topology of pancreatic ductal adenocarcinoma differs from that of normal and chronic pancreatitis,” Mod. Pathol. 28(11), 1470–1480 (2015).
[Crossref] [PubMed]

Dubin, J. A.

C. J. Cicchetti and J. A. Dubin, “A Microeconometric Analysis of Risk Aversion and the Decision to Self-Insure,” J. Polit. Econ. 102(1), 169–186 (1994).
[Crossref]

Eichler, J.

B.-M. Kim, J. Eichler, K. M. Reiser, A. M. Rubenchik, and L. B. Da Silva, “Collagen structure and nonlinear susceptibility: Effects of heat, glycation, and enzymatic cleavage on second harmonic signal intensity,” Lasers Surg. Med. 27(4), 329–335 (2000).
[Crossref] [PubMed]

Eickhoff, J. C.

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned collagen is a prognostic signature for survival in human breast carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

Eikenberry, E. F.

S. Tanaka, G. Avigad, B. Brodsky, and E. F. Eikenberry, “Glycation induces expansion of the molecular packing of collagen,” J. Mol. Biol. 203(2), 495–505 (1988).
[Crossref] [PubMed]

Eliceiri, K.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an Open-Source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Eliceiri, K. W.

C. J. Hanley, F. Noble, M. Ward, M. Bullock, C. Drifka, M. Mellone, A. Manousopoulou, H. E. Johnston, A. Hayden, S. Thirdborough, Y. Liu, D. M. Smith, T. Mellows, W. J. Kao, S. D. Garbis, A. Mirnezami, T. J. Underwood, K. W. Eliceiri, and G. J. Thomas, “A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers,” Oncotarget 7(5), 6159–6174 (2016).
[Crossref] [PubMed]

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Comparison of Picrosirius Red Staining With Second Harmonic Generation Imaging for the Quantification of Clinically Relevant Collagen Fiber Features in Histopathology Samples,” J. Histochem. Cytochem. 64(9), 519–529 (2016).
[Crossref] [PubMed]

C. R. Drifka, J. Tod, A. G. Loeffler, Y. Liu, G. J. Thomas, K. W. Eliceiri, and W. J. Kao, “Periductal stromal collagen topology of pancreatic ductal adenocarcinoma differs from that of normal and chronic pancreatitis,” Mod. Pathol. 28(11), 1470–1480 (2015).
[Crossref] [PubMed]

A. Keikhosravi, J. S. Bredfeldt, A. K. Sagar, and K. W. Eliceiri, “Second-harmonic generation imaging of cancer,” Methods Cell Biol. 123, 531–546 (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]

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]

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]

Feng, Q.

Z. Nong, C. O’Neil, M. Lei, R. Gros, A. Watson, A. Rizkalla, K. Mequanint, S. Li, M. J. Frontini, Q. Feng, and J. G. Pickering, “Type I Collagen Cleavage Is Essential for Effective Fibrotic Repair after Myocardial Infarction,” Am. J. Pathol. 179(5), 2189–2198 (2011).
[Crossref] [PubMed]

Friedl, A.

M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, and P. J. Keely, “Aligned collagen is a prognostic signature for survival in human breast carcinoma,” Am. J. Pathol. 178(3), 1221–1232 (2011).
[Crossref] [PubMed]

Frise, E.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an Open-Source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Frolov, A.

G. Ayala, J. A. Tuxhorn, T. M. Wheeler, A. Frolov, P. T. Scardino, M. Ohori, M. Wheeler, J. Spitler, and D. R. Rowley, “Reactive stroma as a predictor of biochemical-free recurrence in prostate cancer,” Clin. Cancer Res. 9(13), 4792–4801 (2003).
[PubMed]

Frontini, M. J.

Z. Nong, C. O’Neil, M. Lei, R. Gros, A. Watson, A. Rizkalla, K. Mequanint, S. Li, M. J. Frontini, Q. Feng, and J. G. Pickering, “Type I Collagen Cleavage Is Essential for Effective Fibrotic Repair after Myocardial Infarction,” Am. J. Pathol. 179(5), 2189–2198 (2011).
[Crossref] [PubMed]

Furuya, Y.

M. Kobayashi, Y. Furuya, T. Okabayashi, and K. Araki, “Scanning electron microscopic study of the three-dimensional structure of the collagen sheath surrounding cancer cells after single high-dose irradiation,” Med. Mol. Morphol. 39(2), 106–112 (2006).
[Crossref] [PubMed]

Gabriel, V.

N. L. Rosin, N. Agabalyan, K. Olsen, G. Martufi, V. Gabriel, J. Biernaskie, and E. S. Di Martino, “Collagen structural alterations contribute to stiffening of tissue after split-thickness skin grafting,” Wound Repair Regen. 24(2), 263–274 (2016).
[Crossref] [PubMed]

Garbis, S. D.

C. J. Hanley, F. Noble, M. Ward, M. Bullock, C. Drifka, M. Mellone, A. Manousopoulou, H. E. Johnston, A. Hayden, S. Thirdborough, Y. Liu, D. M. Smith, T. Mellows, W. J. Kao, S. D. Garbis, A. Mirnezami, T. J. Underwood, K. W. Eliceiri, and G. J. Thomas, “A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers,” Oncotarget 7(5), 6159–6174 (2016).
[Crossref] [PubMed]

Goel, V. K.

P. P. Provenzano, C. Cuevas, A. E. Chang, V. K. Goel, D. D. Von Hoff, and S. R. Hingorani, “Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma,” Cancer Cell 21(3), 418–429 (2012).
[Crossref] [PubMed]

Gros, R.

Z. Nong, C. O’Neil, M. Lei, R. Gros, A. Watson, A. Rizkalla, K. Mequanint, S. Li, M. J. Frontini, Q. Feng, and J. G. Pickering, “Type I Collagen Cleavage Is Essential for Effective Fibrotic Repair after Myocardial Infarction,” Am. J. Pathol. 179(5), 2189–2198 (2011).
[Crossref] [PubMed]

Hamlett, A.

A. Hamlett, L. Ryan, P. Serrano-Trespalacios, and R. Wolfinger, “Mixed Models for Assessing Correlation in the Presence of Replication,” J. Air Waste Manag. Assoc. 53(4), 442–450 (2003).
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Hanley, C. J.

C. J. Hanley, F. Noble, M. Ward, M. Bullock, C. Drifka, M. Mellone, A. Manousopoulou, H. E. Johnston, A. Hayden, S. Thirdborough, Y. Liu, D. M. Smith, T. Mellows, W. J. Kao, S. D. Garbis, A. Mirnezami, T. J. Underwood, K. W. Eliceiri, and G. J. Thomas, “A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers,” Oncotarget 7(5), 6159–6174 (2016).
[Crossref] [PubMed]

Hartenstein, V.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an Open-Source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

S. Saalfeld, A. Cardona, V. Hartenstein, and P. Tomančák, “As-rigid-as-possible mosaicking and serial section registration of large ssTEM datasets,” Bioinformatics 26(12), i57–i63 (2010).
[Crossref] [PubMed]

Haugen, O. A.

M. B. Lilledahl, O. A. Haugen, C. de Lange Davies, and L. O. Svaasand, “Characterization of vulnerable plaques by multiphoton microscopy,” J. Biomed. Opt. 12(4), 044005 (2007).
[Crossref] [PubMed]

Hayden, A.

C. J. Hanley, F. Noble, M. Ward, M. Bullock, C. Drifka, M. Mellone, A. Manousopoulou, H. E. Johnston, A. Hayden, S. Thirdborough, Y. Liu, D. M. Smith, T. Mellows, W. J. Kao, S. D. Garbis, A. Mirnezami, T. J. Underwood, K. W. Eliceiri, and G. J. Thomas, “A subset of myofibroblastic cancer-associated fibroblasts regulate collagen fiber elongation, which is prognostic in multiple cancers,” Oncotarget 7(5), 6159–6174 (2016).
[Crossref] [PubMed]

Hingorani, S. R.

P. P. Provenzano, C. Cuevas, A. E. Chang, V. K. Goel, D. D. Von Hoff, and S. R. Hingorani, “Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma,” Cancer Cell 21(3), 418–429 (2012).
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Hoppe, P. E.

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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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Figures (7)

Fig. 1
Fig. 1 Schematic diagram of the birefringence LC-PolScope.
Fig. 2
Fig. 2 PolScope can detect all collagen fibers of colon tissue stained with collagen type I antibody. Collagen type I antibody stained colon tissue sample imaged with bright field (B), (D), PolScope in red channel overlaid on bright field (A), (C). The bottom row shows a closer view of the collagen fibers imaged with PolScope overlaid on bright field (E), PolScope image (F) and the bright-field image (G).
Fig. 3
Fig. 3 Collagen imaging using (A) PolScope, (B) traditional polarized microscope and (B) bright field image of a picrosirius stained pancreatic cancer tissue. The collagen fibers are shown in green and red in (A) and (C), respectively, and the collagen fibers have different colors including orange-red for thick ones and green-yellow for thin ones.
Fig. 4
Fig. 4 Comparison of LC-PolScope and SHG imaging on breast tissue slides. Breast tissue sample imaged with PolScope (A) and SHG (B). The CT-FIRE fiber detection results and ROI selection for PolScope (C) and SHG (D). Part (E) shows the bright field image of the same region. To be noted, CT-FIRE was run on the thresholded PolScope image as displayed in (A). The fibers in (C) and (D) are displayed in randomly selected false colors for visualization purpose. Brighter regions in (A) indicate thick or closely packed fibers.
Fig. 5
Fig. 5 Comparison of PolScope and SHG imaging on pancreatic tissue slides. Pancreatic tissue sample imaged with PolScope (A) and SHG (B). The CT-FIRE fiber detection results and ROI selection for PolScope (C) and SHG (D). Part (E) shows the bright field image of the same region. The fibers in (C) and (D) are displayed in randomly selected false colors for visualization purpose. Brighter regions in (A) indicate thick or closely packed fibers.
Fig. 6
Fig. 6 Bland-Altman plot for orientation (left) and alignment (right) in breast cancer. Red dotted lines show the mean values 0.1959 and −0.0141 for the orientation and alignment. Green lines show the 95% confidence interval.
Fig. 7
Fig. 7 Bland-Altman plot for orientation (left) and alignment (right) in pancreatic cancer. Red dotted lines show the mean values 0.0858 and −0.0458 for the orientation and alignment. Green lines show the 95% confidence interval.

Tables (1)

Tables Icon

Table 1 Orientation and alignment summary results for breast and pancreatic cancer

Metrics