Abstract

In the clinical practice of pathology, trichrome stains are commonly used to highlight collagen and to help evaluate fibrosis. Such stains do delineate collagen deposits but are not molecularly specific and can suffer from staining inconsistencies. Moreover, performing histochemical stain evaluation requires the preparation of additional sections beyond the original hematoxylin- and eosin-stained slides, as well as additional staining steps, which together add cost, time, and workflow complications. We have developed a new microscopy approach, termed DUET (DUal-mode Emission and Transmission) that can be used to extract signals that would typically require special stains or advanced optical methods. Our preliminary analysis demonstrates the potential of using the resulting signals to generate virtual histochemical images that resemble trichrome-stained slides and can support clinical evaluation. We demonstrate advantages of this approach over images acquired from conventional trichrome-stained slides and compare them with images created using second harmonic generation microscopy.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

Full Article  |  PDF Article
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  1. M. D. Shoulders and R. T. Raines, “Collagen structure and stability,” Annu. Rev. Biochem. 78(1), 929–958 (2009).
    [Crossref]
  2. C. Frantz, K. M. Stewart, and V. M. Weaver, “The extracellular matrix at a glance,” J. Cell Sci. 123(24), 4195–4200 (2010).
    [Crossref]
  3. D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
    [Crossref]
  4. M. Yamauchi, T. H. Barker, D. L. Gibbons, and J. M. Kurie, “The fibrotic tumor stroma,” J. Clin. Invest. 128(1), 16–25 (2018).
    [Crossref]
  5. Z.-S.J. Chen and D.-H. Yang, Protein Kinase Inhibitors as Sensitizing Agents for Chemotherapy (Academic Press, 2018).
  6. R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
    [Crossref]
  7. C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
    [Crossref]
  8. D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
    [Crossref]
  9. J. E. Cason, “A rapid one-step Mallory-Heidenhain stain for connective tissue,” Stain Technol. 25(4), 225–226 (1950).
    [Crossref]
  10. R. Lillie and G. Miller, “Histochemical acylation of hydroxyl and amino groups. Effect on the periodic acid Schiff reaction, anionic and cationic dye and Van Gieson collagen stains,” J. Histochem. Cytochem. 12(11), 821–841 (1964).
    [Crossref]
  11. P. Whittaker, R. Kloner, D. Boughner, and J. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
    [Crossref]
  12. C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]
  13. M. Shribak, “Polychromatic polarization microscope: bringing colors to a colorless world,” Sci. Rep. 5(1), 17340 (2015).
    [Crossref]
  14. 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]
  15. L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).
  16. E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
    [Crossref]
  17. E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
    [Crossref]
  18. J. Gu, C. Y. Fu, B. K. Ng, S. Gulam Razul, and S. K. Lim, “Quantitative diagnosis of cervical neoplasia using fluorescence lifetime imaging on haematoxylin and eosin stained tissue sections,” J. Biophotonics 7(7), 483–491 (2014).
    [Crossref]
  19. T. Luo, Y. Lu, S. Liu, D. Lin, and J. Qu, “Enhanced Visualization of Hematoxylin and Eosin Stained Pathological Characteristics by Phasor Approach,” Anal. Chem. 89(17), 9224–9231 (2017).
    [Crossref]
  20. S. Abeysekera, M.P.-L. Ooi, Y.C. Kuang, C.P. Tan, and S.S. Hassan, Detecting spongiosis in stained histopathological specimen using multispectral imaging and machine learning, 2014 IEEE Sensors Applications Symposium (SAS), IEEE, 2014, pp. 195–200.
  21. P.A. Bautista and Y. Yagi, “Localization of Eosinophilic Esophagitis from H&E stained images using multispectral imaging,” Diagn. Pathol. 6(S1), S2 (2011).
    [Crossref]
  22. N. Hashimoto, Y. Murakami, P. A. Bautista, M. Yamaguchi, T. Obi, N. Ohyama, K. Uto, and Y. Kosugi, “Multispectral image enhancement for effective visualization,” Opt. Express 19(10), 9315–9329 (2011).
    [Crossref]
  23. P. A. Bautista, T. Abe, M. Yamaguchi, Y. Yagi, and N. Ohyama, “Digital staining for multispectral images of pathological tissue specimens based on combined classification of spectral transmittance,” Computerized Medical Imaging and Graphics 29(8), 649–657 (2005).
    [Crossref]
  24. R. M. Levenson, A. Fornari, and M. Loda, “Multispectral imaging and pathology: seeing and doing more,” Expert Opin. Med. Diagn. 2(9), 1067–1081 (2008).
    [Crossref]
  25. P. A. Bautista and Y. Yagi, “Digital simulation of staining in histopathology multispectral images: enhancement and linear transformation of spectral transmittance,” J. Biomed. Opt. 17(5), 056013 (2012).
    [Crossref]
  26. P.A. Bautista and Y. Yagi, “Localization of eosinophilic esophagitis from H&E stained images using multispectral imaging,” Diagn. Pathol. 6(S1), S2 (2011).
    [Crossref]
  27. P.A. Bautista, T. Abe, M. Yamaguchi, N. Ohyama, and Y. Yagi, Multispectral image enhancement for H&E stained pathological tissue specimens, Medical Imaging 2008: Visualization, Image-Guided Procedures, and Modeling, International Society for Optics and Photonics, 2008, pp. 691836.
  28. Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
    [Crossref]
  29. D. Goldstein, “The fluorescence of elastic fibres stained with eosin and excited by visible light,” Histochem. J. 1(3), 187–198 (1969).
    [Crossref]
  30. R. Lev and P. J. Stoward, “On the use of eosin as a fluorescent dye to demonstrate mucous cells and other structures in tissue sections,” Histochemie 20(4), 363–377 (1969).
    [Crossref]
  31. J. T. McMahon, J. L. Myles, and R. R. Tubbs, “Demonstration of Immune Complex Deposits Using Fluorescence Microscopy of Hematoxylin and Eosin–Stained Sections of Hollande's Fixed Renal Biopsies,” Mod. Pathol. 15(9), 988–997 (2002).
    [Crossref]
  32. J. Jakubovský, L. Guller, M. Černá, K. Balážová, Š Polák, V. Jakubovská, and P. Babál, “Fluorescence of hematoxylin and eosin-stained histological sections of the human spleen,” Acta Histochem. 104(4), 353–356 (2002).
    [Crossref]
  33. H. F. de Carvalho and S. R. Taboga, “Fluorescence and confocal laser scanning microscopy imaging of elastic fibers in hematoxylin-eosin stained sections,” Histochem. Cell Biol. 106(6), 587–592 (1996).
    [Crossref]
  34. S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
    [Crossref]
  35. M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
    [Crossref]
  36. F. Fereidouni, A. N. Bader, A. Colonna, and H. C. Gerritsen, “Phasor analysis of multiphoton spectral images distinguishes autofluorescence components of in vivo human skin,” J. Biophotonics 7, 589–596 (2014).
    [Crossref]
  37. F. Fereidouni, A. N. Bader, and H. C. Gerritsen, “Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images,” Opt. Express 20(12), 12729–12741 (2012).
    [Crossref]
  38. F. Fereidouni, C. Griffin, A. Todd, and R. Levenson, “Multispectral analysis tools can increase utility of RGB color images in histology,” J. Opt. 20(4), 044007 (2018).
    [Crossref]
  39. D. Fu and X. S. Xie, “Reliable cell segmentation based on spectral phasor analysis of hyperspectral stimulated Raman scattering imaging data,” Anal. Chem. 86(9), 4115–4119 (2014).
    [Crossref]
  40. F. J. Vergeldt, A. Prusova, F. Fereidouni, H. Van Amerongen, H. Van As, T. W. Scheenen, and A. N. Bader, “Multi-component quantitative magnetic resonance imaging by phasor representation,” Sci. Rep. 7(1), 861 (2017).
    [Crossref]
  41. F. Fereidouni, K. Reitsma, and H. C. Gerritsen, “High speed multispectral fluorescence lifetime imaging,” Opt. Express 21(10), 11769–11782 (2013).
    [Crossref]
  42. A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
    [Crossref]
  43. A. L. Fidler, S. P. Boudko, A. Rokas, and B. G. Hudson, “The triple helix of collagens–an ancient protein structure that enabled animal multicellularity and tissue evolution,” J. Cell. Sci. 131(7), jcs203950 (2018).
    [Crossref]
  44. A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
    [Crossref]
  45. A. Likas, N. Vlassis, and J. J. Verbeek, “The global k-means clustering algorithm,” Pattern Recognition 36(2), 451–461 (2003).
    [Crossref]
  46. S.-O. Deininger, M. P. Ebert, A. Futterer, M. Gerhard, and C. Rocken, “MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers,” J. Proteome Res. 7(12), 5230–5236 (2008).
    [Crossref]

2019 (2)

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

2018 (5)

F. Fereidouni, C. Griffin, A. Todd, and R. Levenson, “Multispectral analysis tools can increase utility of RGB color images in histology,” J. Opt. 20(4), 044007 (2018).
[Crossref]

A. L. Fidler, S. P. Boudko, A. Rokas, and B. G. Hudson, “The triple helix of collagens–an ancient protein structure that enabled animal multicellularity and tissue evolution,” J. Cell. Sci. 131(7), jcs203950 (2018).
[Crossref]

M. Yamauchi, T. H. Barker, D. L. Gibbons, and J. M. Kurie, “The fibrotic tumor stroma,” J. Clin. Invest. 128(1), 16–25 (2018).
[Crossref]

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
[Crossref]

2017 (3)

T. Luo, Y. Lu, S. Liu, D. Lin, and J. Qu, “Enhanced Visualization of Hematoxylin and Eosin Stained Pathological Characteristics by Phasor Approach,” Anal. Chem. 89(17), 9224–9231 (2017).
[Crossref]

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

F. J. Vergeldt, A. Prusova, F. Fereidouni, H. Van Amerongen, H. Van As, T. W. Scheenen, and A. N. Bader, “Multi-component quantitative magnetic resonance imaging by phasor representation,” Sci. Rep. 7(1), 861 (2017).
[Crossref]

2016 (3)

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

2015 (2)

M. Shribak, “Polychromatic polarization microscope: bringing colors to a colorless world,” Sci. Rep. 5(1), 17340 (2015).
[Crossref]

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

2014 (4)

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

J. Gu, C. Y. Fu, B. K. Ng, S. Gulam Razul, and S. K. Lim, “Quantitative diagnosis of cervical neoplasia using fluorescence lifetime imaging on haematoxylin and eosin stained tissue sections,” J. Biophotonics 7(7), 483–491 (2014).
[Crossref]

D. Fu and X. S. Xie, “Reliable cell segmentation based on spectral phasor analysis of hyperspectral stimulated Raman scattering imaging data,” Anal. Chem. 86(9), 4115–4119 (2014).
[Crossref]

F. Fereidouni, A. N. Bader, A. Colonna, and H. C. Gerritsen, “Phasor analysis of multiphoton spectral images distinguishes autofluorescence components of in vivo human skin,” J. Biophotonics 7, 589–596 (2014).
[Crossref]

2013 (1)

2012 (3)

F. Fereidouni, A. N. Bader, and H. C. Gerritsen, “Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images,” Opt. Express 20(12), 12729–12741 (2012).
[Crossref]

P. A. Bautista and Y. Yagi, “Digital simulation of staining in histopathology multispectral images: enhancement and linear transformation of spectral transmittance,” J. Biomed. Opt. 17(5), 056013 (2012).
[Crossref]

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]

2011 (4)

P.A. Bautista and Y. Yagi, “Localization of Eosinophilic Esophagitis from H&E stained images using multispectral imaging,” Diagn. Pathol. 6(S1), S2 (2011).
[Crossref]

P.A. Bautista and Y. Yagi, “Localization of eosinophilic esophagitis from H&E stained images using multispectral imaging,” Diagn. Pathol. 6(S1), S2 (2011).
[Crossref]

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

N. Hashimoto, Y. Murakami, P. A. Bautista, M. Yamaguchi, T. Obi, N. Ohyama, K. Uto, and Y. Kosugi, “Multispectral image enhancement for effective visualization,” Opt. Express 19(10), 9315–9329 (2011).
[Crossref]

2010 (1)

C. Frantz, K. M. Stewart, and V. M. Weaver, “The extracellular matrix at a glance,” J. Cell Sci. 123(24), 4195–4200 (2010).
[Crossref]

2009 (1)

M. D. Shoulders and R. T. Raines, “Collagen structure and stability,” Annu. Rev. Biochem. 78(1), 929–958 (2009).
[Crossref]

2008 (4)

D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
[Crossref]

R. M. Levenson, A. Fornari, and M. Loda, “Multispectral imaging and pathology: seeing and doing more,” Expert Opin. Med. Diagn. 2(9), 1067–1081 (2008).
[Crossref]

S.-O. Deininger, M. P. Ebert, A. Futterer, M. Gerhard, and C. Rocken, “MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers,” J. Proteome Res. 7(12), 5230–5236 (2008).
[Crossref]

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref]

2005 (1)

P. A. Bautista, T. Abe, M. Yamaguchi, Y. Yagi, and N. Ohyama, “Digital staining for multispectral images of pathological tissue specimens based on combined classification of spectral transmittance,” Computerized Medical Imaging and Graphics 29(8), 649–657 (2005).
[Crossref]

2003 (1)

A. Likas, N. Vlassis, and J. J. Verbeek, “The global k-means clustering algorithm,” Pattern Recognition 36(2), 451–461 (2003).
[Crossref]

2002 (2)

J. T. McMahon, J. L. Myles, and R. R. Tubbs, “Demonstration of Immune Complex Deposits Using Fluorescence Microscopy of Hematoxylin and Eosin–Stained Sections of Hollande's Fixed Renal Biopsies,” Mod. Pathol. 15(9), 988–997 (2002).
[Crossref]

J. Jakubovský, L. Guller, M. Černá, K. Balážová, Š Polák, V. Jakubovská, and P. Babál, “Fluorescence of hematoxylin and eosin-stained histological sections of the human spleen,” Acta Histochem. 104(4), 353–356 (2002).
[Crossref]

1996 (1)

H. F. de Carvalho and S. R. Taboga, “Fluorescence and confocal laser scanning microscopy imaging of elastic fibers in hematoxylin-eosin stained sections,” Histochem. Cell Biol. 106(6), 587–592 (1996).
[Crossref]

1994 (1)

P. Whittaker, R. Kloner, D. Boughner, and J. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
[Crossref]

1969 (2)

D. Goldstein, “The fluorescence of elastic fibres stained with eosin and excited by visible light,” Histochem. J. 1(3), 187–198 (1969).
[Crossref]

R. Lev and P. J. Stoward, “On the use of eosin as a fluorescent dye to demonstrate mucous cells and other structures in tissue sections,” Histochemie 20(4), 363–377 (1969).
[Crossref]

1964 (1)

R. Lillie and G. Miller, “Histochemical acylation of hydroxyl and amino groups. Effect on the periodic acid Schiff reaction, anionic and cationic dye and Van Gieson collagen stains,” J. Histochem. Cytochem. 12(11), 821–841 (1964).
[Crossref]

1950 (1)

J. E. Cason, “A rapid one-step Mallory-Heidenhain stain for connective tissue,” Stain Technol. 25(4), 225–226 (1950).
[Crossref]

Abe, T.

P. A. Bautista, T. Abe, M. Yamaguchi, Y. Yagi, and N. Ohyama, “Digital staining for multispectral images of pathological tissue specimens based on combined classification of spectral transmittance,” Computerized Medical Imaging and Graphics 29(8), 649–657 (2005).
[Crossref]

P.A. Bautista, T. Abe, M. Yamaguchi, N. Ohyama, and Y. Yagi, Multispectral image enhancement for H&E stained pathological tissue specimens, Medical Imaging 2008: Visualization, Image-Guided Procedures, and Modeling, International Society for Optics and Photonics, 2008, pp. 691836.

Abeysekera, S.

S. Abeysekera, M.P.-L. Ooi, Y.C. Kuang, C.P. Tan, and S.S. Hassan, Detecting spongiosis in stained histopathological specimen using multispectral imaging and machine learning, 2014 IEEE Sensors Applications Symposium (SAS), IEEE, 2014, pp. 195–200.

Adams, C. D.

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

Andronia, L.

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Arzani, D.

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

Asa, S.L.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Awasthi, S.

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

Babál, P.

J. Jakubovský, L. Guller, M. Černá, K. Balážová, Š Polák, V. Jakubovská, and P. Babál, “Fluorescence of hematoxylin and eosin-stained histological sections of the human spleen,” Acta Histochem. 104(4), 353–356 (2002).
[Crossref]

Bader, A. N.

F. J. Vergeldt, A. Prusova, F. Fereidouni, H. Van Amerongen, H. Van As, T. W. Scheenen, and A. N. Bader, “Multi-component quantitative magnetic resonance imaging by phasor representation,” Sci. Rep. 7(1), 861 (2017).
[Crossref]

F. Fereidouni, A. N. Bader, A. Colonna, and H. C. Gerritsen, “Phasor analysis of multiphoton spectral images distinguishes autofluorescence components of in vivo human skin,” J. Biophotonics 7, 589–596 (2014).
[Crossref]

F. Fereidouni, A. N. Bader, and H. C. Gerritsen, “Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images,” Opt. Express 20(12), 12729–12741 (2012).
[Crossref]

Balážová, K.

J. Jakubovský, L. Guller, M. Černá, K. Balážová, Š Polák, V. Jakubovská, and P. Babál, “Fluorescence of hematoxylin and eosin-stained histological sections of the human spleen,” Acta Histochem. 104(4), 353–356 (2002).
[Crossref]

Barbosa, G. O.

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Barker, T. H.

M. Yamauchi, T. H. Barker, D. L. Gibbons, and J. M. Kurie, “The fibrotic tumor stroma,” J. Clin. Invest. 128(1), 16–25 (2018).
[Crossref]

Barzda, V.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Bautista, P. A.

P. A. Bautista and Y. Yagi, “Digital simulation of staining in histopathology multispectral images: enhancement and linear transformation of spectral transmittance,” J. Biomed. Opt. 17(5), 056013 (2012).
[Crossref]

N. Hashimoto, Y. Murakami, P. A. Bautista, M. Yamaguchi, T. Obi, N. Ohyama, K. Uto, and Y. Kosugi, “Multispectral image enhancement for effective visualization,” Opt. Express 19(10), 9315–9329 (2011).
[Crossref]

P. A. Bautista, T. Abe, M. Yamaguchi, Y. Yagi, and N. Ohyama, “Digital staining for multispectral images of pathological tissue specimens based on combined classification of spectral transmittance,” Computerized Medical Imaging and Graphics 29(8), 649–657 (2005).
[Crossref]

Bautista, P.A.

P.A. Bautista and Y. Yagi, “Localization of eosinophilic esophagitis from H&E stained images using multispectral imaging,” Diagn. Pathol. 6(S1), S2 (2011).
[Crossref]

P.A. Bautista and Y. Yagi, “Localization of Eosinophilic Esophagitis from H&E stained images using multispectral imaging,” Diagn. Pathol. 6(S1), S2 (2011).
[Crossref]

P.A. Bautista, T. Abe, M. Yamaguchi, N. Ohyama, and Y. Yagi, Multispectral image enhancement for H&E stained pathological tissue specimens, Medical Imaging 2008: Visualization, Image-Guided Procedures, and Modeling, International Society for Optics and Photonics, 2008, pp. 691836.

Bocklitz, T.

E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
[Crossref]

Bondarik, C.

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Bossuyt, J.

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

Boudko, S. P.

A. L. Fidler, S. P. Boudko, A. Rokas, and B. G. Hudson, “The triple helix of collagens–an ancient protein structure that enabled animal multicellularity and tissue evolution,” J. Cell. Sci. 131(7), jcs203950 (2018).
[Crossref]

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

Boughner, D.

P. Whittaker, R. Kloner, D. Boughner, and J. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
[Crossref]

Bozorgzadeh, A.

D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
[Crossref]

Brennan, P.

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

Brousaides, N.

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

Brown, K. L.

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

Cadoni, G.

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

Caiolfa, V. R.

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref]

Campagnola, P. J.

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]

Carvalho, H. F.

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Cason, J. E.

J. E. Cason, “A rapid one-step Mallory-Heidenhain stain for connective tissue,” Stain Technol. 25(4), 225–226 (1950).
[Crossref]

Cerná, M.

J. Jakubovský, L. Guller, M. Černá, K. Balážová, Š Polák, V. Jakubovská, and P. Babál, “Fluorescence of hematoxylin and eosin-stained histological sections of the human spleen,” Acta Histochem. 104(4), 353–356 (2002).
[Crossref]

Chen, X.

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

Chen, Z.-S.J.

Z.-S.J. Chen and D.-H. Yang, Protein Kinase Inhibitors as Sensitizing Agents for Chemotherapy (Academic Press, 2018).

Chernavskaia, O.

E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
[Crossref]

Chetyrkin, S. V.

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

Chong, T.

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Cisek, R.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Cocan, D.

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Collins, A. B.

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

Colonna, A.

F. Fereidouni, A. N. Bader, A. Colonna, and H. C. Gerritsen, “Phasor analysis of multiphoton spectral images distinguishes autofluorescence components of in vivo human skin,” J. Biophotonics 7, 589–596 (2014).
[Crossref]

Colvin, R. B.

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

Coroian, A.

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Coroian, C.O.

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Darris, C. E.

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

de Carvalho, H. F.

H. F. de Carvalho and S. R. Taboga, “Fluorescence and confocal laser scanning microscopy imaging of elastic fibers in hematoxylin-eosin stained sections,” Histochem. Cell Biol. 106(6), 587–592 (1996).
[Crossref]

de Haan, K.

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Deininger, S.-O.

S.-O. Deininger, M. P. Ebert, A. Futterer, M. Gerhard, and C. Rocken, “MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers,” J. Proteome Res. 7(12), 5230–5236 (2008).
[Crossref]

Della Pelle, P. A.

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

Denzler, J.

E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
[Crossref]

Derchain, S. F.

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Digman, M. A.

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref]

Dom?a, I.

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Drifka, C. R.

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

Ebert, M. P.

S.-O. Deininger, M. P. Ebert, A. Futterer, M. Gerhard, and C. Rocken, “MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers,” J. Proteome Res. 7(12), 5230–5236 (2008).
[Crossref]

Eickhoff, J. C.

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

Eliceiri, K. W.

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

Ernst, G.

E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
[Crossref]

Farris, A. B.

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

Fereidouni, F.

F. Fereidouni, C. Griffin, A. Todd, and R. Levenson, “Multispectral analysis tools can increase utility of RGB color images in histology,” J. Opt. 20(4), 044007 (2018).
[Crossref]

F. J. Vergeldt, A. Prusova, F. Fereidouni, H. Van Amerongen, H. Van As, T. W. Scheenen, and A. N. Bader, “Multi-component quantitative magnetic resonance imaging by phasor representation,” Sci. Rep. 7(1), 861 (2017).
[Crossref]

F. Fereidouni, A. N. Bader, A. Colonna, and H. C. Gerritsen, “Phasor analysis of multiphoton spectral images distinguishes autofluorescence components of in vivo human skin,” J. Biophotonics 7, 589–596 (2014).
[Crossref]

F. Fereidouni, K. Reitsma, and H. C. Gerritsen, “High speed multispectral fluorescence lifetime imaging,” Opt. Express 21(10), 11769–11782 (2013).
[Crossref]

F. Fereidouni, A. N. Bader, and H. C. Gerritsen, “Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images,” Opt. Express 20(12), 12729–12741 (2012).
[Crossref]

Fidler, A. L.

A. L. Fidler, S. P. Boudko, A. Rokas, and B. G. Hudson, “The triple helix of collagens–an ancient protein structure that enabled animal multicellularity and tissue evolution,” J. Cell. Sci. 131(7), jcs203950 (2018).
[Crossref]

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

Fornari, A.

R. M. Levenson, A. Fornari, and M. Loda, “Multispectral imaging and pathology: seeing and doing more,” Expert Opin. Med. Diagn. 2(9), 1067–1081 (2008).
[Crossref]

Frantz, C.

C. Frantz, K. M. Stewart, and V. M. Weaver, “The extracellular matrix at a glance,” J. Cell Sci. 123(24), 4195–4200 (2010).
[Crossref]

Fu, C. Y.

J. Gu, C. Y. Fu, B. K. Ng, S. Gulam Razul, and S. K. Lim, “Quantitative diagnosis of cervical neoplasia using fluorescence lifetime imaging on haematoxylin and eosin stained tissue sections,” J. Biophotonics 7(7), 483–491 (2014).
[Crossref]

Fu, D.

D. Fu and X. S. Xie, “Reliable cell segmentation based on spectral phasor analysis of hyperspectral stimulated Raman scattering imaging data,” Anal. Chem. 86(9), 4115–4119 (2014).
[Crossref]

Futterer, A.

S.-O. Deininger, M. P. Ebert, A. Futterer, M. Gerhard, and C. Rocken, “MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers,” J. Proteome Res. 7(12), 5230–5236 (2008).
[Crossref]

Gerhard, M.

S.-O. Deininger, M. P. Ebert, A. Futterer, M. Gerhard, and C. Rocken, “MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers,” J. Proteome Res. 7(12), 5230–5236 (2008).
[Crossref]

Gerritsen, H. C.

Gibbons, D. L.

M. Yamauchi, T. H. Barker, D. L. Gibbons, and J. M. Kurie, “The fibrotic tumor stroma,” J. Clin. Invest. 128(1), 16–25 (2018).
[Crossref]

Golaraei, A.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Goldstein, D.

D. Goldstein, “The fluorescence of elastic fibres stained with eosin and excited by visible light,” Histochem. J. 1(3), 187–198 (1969).
[Crossref]

Gratton, E.

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref]

Griffin, C.

F. Fereidouni, C. Griffin, A. Todd, and R. Levenson, “Multispectral analysis tools can increase utility of RGB color images in histology,” J. Opt. 20(4), 044007 (2018).
[Crossref]

Grimm, P. C.

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

Gu, J.

J. Gu, C. Y. Fu, B. K. Ng, S. Gulam Razul, and S. K. Lim, “Quantitative diagnosis of cervical neoplasia using fluorescence lifetime imaging on haematoxylin and eosin stained tissue sections,” J. Biophotonics 7(7), 483–491 (2014).
[Crossref]

Gulam Razul, S.

J. Gu, C. Y. Fu, B. K. Ng, S. Gulam Razul, and S. K. Lim, “Quantitative diagnosis of cervical neoplasia using fluorescence lifetime imaging on haematoxylin and eosin stained tissue sections,” J. Biophotonics 7(7), 483–491 (2014).
[Crossref]

Guller, L.

J. Jakubovský, L. Guller, M. Černá, K. Balážová, Š Polák, V. Jakubovská, and P. Babál, “Fluorescence of hematoxylin and eosin-stained histological sections of the human spleen,” Acta Histochem. 104(4), 353–356 (2002).
[Crossref]

Günaydin, H.

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Guntinas-Lichius, O.

E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
[Crossref]

Hashimoto, N.

Hassan, S.S.

S. Abeysekera, M.P.-L. Ooi, Y.C. Kuang, C.P. Tan, and S.S. Hassan, Detecting spongiosis in stained histopathological specimen using multispectral imaging and machine learning, 2014 IEEE Sensors Applications Symposium (SAS), IEEE, 2014, pp. 195–200.

Hudson, B. G.

A. L. Fidler, S. P. Boudko, A. Rokas, and B. G. Hudson, “The triple helix of collagens–an ancient protein structure that enabled animal multicellularity and tissue evolution,” J. Cell. Sci. 131(7), jcs203950 (2018).
[Crossref]

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

Hudson, J. K.

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

Izu, L. T.

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

Jain, A.

D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
[Crossref]

Jakubovská, V.

J. Jakubovský, L. Guller, M. Černá, K. Balážová, Š Polák, V. Jakubovská, and P. Babál, “Fluorescence of hematoxylin and eosin-stained histological sections of the human spleen,” Acta Histochem. 104(4), 353–356 (2002).
[Crossref]

Jakubovský, J.

J. Jakubovský, L. Guller, M. Černá, K. Balážová, Š Polák, V. Jakubovská, and P. Babál, “Fluorescence of hematoxylin and eosin-stained histological sections of the human spleen,” Acta Histochem. 104(4), 353–356 (2002).
[Crossref]

Jerome, W. G.

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

Jian, Z.

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

Joseph, A.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Kao, W. J.

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

Keikhosravi, A.

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

Kloner, R.

P. Whittaker, R. Kloner, D. Boughner, and J. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
[Crossref]

Kosugi, Y.

Krouglov, S.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Kuang, Y.C.

S. Abeysekera, M.P.-L. Ooi, Y.C. Kuang, C.P. Tan, and S.S. Hassan, Detecting spongiosis in stained histopathological specimen using multispectral imaging and machine learning, 2014 IEEE Sensors Applications Symposium (SAS), IEEE, 2014, pp. 195–200.

Kurie, J. M.

M. Yamauchi, T. H. Barker, D. L. Gibbons, and J. M. Kurie, “The fibrotic tumor stroma,” J. Clin. Invest. 128(1), 16–25 (2018).
[Crossref]

Landas, T.

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

LaPoint, R.

D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
[Crossref]

Lemancik, S.

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

Leoncini, E.

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

Lerner, A.

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

Lev, R.

R. Lev and P. J. Stoward, “On the use of eosin as a fluorescent dye to demonstrate mucous cells and other structures in tissue sections,” Histochemie 20(4), 363–377 (1969).
[Crossref]

Levenson, R.

F. Fereidouni, C. Griffin, A. Todd, and R. Levenson, “Multispectral analysis tools can increase utility of RGB color images in histology,” J. Opt. 20(4), 044007 (2018).
[Crossref]

Levenson, R. M.

R. M. Levenson, A. Fornari, and M. Loda, “Multispectral imaging and pathology: seeing and doing more,” Expert Opin. Med. Diagn. 2(9), 1067–1081 (2008).
[Crossref]

Likas, A.

A. Likas, N. Vlassis, and J. J. Verbeek, “The global k-means clustering algorithm,” Pattern Recognition 36(2), 451–461 (2003).
[Crossref]

Lillie, R.

R. Lillie and G. Miller, “Histochemical acylation of hydroxyl and amino groups. Effect on the periodic acid Schiff reaction, anionic and cationic dye and Van Gieson collagen stains,” J. Histochem. Cytochem. 12(11), 821–841 (1964).
[Crossref]

Lim, S. K.

J. Gu, C. Y. Fu, B. K. Ng, S. Gulam Razul, and S. K. Lim, “Quantitative diagnosis of cervical neoplasia using fluorescence lifetime imaging on haematoxylin and eosin stained tissue sections,” J. Biophotonics 7(7), 483–491 (2014).
[Crossref]

Lima, C. S.

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Lin, D.

T. Luo, Y. Lu, S. Liu, D. Lin, and J. Qu, “Enhanced Visualization of Hematoxylin and Eosin Stained Pathological Characteristics by Phasor Approach,” Anal. Chem. 89(17), 9224–9231 (2017).
[Crossref]

Liu, S.

T. Luo, Y. Lu, S. Liu, D. Lin, and J. Qu, “Enhanced Visualization of Hematoxylin and Eosin Stained Pathological Characteristics by Phasor Approach,” Anal. Chem. 89(17), 9224–9231 (2017).
[Crossref]

Liu, Y.

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

Loda, M.

R. M. Levenson, A. Fornari, and M. Loda, “Multispectral imaging and pathology: seeing and doing more,” Expert Opin. Med. Diagn. 2(9), 1067–1081 (2008).
[Crossref]

Loeffler, A. G.

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

Lu, Y.

T. Luo, Y. Lu, S. Liu, D. Lin, and J. Qu, “Enhanced Visualization of Hematoxylin and Eosin Stained Pathological Characteristics by Phasor Approach,” Anal. Chem. 89(17), 9224–9231 (2017).
[Crossref]

Luce, D.

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

Luo, T.

T. Luo, Y. Lu, S. Liu, D. Lin, and J. Qu, “Enhanced Visualization of Hematoxylin and Eosin Stained Pathological Characteristics by Phasor Approach,” Anal. Chem. 89(17), 9224–9231 (2017).
[Crossref]

Mao, Z.

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

Mathewson, K.

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

Matsuo, K.

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

McMahon, J. T.

J. T. McMahon, J. L. Myles, and R. R. Tubbs, “Demonstration of Immune Complex Deposits Using Fluorescence Microscopy of Hematoxylin and Eosin–Stained Sections of Hollande's Fixed Renal Biopsies,” Mod. Pathol. 15(9), 988–997 (2002).
[Crossref]

Mehta, G.

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

Mendonça, G. R.

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Miller, G.

R. Lillie and G. Miller, “Histochemical acylation of hydroxyl and amino groups. Effect on the periodic acid Schiff reaction, anionic and cationic dye and Van Gieson collagen stains,” J. Histochem. Cytochem. 12(11), 821–841 (1964).
[Crossref]

Milot, P.

D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
[Crossref]

Mire?an, V.

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Mirsanaye, K.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Moradi, E.

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

Murakami, Y.

Myles, J. L.

J. T. McMahon, J. L. Myles, and R. R. Tubbs, “Demonstration of Immune Complex Deposits Using Fluorescence Microscopy of Hematoxylin and Eosin–Stained Sections of Hollande's Fixed Renal Biopsies,” Mod. Pathol. 15(9), 988–997 (2002).
[Crossref]

Nadiarynkh, O.

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

Natal, R. A.

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Ng, B. K.

J. Gu, C. Y. Fu, B. K. Ng, S. Gulam Razul, and S. K. Lim, “Quantitative diagnosis of cervical neoplasia using fluorescence lifetime imaging on haematoxylin and eosin stained tissue sections,” J. Biophotonics 7(7), 483–491 (2014).
[Crossref]

Obi, T.

Ohyama, N.

N. Hashimoto, Y. Murakami, P. A. Bautista, M. Yamaguchi, T. Obi, N. Ohyama, K. Uto, and Y. Kosugi, “Multispectral image enhancement for effective visualization,” Opt. Express 19(10), 9315–9329 (2011).
[Crossref]

P. A. Bautista, T. Abe, M. Yamaguchi, Y. Yagi, and N. Ohyama, “Digital staining for multispectral images of pathological tissue specimens based on combined classification of spectral transmittance,” Computerized Medical Imaging and Graphics 29(8), 649–657 (2005).
[Crossref]

P.A. Bautista, T. Abe, M. Yamaguchi, N. Ohyama, and Y. Yagi, Multispectral image enhancement for H&E stained pathological tissue specimens, Medical Imaging 2008: Visualization, Image-Guided Procedures, and Modeling, International Society for Optics and Photonics, 2008, pp. 691836.

Ooi, M.P.-L.

S. Abeysekera, M.P.-L. Ooi, Y.C. Kuang, C.P. Tan, and S.S. Hassan, Detecting spongiosis in stained histopathological specimen using multispectral imaging and machine learning, 2014 IEEE Sensors Applications Symposium (SAS), IEEE, 2014, pp. 195–200.

Orloff, M.

D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
[Crossref]

Paiva, G. R.

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Paludetti, G.

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

Pânzaru, S.C.

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Pedchenko, V. K.

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

Pelegati, V. B.

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Petrelli, L.

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

Pickering, J.

P. Whittaker, R. Kloner, D. Boughner, and J. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
[Crossref]

Plotnikov, S.

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

Polák, Š

J. Jakubovský, L. Guller, M. Černá, K. Balážová, Š Polák, V. Jakubovská, and P. Babál, “Fluorescence of hematoxylin and eosin-stained histological sections of the human spleen,” Acta Histochem. 104(4), 353–356 (2002).
[Crossref]

Pop, I.

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Popp, J.

E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
[Crossref]

Prusova, A.

F. J. Vergeldt, A. Prusova, F. Fereidouni, H. Van Amerongen, H. Van As, T. W. Scheenen, and A. N. Bader, “Multi-component quantitative magnetic resonance imaging by phasor representation,” Sci. Rep. 7(1), 861 (2017).
[Crossref]

Qu, J.

T. Luo, Y. Lu, S. Liu, D. Lin, and J. Qu, “Enhanced Visualization of Hematoxylin and Eosin Stained Pathological Characteristics by Phasor Approach,” Anal. Chem. 89(17), 9224–9231 (2017).
[Crossref]

Raducu, C.

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Raines, R. T.

M. D. Shoulders and R. T. Raines, “Collagen structure and stability,” Annu. Rev. Biochem. 78(1), 929–958 (2009).
[Crossref]

Reitsma, K.

Ricciardi, W.

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

Ricke, W. A.

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

Rivenson, Y.

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Rocken, C.

S.-O. Deininger, M. P. Ebert, A. Futterer, M. Gerhard, and C. Rocken, “MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers,” J. Proteome Res. 7(12), 5230–5236 (2008).
[Crossref]

Rodner, E.

E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
[Crossref]

Rokas, A.

A. L. Fidler, S. P. Boudko, A. Rokas, and B. G. Hudson, “The triple helix of collagens–an ancient protein structure that enabled animal multicellularity and tissue evolution,” J. Cell. Sci. 131(7), jcs203950 (2018).
[Crossref]

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

Rotaru, A.

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Ryan, C.

D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
[Crossref]

Scheenen, T. W.

F. J. Vergeldt, A. Prusova, F. Fereidouni, H. Van Amerongen, H. Van As, T. W. Scheenen, and A. N. Bader, “Multi-component quantitative magnetic resonance imaging by phasor representation,” Sci. Rep. 7(1), 861 (2017).
[Crossref]

Sharma, R.

D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
[Crossref]

Shimkunas, R.

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

Shoulders, M. D.

M. D. Shoulders and R. T. Raines, “Collagen structure and stability,” Annu. Rev. Biochem. 78(1), 929–958 (2009).
[Crossref]

Shribak, M.

M. Shribak, “Polychromatic polarization microscope: bringing colors to a colorless world,” Sci. Rep. 5(1), 17340 (2015).
[Crossref]

Sisk, A. E.

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Smith, R. N.

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

Stewart, K. M.

C. Frantz, K. M. Stewart, and V. M. Weaver, “The extracellular matrix at a glance,” J. Cell Sci. 123(24), 4195–4200 (2010).
[Crossref]

Stoward, P. J.

R. Lev and P. J. Stoward, “On the use of eosin as a fluorescent dye to demonstrate mucous cells and other structures in tissue sections,” Histochemie 20(4), 363–377 (1969).
[Crossref]

Stucker, I.

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

Taboga, S. R.

H. F. de Carvalho and S. R. Taboga, “Fluorescence and confocal laser scanning microscopy imaging of elastic fibers in hematoxylin-eosin stained sections,” Histochem. Cell Biol. 106(6), 587–592 (1996).
[Crossref]

Tan, C.P.

S. Abeysekera, M.P.-L. Ooi, Y.C. Kuang, C.P. Tan, and S.S. Hassan, Detecting spongiosis in stained histopathological specimen using multispectral imaging and machine learning, 2014 IEEE Sensors Applications Symposium (SAS), IEEE, 2014, pp. 195–200.

Todd, A.

F. Fereidouni, C. Griffin, A. Todd, and R. Levenson, “Multispectral analysis tools can increase utility of RGB color images in histology,” J. Opt. 20(4), 044007 (2018).
[Crossref]

Tokarz, D.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Tretheway, D.

D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
[Crossref]

Tubbs, R. R.

J. T. McMahon, J. L. Myles, and R. R. Tubbs, “Demonstration of Immune Complex Deposits Using Fluorescence Microscopy of Hematoxylin and Eosin–Stained Sections of Hollande's Fixed Renal Biopsies,” Mod. Pathol. 15(9), 988–997 (2002).
[Crossref]

Uto, K.

Van Amerongen, H.

F. J. Vergeldt, A. Prusova, F. Fereidouni, H. Van Amerongen, H. Van As, T. W. Scheenen, and A. N. Bader, “Multi-component quantitative magnetic resonance imaging by phasor representation,” Sci. Rep. 7(1), 861 (2017).
[Crossref]

Van As, H.

F. J. Vergeldt, A. Prusova, F. Fereidouni, H. Van Amerongen, H. Van As, T. W. Scheenen, and A. N. Bader, “Multi-component quantitative magnetic resonance imaging by phasor representation,” Sci. Rep. 7(1), 861 (2017).
[Crossref]

Vassallo, J.

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Verbeek, J. J.

A. Likas, N. Vlassis, and J. J. Verbeek, “The global k-means clustering algorithm,” Pattern Recognition 36(2), 451–461 (2003).
[Crossref]

Vergeldt, F. J.

F. J. Vergeldt, A. Prusova, F. Fereidouni, H. Van Amerongen, H. Van As, T. W. Scheenen, and A. N. Bader, “Multi-component quantitative magnetic resonance imaging by phasor representation,” Sci. Rep. 7(1), 861 (2017).
[Crossref]

Vlassis, N.

A. Likas, N. Vlassis, and J. J. Verbeek, “The global k-means clustering algorithm,” Pattern Recognition 36(2), 451–461 (2003).
[Crossref]

von Eggeling, F.

E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
[Crossref]

Wang, H.

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Weaver, V. M.

C. Frantz, K. M. Stewart, and V. M. Weaver, “The extracellular matrix at a glance,” J. Cell Sci. 123(24), 4195–4200 (2010).
[Crossref]

Weber, S. M.

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

Wei, Z.

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Whittaker, P.

P. Whittaker, R. Kloner, D. Boughner, and J. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
[Crossref]

Wilson, B.C.

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Woldeyesus, R.

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

Wood, B. M.

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

Wu, Y.

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Xie, X. S.

D. Fu and X. S. Xie, “Reliable cell segmentation based on spectral phasor analysis of hyperspectral stimulated Raman scattering imaging data,” Anal. Chem. 86(9), 4115–4119 (2014).
[Crossref]

Yagi, Y.

P. A. Bautista and Y. Yagi, “Digital simulation of staining in histopathology multispectral images: enhancement and linear transformation of spectral transmittance,” J. Biomed. Opt. 17(5), 056013 (2012).
[Crossref]

P.A. Bautista and Y. Yagi, “Localization of eosinophilic esophagitis from H&E stained images using multispectral imaging,” Diagn. Pathol. 6(S1), S2 (2011).
[Crossref]

P.A. Bautista and Y. Yagi, “Localization of Eosinophilic Esophagitis from H&E stained images using multispectral imaging,” Diagn. Pathol. 6(S1), S2 (2011).
[Crossref]

P. A. Bautista, T. Abe, M. Yamaguchi, Y. Yagi, and N. Ohyama, “Digital staining for multispectral images of pathological tissue specimens based on combined classification of spectral transmittance,” Computerized Medical Imaging and Graphics 29(8), 649–657 (2005).
[Crossref]

P.A. Bautista, T. Abe, M. Yamaguchi, N. Ohyama, and Y. Yagi, Multispectral image enhancement for H&E stained pathological tissue specimens, Medical Imaging 2008: Visualization, Image-Guided Procedures, and Modeling, International Society for Optics and Photonics, 2008, pp. 691836.

Yamaguchi, M.

N. Hashimoto, Y. Murakami, P. A. Bautista, M. Yamaguchi, T. Obi, N. Ohyama, K. Uto, and Y. Kosugi, “Multispectral image enhancement for effective visualization,” Opt. Express 19(10), 9315–9329 (2011).
[Crossref]

P. A. Bautista, T. Abe, M. Yamaguchi, Y. Yagi, and N. Ohyama, “Digital staining for multispectral images of pathological tissue specimens based on combined classification of spectral transmittance,” Computerized Medical Imaging and Graphics 29(8), 649–657 (2005).
[Crossref]

P.A. Bautista, T. Abe, M. Yamaguchi, N. Ohyama, and Y. Yagi, Multispectral image enhancement for H&E stained pathological tissue specimens, Medical Imaging 2008: Visualization, Image-Guided Procedures, and Modeling, International Society for Optics and Photonics, 2008, pp. 691836.

Yamauchi, M.

M. Yamauchi, T. H. Barker, D. L. Gibbons, and J. M. Kurie, “The fibrotic tumor stroma,” J. Clin. Invest. 128(1), 16–25 (2018).
[Crossref]

Yang, D.-H.

Z.-S.J. Chen and D.-H. Yang, Protein Kinase Inhibitors as Sensitizing Agents for Chemotherapy (Academic Press, 2018).

Zamai, M.

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref]

Zhang, Y.

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Zuckerman, J. E.

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Acta Histochem. (1)

J. Jakubovský, L. Guller, M. Černá, K. Balážová, Š Polák, V. Jakubovská, and P. Babál, “Fluorescence of hematoxylin and eosin-stained histological sections of the human spleen,” Acta Histochem. 104(4), 353–356 (2002).
[Crossref]

Anal. Chem. (2)

T. Luo, Y. Lu, S. Liu, D. Lin, and J. Qu, “Enhanced Visualization of Hematoxylin and Eosin Stained Pathological Characteristics by Phasor Approach,” Anal. Chem. 89(17), 9224–9231 (2017).
[Crossref]

D. Fu and X. S. Xie, “Reliable cell segmentation based on spectral phasor analysis of hyperspectral stimulated Raman scattering imaging data,” Anal. Chem. 86(9), 4115–4119 (2014).
[Crossref]

Annu. Rev. Biochem. (1)

M. D. Shoulders and R. T. Raines, “Collagen structure and stability,” Annu. Rev. Biochem. 78(1), 929–958 (2009).
[Crossref]

Basic Res. Cardiol. (1)

P. Whittaker, R. Kloner, D. Boughner, and J. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
[Crossref]

Biophys. J. (1)

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref]

Circ. Res. (1)

S. Awasthi, L. T. Izu, Z. Mao, Z. Jian, T. Landas, A. Lerner, R. Shimkunas, R. Woldeyesus, J. Bossuyt, and B. M. Wood, “Multimodal SHG-2PF imaging of microdomain Ca2+-contraction coupling in live cardiac myocytes,” Circ. Res. 118(2), e19–e28 (2016).
[Crossref]

Computerized Medical Imaging and Graphics (1)

P. A. Bautista, T. Abe, M. Yamaguchi, Y. Yagi, and N. Ohyama, “Digital staining for multispectral images of pathological tissue specimens based on combined classification of spectral transmittance,” Computerized Medical Imaging and Graphics 29(8), 649–657 (2005).
[Crossref]

Diagn. Pathol. (2)

P.A. Bautista and Y. Yagi, “Localization of eosinophilic esophagitis from H&E stained images using multispectral imaging,” Diagn. Pathol. 6(S1), S2 (2011).
[Crossref]

P.A. Bautista and Y. Yagi, “Localization of Eosinophilic Esophagitis from H&E stained images using multispectral imaging,” Diagn. Pathol. 6(S1), S2 (2011).
[Crossref]

elife (1)

A. L. Fidler, C. E. Darris, S. V. Chetyrkin, V. K. Pedchenko, S. P. Boudko, K. L. Brown, W. G. Jerome, J. K. Hudson, A. Rokas, and B. G. Hudson, “Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues,” elife 6, e24176 (2017).
[Crossref]

Eur. J. Epidemiol. (1)

E. Leoncini, W. Ricciardi, G. Cadoni, D. Arzani, L. Petrelli, G. Paludetti, P. Brennan, D. Luce, I. Stucker, and K. Matsuo, “Adult height and head and neck cancer: a pooled analysis within the INHANCE Consortium,” Eur. J. Epidemiol. 29(1), 35–48 (2014).
[Crossref]

Expert Opin. Med. Diagn. (1)

R. M. Levenson, A. Fornari, and M. Loda, “Multispectral imaging and pathology: seeing and doing more,” Expert Opin. Med. Diagn. 2(9), 1067–1081 (2008).
[Crossref]

Front. Oncol. (1)

D. Tokarz, R. Cisek, A. Joseph, A. Golaraei, K. Mirsanaye, S. Krouglov, S.L. Asa, B.C. Wilson, and V. Barzda, “Characterization of Pancreatic Cancer Tissue using Multiphoton Excitation Fluorescence and Polarization-Sensitive Harmonic Generation Microscopy,” Front. Oncol. 9, 272 (2019).
[Crossref]

Head & Neck (1)

E. Rodner, T. Bocklitz, F. von Eggeling, G. Ernst, O. Chernavskaia, J. Popp, J. Denzler, and O. Guntinas-Lichius, “Fully convolutional networks in multimodal nonlinear microscopy images for automated detection of head and neck carcinoma: Pilot study,” Head & Neck 41(1), hed.25489 (2018).
[Crossref]

Histochem. Cell Biol. (1)

H. F. de Carvalho and S. R. Taboga, “Fluorescence and confocal laser scanning microscopy imaging of elastic fibers in hematoxylin-eosin stained sections,” Histochem. Cell Biol. 106(6), 587–592 (1996).
[Crossref]

Histochem. J. (1)

D. Goldstein, “The fluorescence of elastic fibres stained with eosin and excited by visible light,” Histochem. J. 1(3), 187–198 (1969).
[Crossref]

Histochemie (1)

R. Lev and P. J. Stoward, “On the use of eosin as a fluorescent dye to demonstrate mucous cells and other structures in tissue sections,” Histochemie 20(4), 363–377 (1969).
[Crossref]

J. Am. Soc. Nephrol. (1)

A. B. Farris, C. D. Adams, N. Brousaides, P. A. Della Pelle, A. B. Collins, E. Moradi, R. N. Smith, P. C. Grimm, and R. B. Colvin, “Morphometric and visual evaluation of fibrosis in renal biopsies,” J. Am. Soc. Nephrol. 22(1), 176–186 (2011).
[Crossref]

J. Biomed. Opt. (1)

P. A. Bautista and Y. Yagi, “Digital simulation of staining in histopathology multispectral images: enhancement and linear transformation of spectral transmittance,” J. Biomed. Opt. 17(5), 056013 (2012).
[Crossref]

J. Biophotonics (2)

F. Fereidouni, A. N. Bader, A. Colonna, and H. C. Gerritsen, “Phasor analysis of multiphoton spectral images distinguishes autofluorescence components of in vivo human skin,” J. Biophotonics 7, 589–596 (2014).
[Crossref]

J. Gu, C. Y. Fu, B. K. Ng, S. Gulam Razul, and S. K. Lim, “Quantitative diagnosis of cervical neoplasia using fluorescence lifetime imaging on haematoxylin and eosin stained tissue sections,” J. Biophotonics 7(7), 483–491 (2014).
[Crossref]

J. Cell Sci. (1)

C. Frantz, K. M. Stewart, and V. M. Weaver, “The extracellular matrix at a glance,” J. Cell Sci. 123(24), 4195–4200 (2010).
[Crossref]

J. Cell. Sci. (1)

A. L. Fidler, S. P. Boudko, A. Rokas, and B. G. Hudson, “The triple helix of collagens–an ancient protein structure that enabled animal multicellularity and tissue evolution,” J. Cell. Sci. 131(7), jcs203950 (2018).
[Crossref]

J. Clin. Invest. (1)

M. Yamauchi, T. H. Barker, D. L. Gibbons, and J. M. Kurie, “The fibrotic tumor stroma,” J. Clin. Invest. 128(1), 16–25 (2018).
[Crossref]

J. Histochem. Cytochem. (2)

R. Lillie and G. Miller, “Histochemical acylation of hydroxyl and amino groups. Effect on the periodic acid Schiff reaction, anionic and cationic dye and Van Gieson collagen stains,” J. Histochem. Cytochem. 12(11), 821–841 (1964).
[Crossref]

C. R. Drifka, A. G. Loeffler, K. Mathewson, G. Mehta, A. Keikhosravi, Y. Liu, S. Lemancik, W. A. Ricke, S. M. Weber, and W. J. Kao, “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]

J. Opt. (1)

F. Fereidouni, C. Griffin, A. Todd, and R. Levenson, “Multispectral analysis tools can increase utility of RGB color images in histology,” J. Opt. 20(4), 044007 (2018).
[Crossref]

J. Proteome Res. (1)

S.-O. Deininger, M. P. Ebert, A. Futterer, M. Gerhard, and C. Rocken, “MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers,” J. Proteome Res. 7(12), 5230–5236 (2008).
[Crossref]

Liver Transpl. (1)

D. Tretheway, A. Jain, R. LaPoint, R. Sharma, M. Orloff, P. Milot, A. Bozorgzadeh, and C. Ryan, “Should trichrome stain be used on all post–liver transplant biopsies with hepatitis C virus infection to estimate the fibrosis score?” Liver Transpl. 14, 695–700 (2008).
[Crossref]

Mod. Pathol. (1)

J. T. McMahon, J. L. Myles, and R. R. Tubbs, “Demonstration of Immune Complex Deposits Using Fluorescence Microscopy of Hematoxylin and Eosin–Stained Sections of Hollande's Fixed Renal Biopsies,” Mod. Pathol. 15(9), 988–997 (2002).
[Crossref]

Nat. Biomed. Eng. (1)

Y. Rivenson, H. Wang, Z. Wei, K. de Haan, Y. Zhang, Y. Wu, H. Günaydın, J. E. Zuckerman, T. Chong, and A. E. Sisk, “Virtual histological staining of unlabelled tissue-autofluorescence images via deep learning,” Nat. Biomed. Eng. 3(6), 466–477 (2019).
[Crossref]

Nat. Protoc. (1)

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

Oncotarget (1)

C. R. Drifka, A. G. Loeffler, K. Mathewson, A. Keikhosravi, J. C. Eickhoff, Y. Liu, S. M. Weber, W. J. Kao, and K. W. Eliceiri, “Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection,” Oncotarget 7, 76197 (2016).
[Crossref]

Opt. Express (3)

Pattern Recognition (1)

A. Likas, N. Vlassis, and J. J. Verbeek, “The global k-means clustering algorithm,” Pattern Recognition 36(2), 451–461 (2003).
[Crossref]

ProEnvironment/ProMediu (1)

L. Andronia, V. Mireșan, A. Coroian, I. Pop, C. Răducu, A. Rotaru, D. Cocan, S.C. Pânzaru, I. Domșa, and C.O. Coroian, “Raman Spectroscopy of the Hematoxylin-Eosin Stained Tissue,” ProEnvironment/ProMediu 8(24), 590–600 (2015).

Sci. Rep. (2)

M. Shribak, “Polychromatic polarization microscope: bringing colors to a colorless world,” Sci. Rep. 5(1), 17340 (2015).
[Crossref]

F. J. Vergeldt, A. Prusova, F. Fereidouni, H. Van Amerongen, H. Van As, T. W. Scheenen, and A. N. Bader, “Multi-component quantitative magnetic resonance imaging by phasor representation,” Sci. Rep. 7(1), 861 (2017).
[Crossref]

Stain Technol. (1)

J. E. Cason, “A rapid one-step Mallory-Heidenhain stain for connective tissue,” Stain Technol. 25(4), 225–226 (1950).
[Crossref]

Tumor Biol. (1)

R. A. Natal, J. Vassallo, G. R. Paiva, V. B. Pelegati, G. O. Barbosa, G. R. Mendonça, C. Bondarik, S. F. Derchain, H. F. Carvalho, and C. S. Lima, “Collagen analysis by second-harmonic generation microscopy predicts outcome of luminal breast cancer,” Tumor Biol. 40(4), 1010428318770953 (2018).
[Crossref]

Other (3)

Z.-S.J. Chen and D.-H. Yang, Protein Kinase Inhibitors as Sensitizing Agents for Chemotherapy (Academic Press, 2018).

S. Abeysekera, M.P.-L. Ooi, Y.C. Kuang, C.P. Tan, and S.S. Hassan, Detecting spongiosis in stained histopathological specimen using multispectral imaging and machine learning, 2014 IEEE Sensors Applications Symposium (SAS), IEEE, 2014, pp. 195–200.

P.A. Bautista, T. Abe, M. Yamaguchi, N. Ohyama, and Y. Yagi, Multispectral image enhancement for H&E stained pathological tissue specimens, Medical Imaging 2008: Visualization, Image-Guided Procedures, and Modeling, International Society for Optics and Photonics, 2008, pp. 691836.

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Figures (10)

Fig. 1.
Fig. 1. (Visual abstract) DUET imaging can identify collagen faithfully on H&E-stained slides and generate images that can improve upon conventional histochemical stains for better diagnostics and patient care.
Fig. 2.
Fig. 2. Concept of the spectral phasor approach. A) Transformation of three example spectra into phasor points within the unit circle. B) Synthetic image composed of three (noisy) components. C) The phasor transformation of the image in panel B. D) Fitting a rotating two-dimensional Gaussian function to a phasor plot lobe and the fit parameters.
Fig. 3.
Fig. 3. DUET dual-mode imaging. An H&E slide is illuminated from below using a high color rendering index white LED and a color image is acquired; the white LEDs are turned off, and a 405-nm LED then is used in standard epifluorescence mode to excite fluorescence signals that are then collected using the same light path and camera. The two image modes are naturally pixel-registered. The process is repeated at each position of a whole-slide scanning procedure, using an XY stage and 10X lens. Brightfield image of human (B) kidney (C) liver and (D) breast from H&E slide. E-F: fluorescence images of human kidney, liver and breast from the same regions shown on B, C and D.
Fig. 4.
Fig. 4. Multispectral fluorescence imaging and phasor plot analysis of an H&E-stained slide of human kidney. A) Brightfield image; B) fluorescence color image synthesized from a 420-720-nm spectral data stack; C) spectra from representative regions containing collagen, basement membrane, tubules, and red blood cells; D) same spectra plotted in log scale for better visibility. E) Phasor plot of spectral data from the complete image with phasor clusters representing specific components identified as follows: Col (collagen); AF (autofluorescence); BM (basement membrane); PT (proximal tubules); and RBC (red blood cells). F-I) phasor-segmented images corresponding to the outlined clusters.
Fig. 5.
Fig. 5. RGB images of H&E-stained slide fluorescence. Top row: kidney; middle row: ovarian cancer; bottom row: breast cancer. Phasor plots are shown in the middle column, with unmixed collagen signals shown as monochrome images and as blue overlays on top of the original brightfield images. Compared to the multispectral phasor plot shown in Fig. 4, these plots have fewer clusters, and it is not possible to separate collagen from basement membrane signals. The shapes of the phasor clusters differ from each other, reflecting the fact the slides were stained in different laboratories, and that 3 different color cameras (CCD, CMOS and 3-band filter-wheel-equipped monochrome) were used to capture these images.
Fig. 6.
Fig. 6. Brightfield and fluorescence images from the slides processed at UC Davis and Johns Hopkins University. Phasor plots demonstrate extractable components in spite of large color discrepancy between the fluorescence images from two institutions.
Fig. 7.
Fig. 7. A) Brightfield and B) fluorescence image of human liver biopsy from H&E slide. C) Serial section from the same region stained with trichrome. D) SHG signal and E) collagen image from DUET imaged from H&E slide. F) Overlaid image of collagen distribution from DUET on brightfield image. Zoomed in version of G) brightfield, H) overlaid, I) SHG and J) collagen extracted from DUET setup.
Fig. 8.
Fig. 8. A) Brightfield and B) fluorescence image of kidney biopsy from an H&E slide. C) Image of a serial section stained with trichrome. D) SHG image of the same region. Unlike DUET, SHG is does not highlight collagen structures (mostly collagen IV) within the glomerulus. E) Collagen distribution from the DUET-analyzed fluorescence image. F) Overlaid image of collagen distribution from DUET onto the corresponding brightfield image.
Fig. 9.
Fig. 9. Serial section images of kidney stained with H&E (A), DUET overlaid (B), IHC staining for collagen type III (C). The blue pseudocolor in panel B correlates well with COLIII IHC.
Fig. 10.
Fig. 10. A) Brightfield and B) DUET overlay image. C) Image of a serial section stained with trichrome. The yellow arrow points to the location of a nerve and the green arrow indicates the smooth muscle of arterial wall. These structures do not contain collagen, and do not show as positive in the DUET overlay image; however, they do appear blue (positive for collagen) in the trichrome-stained slide.

Equations (6)

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G = l = 1 L a l cos ( 2 π L l ) / l = 1 L a l  and  S = l = 1 L a l sin ( 2 π L l ) / l = 1 L a l
f ( x , y ) = A exp ( a ( x x 0 ) 2 2 b ( x x 0 ) ( y y 0 ) c ( y y 0 ) 2 )
a = cos 2 θ 2 σ x 2 + sin 2 θ 2 σ y 2 b = sin 2 θ 4 σ x 2 + sin 2 θ 4 σ y 2 c = sin 2 θ 2 σ x 2 + cos 2 θ 2 σ y 2
B i = I 0 e O D i
O D i = ln ( I 0 B i )
O i = I 0 e ( O D i + c i F i ) = I 0 e ln ( I 0 / B i ) c i F i = B i e c i F i