Abstract

Tumor-adjacent “normal” tissue constitutes a peri-tumoral field that affects early cancer detection, risk assessment, surgical decision, and postoperative surveillance. Modern genetic analysis has revealed valuable information from this field, but without the spatial resolution of optical microscopy to understand the vital microenvironments that surround individual cells. Rapidly advanced optical imaging techniques free of labor-intensive sample preparation, despite great promise to perform slide-free imaging of cell structure and shift the histology-centered cancer diagnostic paradigm, have lacked compatible and complementary histochemical imaging of cell function or phenotype to interrogate the peri-tumoral field. In the first part (Part I) of this two-part series study, we developed a technique of slide-free virtual histochemistry to phenotype various cells in in vivo animal and ex vivo human tissue. Here, in the second part (Part II) of this two-part series study, we employ this technique to examine various peri-tumoral fields and produce the volumetric histochemical evidence of field cancerization consistent with the structural changes at larger spatial scales. We also link the field cancerization with cancer dormancy in a significant portion of breast cancer patients.

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

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  28. M. Kamei, W. B. Saunders, K. J. Bayless, L. Dye, G. E. Davis, and B. M. Weinstein, “Endothelial tubes assemble from intracellular vacuoles in vivo,” Nature 442(7101), 453–456 (2006).
    [Crossref] [PubMed]

2018 (1)

2017 (8)

R. He, Y. Xu, L. Zhang, S. Ma, X. Wang, D. Ye, and M. Ji, “Dual-phase stimulated Raman scattering microscopy for real-time two-color imaging,” Optica 4(1), 44–47 (2017).
[Crossref]

D. A. Orringer, B. Pandian, Y. S. Niknafs, T. C. Hollon, J. Boyle, S. Lewis, M. Garrard, S. L. Hervey-Jumper, H. J. L. Garton, C. O. Maher, J. A. Heth, O. Sagher, D. A. Wilkinson, M. Snuderl, S. Venneti, S. H. Ramkissoon, K. A. McFadden, A. Fisher-Hubbard, A. P. Lieberman, T. D. Johnson, X. S. Xie, J. K. Trautman, C. W. Freudiger, and S. Camelo-Piragua, “Rapid intraoperative histology of unprocessed surgical specimens via fibre-laser-based stimulated Raman scattering microscopy,” Nat. Biomed. Eng. 1, 0027 (2017).

T. T. W. Wong, R. Zhang, P. Hai, C. Zhang, M. A. Pleitez, R. L. Aft, D. V. Novack, and L. V. Wang, “Fast label-free multilayered histology-like imaging of human breast cancer by photoacoustic microscopy,” Sci. Adv. 3, e1602168 (2017).

F. Fereidouni, Z. T. Harmany, M. Tian, A. Todd, J. A. Kintner, J. D. McPherson, A. D. Borowsky, J. Bishop, M. Lechpammer, S. G. Demos, and R. Levenson, “Microscopy with ultraviolet surface excitation for rapid slide-free histology,” Nat. Biomed. Eng. 1(12), 957–966 (2017).
[Crossref]

A. K. Glaser, N. P. Reder, Y. Chen, E. F. McCarty, C. Yin, L. Wei, Y. Wang, L. D. True, and J. T. C. Liu, “Light-sheet microscopy for slide-free non-destructive pathology of large clinical specimens,” Nat. Biomed. Eng. 1, 0084 (2017).

D. A. Orringer and S. Camelo-Piragua, “Fast and slide-free imaging,” Nat. Biomed. Eng. 1(12), 926–928 (2017).
[Crossref]

N. Tanaka, S. Kanatani, R. Tomer, C. Sahlgren, P. Kronqvist, D. Kaczynska, L. Louhivuori, L. Kis, C. Lindh, P. Mitura, A. Stepulak, S. Corvigno, J. Hartman, P. Micke, A. Mezheyeuski, C. Strell, J. W. Carlson, C. F. Moro, H. Dahlstrand, A. Östman, K. Matsumoto, P. Wiklund, M. Oya, A. Miyakawa, K. Deisseroth, and P. Uhlén, “Whole-tissue biopsy phenotyping of three-dimensional tumours reveals patterns of cancer heterogeneity,” Nat. Biomed. Eng. 1(10), 796–806 (2017).
[Crossref]

K. Curtius, N. A. Wright, and T. A. Graham, “An evolutionary perspective on field cancerization,” Nat. Rev. Cancer 18(1), 19–32 (2017).
[Crossref] [PubMed]

2016 (4)

S. R. Kantelhardt, D. Kalasauskas, K. König, E. Kim, M. Weinigel, A. Uchugonova, and A. Giese, “In vivo multiphoton tomography and fluorescence lifetime imaging of human brain tumor tissue,” J. Neurooncol. 127(3), 473–482 (2016).
[Crossref] [PubMed]

J. M. Szulczewski, D. R. Inman, D. Entenberg, S. M. Ponik, J. Aguirre-Ghiso, J. Castracane, J. Condeelis, K. W. Eliceiri, and P. J. Keely, “In vivo visualization of stromal macrophages via label-free FLIM-based metabolite imaging,” Sci. Rep. 6(1), 25086 (2016).
[Crossref] [PubMed]

K. L. Harper, M. S. Sosa, D. Entenberg, H. Hosseini, J. F. Cheung, R. Nobre, A. Avivar-Valderas, C. Nagi, N. Girnius, R. J. Davis, E. F. Farias, J. Condeelis, C. A. Klein, and J. A. Aguirre-Ghiso, “Mechanism of early dissemination and metastasis in Her2+ mammary cancer,” Nature 540(7634), 588–592 (2016).
[Crossref] [PubMed]

H. Hosseini, M. M. S. Obradović, M. Hoffmann, K. L. Harper, M. S. Sosa, M. Werner-Klein, L. K. Nanduri, C. Werno, C. Ehrl, M. Maneck, N. Patwary, G. Haunschild, M. Gužvić, C. Reimelt, M. Grauvogl, N. Eichner, F. Weber, A. D. Hartkopf, F.-A. Taran, S. Y. Brucker, T. Fehm, B. Rack, S. Buchholz, R. Spang, G. Meister, J. A. Aguirre-Ghiso, and C. A. Klein, “Early dissemination seeds metastasis in breast cancer,” Nature 540(7634), 552–558 (2016).
[Crossref] [PubMed]

2015 (1)

D. A. Lawson, N. R. Bhakta, K. Kessenbrock, K. D. Prummel, Y. Yu, K. Takai, A. Zhou, H. Eyob, S. Balakrishnan, C.-Y. Wang, P. Yaswen, A. Goga, and Z. Werb, “Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells,” Nature 526(7571), 131–135 (2015).
[Crossref] [PubMed]

2014 (2)

Y. K. Tao, D. Shen, Y. Sheikine, O. O. Ahsen, H. H. Wang, D. B. Schmolze, N. B. Johnson, J. S. Brooker, A. E. Cable, J. L. Connolly, and J. G. Fujimoto, “Assessment of breast pathologies using nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 111(43), 15304–15309 (2014).
[Crossref] [PubMed]

O. Assayag, M. Antoine, B. Sigal-Zafrani, M. Riben, F. Harms, A. Burcheri, K. Grieve, E. Dalimier, B. Le Conte de Poly, and C. Boccara, “Large field, high resolution full-field optical coherence tomography: a pre-clinical study of human Breast tissue and cancer assessment,” Technol. Cancer Res. Treat. 13, 455–468 (2014).

2012 (2)

N. Roberts, D. Magee, Y. Song, K. Brabazon, M. Shires, D. Crellin, N. M. Orsi, R. Quirke, P. Quirke, and D. Treanor, “Toward routine use of 3D histopathology as a research tool,” Am. J. Pathol. 180(5), 1835–1842 (2012).
[Crossref] [PubMed]

B. K. Wright, L. M. Andrews, M. R. Jones, C. Stringari, M. A. Digman, and E. Gratton, “Phasor-FLIM analysis of NADH distribution and localization in the nucleus of live progenitor myoblast cells,” Microsc. Res. Tech. 75(12), 1717–1722 (2012).
[Crossref] [PubMed]

2008 (1)

A. J. Ewald, A. Brenot, M. Duong, B. S. Chan, and Z. Werb, “Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis,” Dev. Cell 14(4), 570–581 (2008).
[Crossref] [PubMed]

2007 (2)

J. A. Aguirre-Ghiso, “Models, mechanisms and clinical evidence for cancer dormancy,” Nat. Rev. Cancer 7(11), 834–846 (2007).
[Crossref] [PubMed]

G. D. Dakubo, J. P. Jakupciak, M. A. Birch-Machin, and R. L. Parr, “Clinical implications and utility of field cancerization,” Cancer Cell Int. 7(1), 2 (2007).
[Crossref] [PubMed]

2006 (1)

M. Kamei, W. B. Saunders, K. J. Bayless, L. Dye, G. E. Davis, and B. M. Weinstein, “Endothelial tubes assemble from intracellular vacuoles in vivo,” Nature 442(7101), 453–456 (2006).
[Crossref] [PubMed]

2005 (3)

W. A. Woodward, M. S. Chen, F. Behbod, and J. M. Rosen, “On mammary stem cells,” J. Cell Sci. 118(16), 3585–3594 (2005).
[Crossref] [PubMed]

R. Rouzier, C. M. Perou, W. F. Symmans, N. Ibrahim, M. Cristofanilli, K. Anderson, K. R. Hess, J. Stec, M. Ayers, P. Wagner, P. Morandi, C. Fan, I. Rabiul, J. S. Ross, G. N. Hortobagyi, and L. Pusztai, “Breast cancer molecular subtypes respond differently to preoperative chemotherapy,” Clin. Cancer Res. 11(16), 5678–5685 (2005).
[Crossref] [PubMed]

B. Weigelt, J. L. Peterse, and L. J. van ’t Veer, “Breast cancer metastasis: markers and models,” Nat. Rev. Cancer 5(8), 591–602 (2005).
[Crossref] [PubMed]

2003 (1)

B. J. Braakhuis, M. P. Tabor, J. A. Kummer, C. R. Leemans, and R. H. Brakenhoff, “A genetic explanation of Slaughter’s concept of field cancerization: evidence and clinical implications,” Cancer Res. 63(8), 1727–1730 (2003).
[PubMed]

1996 (1)

G. Deng, Y. Lu, G. Zlotnikov, A. D. Thor, and H. S. Smith, “Loss of heterozygosity in normal tissue adjacent to breast carcinomas,” Science 274(5295), 2057–2059 (1996).
[Crossref] [PubMed]

1953 (1)

D. P. Slaughter, H. W. Southwick, and W. Smejkal, “Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin,” Cancer 6(5), 963–968 (1953).
[Crossref] [PubMed]

Aft, R. L.

T. T. W. Wong, R. Zhang, P. Hai, C. Zhang, M. A. Pleitez, R. L. Aft, D. V. Novack, and L. V. Wang, “Fast label-free multilayered histology-like imaging of human breast cancer by photoacoustic microscopy,” Sci. Adv. 3, e1602168 (2017).

Aguirre-Ghiso, J.

J. M. Szulczewski, D. R. Inman, D. Entenberg, S. M. Ponik, J. Aguirre-Ghiso, J. Castracane, J. Condeelis, K. W. Eliceiri, and P. J. Keely, “In vivo visualization of stromal macrophages via label-free FLIM-based metabolite imaging,” Sci. Rep. 6(1), 25086 (2016).
[Crossref] [PubMed]

Aguirre-Ghiso, J. A.

K. L. Harper, M. S. Sosa, D. Entenberg, H. Hosseini, J. F. Cheung, R. Nobre, A. Avivar-Valderas, C. Nagi, N. Girnius, R. J. Davis, E. F. Farias, J. Condeelis, C. A. Klein, and J. A. Aguirre-Ghiso, “Mechanism of early dissemination and metastasis in Her2+ mammary cancer,” Nature 540(7634), 588–592 (2016).
[Crossref] [PubMed]

H. Hosseini, M. M. S. Obradović, M. Hoffmann, K. L. Harper, M. S. Sosa, M. Werner-Klein, L. K. Nanduri, C. Werno, C. Ehrl, M. Maneck, N. Patwary, G. Haunschild, M. Gužvić, C. Reimelt, M. Grauvogl, N. Eichner, F. Weber, A. D. Hartkopf, F.-A. Taran, S. Y. Brucker, T. Fehm, B. Rack, S. Buchholz, R. Spang, G. Meister, J. A. Aguirre-Ghiso, and C. A. Klein, “Early dissemination seeds metastasis in breast cancer,” Nature 540(7634), 552–558 (2016).
[Crossref] [PubMed]

J. A. Aguirre-Ghiso, “Models, mechanisms and clinical evidence for cancer dormancy,” Nat. Rev. Cancer 7(11), 834–846 (2007).
[Crossref] [PubMed]

Ahsen, O. O.

Y. K. Tao, D. Shen, Y. Sheikine, O. O. Ahsen, H. H. Wang, D. B. Schmolze, N. B. Johnson, J. S. Brooker, A. E. Cable, J. L. Connolly, and J. G. Fujimoto, “Assessment of breast pathologies using nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 111(43), 15304–15309 (2014).
[Crossref] [PubMed]

Anderson, K.

R. Rouzier, C. M. Perou, W. F. Symmans, N. Ibrahim, M. Cristofanilli, K. Anderson, K. R. Hess, J. Stec, M. Ayers, P. Wagner, P. Morandi, C. Fan, I. Rabiul, J. S. Ross, G. N. Hortobagyi, and L. Pusztai, “Breast cancer molecular subtypes respond differently to preoperative chemotherapy,” Clin. Cancer Res. 11(16), 5678–5685 (2005).
[Crossref] [PubMed]

Andrews, L. M.

B. K. Wright, L. M. Andrews, M. R. Jones, C. Stringari, M. A. Digman, and E. Gratton, “Phasor-FLIM analysis of NADH distribution and localization in the nucleus of live progenitor myoblast cells,” Microsc. Res. Tech. 75(12), 1717–1722 (2012).
[Crossref] [PubMed]

Antoine, M.

O. Assayag, M. Antoine, B. Sigal-Zafrani, M. Riben, F. Harms, A. Burcheri, K. Grieve, E. Dalimier, B. Le Conte de Poly, and C. Boccara, “Large field, high resolution full-field optical coherence tomography: a pre-clinical study of human Breast tissue and cancer assessment,” Technol. Cancer Res. Treat. 13, 455–468 (2014).

Assayag, O.

O. Assayag, M. Antoine, B. Sigal-Zafrani, M. Riben, F. Harms, A. Burcheri, K. Grieve, E. Dalimier, B. Le Conte de Poly, and C. Boccara, “Large field, high resolution full-field optical coherence tomography: a pre-clinical study of human Breast tissue and cancer assessment,” Technol. Cancer Res. Treat. 13, 455–468 (2014).

Avivar-Valderas, A.

K. L. Harper, M. S. Sosa, D. Entenberg, H. Hosseini, J. F. Cheung, R. Nobre, A. Avivar-Valderas, C. Nagi, N. Girnius, R. J. Davis, E. F. Farias, J. Condeelis, C. A. Klein, and J. A. Aguirre-Ghiso, “Mechanism of early dissemination and metastasis in Her2+ mammary cancer,” Nature 540(7634), 588–592 (2016).
[Crossref] [PubMed]

Ayers, M.

R. Rouzier, C. M. Perou, W. F. Symmans, N. Ibrahim, M. Cristofanilli, K. Anderson, K. R. Hess, J. Stec, M. Ayers, P. Wagner, P. Morandi, C. Fan, I. Rabiul, J. S. Ross, G. N. Hortobagyi, and L. Pusztai, “Breast cancer molecular subtypes respond differently to preoperative chemotherapy,” Clin. Cancer Res. 11(16), 5678–5685 (2005).
[Crossref] [PubMed]

Balakrishnan, S.

D. A. Lawson, N. R. Bhakta, K. Kessenbrock, K. D. Prummel, Y. Yu, K. Takai, A. Zhou, H. Eyob, S. Balakrishnan, C.-Y. Wang, P. Yaswen, A. Goga, and Z. Werb, “Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells,” Nature 526(7571), 131–135 (2015).
[Crossref] [PubMed]

Bayless, K. J.

M. Kamei, W. B. Saunders, K. J. Bayless, L. Dye, G. E. Davis, and B. M. Weinstein, “Endothelial tubes assemble from intracellular vacuoles in vivo,” Nature 442(7101), 453–456 (2006).
[Crossref] [PubMed]

Behbod, F.

W. A. Woodward, M. S. Chen, F. Behbod, and J. M. Rosen, “On mammary stem cells,” J. Cell Sci. 118(16), 3585–3594 (2005).
[Crossref] [PubMed]

Bhakta, N. R.

D. A. Lawson, N. R. Bhakta, K. Kessenbrock, K. D. Prummel, Y. Yu, K. Takai, A. Zhou, H. Eyob, S. Balakrishnan, C.-Y. Wang, P. Yaswen, A. Goga, and Z. Werb, “Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells,” Nature 526(7571), 131–135 (2015).
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M. Kamei, W. B. Saunders, K. J. Bayless, L. Dye, G. E. Davis, and B. M. Weinstein, “Endothelial tubes assemble from intracellular vacuoles in vivo,” Nature 442(7101), 453–456 (2006).
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J. M. Szulczewski, D. R. Inman, D. Entenberg, S. M. Ponik, J. Aguirre-Ghiso, J. Castracane, J. Condeelis, K. W. Eliceiri, and P. J. Keely, “In vivo visualization of stromal macrophages via label-free FLIM-based metabolite imaging,” Sci. Rep. 6(1), 25086 (2016).
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A. J. Ewald, A. Brenot, M. Duong, B. S. Chan, and Z. Werb, “Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis,” Dev. Cell 14(4), 570–581 (2008).
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Eyob, H.

D. A. Lawson, N. R. Bhakta, K. Kessenbrock, K. D. Prummel, Y. Yu, K. Takai, A. Zhou, H. Eyob, S. Balakrishnan, C.-Y. Wang, P. Yaswen, A. Goga, and Z. Werb, “Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells,” Nature 526(7571), 131–135 (2015).
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K. L. Harper, M. S. Sosa, D. Entenberg, H. Hosseini, J. F. Cheung, R. Nobre, A. Avivar-Valderas, C. Nagi, N. Girnius, R. J. Davis, E. F. Farias, J. Condeelis, C. A. Klein, and J. A. Aguirre-Ghiso, “Mechanism of early dissemination and metastasis in Her2+ mammary cancer,” Nature 540(7634), 588–592 (2016).
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H. Hosseini, M. M. S. Obradović, M. Hoffmann, K. L. Harper, M. S. Sosa, M. Werner-Klein, L. K. Nanduri, C. Werno, C. Ehrl, M. Maneck, N. Patwary, G. Haunschild, M. Gužvić, C. Reimelt, M. Grauvogl, N. Eichner, F. Weber, A. D. Hartkopf, F.-A. Taran, S. Y. Brucker, T. Fehm, B. Rack, S. Buchholz, R. Spang, G. Meister, J. A. Aguirre-Ghiso, and C. A. Klein, “Early dissemination seeds metastasis in breast cancer,” Nature 540(7634), 552–558 (2016).
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F. Fereidouni, Z. T. Harmany, M. Tian, A. Todd, J. A. Kintner, J. D. McPherson, A. D. Borowsky, J. Bishop, M. Lechpammer, S. G. Demos, and R. Levenson, “Microscopy with ultraviolet surface excitation for rapid slide-free histology,” Nat. Biomed. Eng. 1(12), 957–966 (2017).
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Freudiger, C. W.

D. A. Orringer, B. Pandian, Y. S. Niknafs, T. C. Hollon, J. Boyle, S. Lewis, M. Garrard, S. L. Hervey-Jumper, H. J. L. Garton, C. O. Maher, J. A. Heth, O. Sagher, D. A. Wilkinson, M. Snuderl, S. Venneti, S. H. Ramkissoon, K. A. McFadden, A. Fisher-Hubbard, A. P. Lieberman, T. D. Johnson, X. S. Xie, J. K. Trautman, C. W. Freudiger, and S. Camelo-Piragua, “Rapid intraoperative histology of unprocessed surgical specimens via fibre-laser-based stimulated Raman scattering microscopy,” Nat. Biomed. Eng. 1, 0027 (2017).

Fujimoto, J. G.

Y. K. Tao, D. Shen, Y. Sheikine, O. O. Ahsen, H. H. Wang, D. B. Schmolze, N. B. Johnson, J. S. Brooker, A. E. Cable, J. L. Connolly, and J. G. Fujimoto, “Assessment of breast pathologies using nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 111(43), 15304–15309 (2014).
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Garton, H. J. L.

D. A. Orringer, B. Pandian, Y. S. Niknafs, T. C. Hollon, J. Boyle, S. Lewis, M. Garrard, S. L. Hervey-Jumper, H. J. L. Garton, C. O. Maher, J. A. Heth, O. Sagher, D. A. Wilkinson, M. Snuderl, S. Venneti, S. H. Ramkissoon, K. A. McFadden, A. Fisher-Hubbard, A. P. Lieberman, T. D. Johnson, X. S. Xie, J. K. Trautman, C. W. Freudiger, and S. Camelo-Piragua, “Rapid intraoperative histology of unprocessed surgical specimens via fibre-laser-based stimulated Raman scattering microscopy,” Nat. Biomed. Eng. 1, 0027 (2017).

Giese, A.

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B. K. Wright, L. M. Andrews, M. R. Jones, C. Stringari, M. A. Digman, and E. Gratton, “Phasor-FLIM analysis of NADH distribution and localization in the nucleus of live progenitor myoblast cells,” Microsc. Res. Tech. 75(12), 1717–1722 (2012).
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K. L. Harper, M. S. Sosa, D. Entenberg, H. Hosseini, J. F. Cheung, R. Nobre, A. Avivar-Valderas, C. Nagi, N. Girnius, R. J. Davis, E. F. Farias, J. Condeelis, C. A. Klein, and J. A. Aguirre-Ghiso, “Mechanism of early dissemination and metastasis in Her2+ mammary cancer,” Nature 540(7634), 588–592 (2016).
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O. Assayag, M. Antoine, B. Sigal-Zafrani, M. Riben, F. Harms, A. Burcheri, K. Grieve, E. Dalimier, B. Le Conte de Poly, and C. Boccara, “Large field, high resolution full-field optical coherence tomography: a pre-clinical study of human Breast tissue and cancer assessment,” Technol. Cancer Res. Treat. 13, 455–468 (2014).

Lechpammer, M.

F. Fereidouni, Z. T. Harmany, M. Tian, A. Todd, J. A. Kintner, J. D. McPherson, A. D. Borowsky, J. Bishop, M. Lechpammer, S. G. Demos, and R. Levenson, “Microscopy with ultraviolet surface excitation for rapid slide-free histology,” Nat. Biomed. Eng. 1(12), 957–966 (2017).
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D. A. Orringer, B. Pandian, Y. S. Niknafs, T. C. Hollon, J. Boyle, S. Lewis, M. Garrard, S. L. Hervey-Jumper, H. J. L. Garton, C. O. Maher, J. A. Heth, O. Sagher, D. A. Wilkinson, M. Snuderl, S. Venneti, S. H. Ramkissoon, K. A. McFadden, A. Fisher-Hubbard, A. P. Lieberman, T. D. Johnson, X. S. Xie, J. K. Trautman, C. W. Freudiger, and S. Camelo-Piragua, “Rapid intraoperative histology of unprocessed surgical specimens via fibre-laser-based stimulated Raman scattering microscopy,” Nat. Biomed. Eng. 1, 0027 (2017).

Lieberman, A. P.

D. A. Orringer, B. Pandian, Y. S. Niknafs, T. C. Hollon, J. Boyle, S. Lewis, M. Garrard, S. L. Hervey-Jumper, H. J. L. Garton, C. O. Maher, J. A. Heth, O. Sagher, D. A. Wilkinson, M. Snuderl, S. Venneti, S. H. Ramkissoon, K. A. McFadden, A. Fisher-Hubbard, A. P. Lieberman, T. D. Johnson, X. S. Xie, J. K. Trautman, C. W. Freudiger, and S. Camelo-Piragua, “Rapid intraoperative histology of unprocessed surgical specimens via fibre-laser-based stimulated Raman scattering microscopy,” Nat. Biomed. Eng. 1, 0027 (2017).

Lindh, C.

N. Tanaka, S. Kanatani, R. Tomer, C. Sahlgren, P. Kronqvist, D. Kaczynska, L. Louhivuori, L. Kis, C. Lindh, P. Mitura, A. Stepulak, S. Corvigno, J. Hartman, P. Micke, A. Mezheyeuski, C. Strell, J. W. Carlson, C. F. Moro, H. Dahlstrand, A. Östman, K. Matsumoto, P. Wiklund, M. Oya, A. Miyakawa, K. Deisseroth, and P. Uhlén, “Whole-tissue biopsy phenotyping of three-dimensional tumours reveals patterns of cancer heterogeneity,” Nat. Biomed. Eng. 1(10), 796–806 (2017).
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Supplementary Material (4)

NameDescription
» Visualization 1       Volumetric image corresponding to Fig. 3r.
» Visualization 2       Volumetric image corresponding to Fig. 3t.
» Visualization 3       Volumetric image corresponding to Fig. 6b.
» Visualization 4       Volumetric image corresponding to Fig. 6c.

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Figures (6)

Fig. 1
Fig. 1 Selective biopsy and imaging of a specimen with field cancerization.
Fig. 2
Fig. 2 Standard H&E histology of mammary tissue in a control rat and a carcinogen-induced rat. (a) H&E image of control mammary tissue reveals normal mammary ducts (cyan arrowhead) and alveoli (green arrowhead) lined with luminal epithelial cells. (b) H&E image of the same mammary tissue in a different field-of-view reveals a normal mammary duct filled with luminal epithelial cells (cyan arrowhead). (c) H&E image of the peri-tumoral field reveals a precancerous mammary duct (cyan arrowheads). (d) H&E image of the same tumor-adjacent mammary tissue in a different field-of-view reveals the coupling between a branched mammary duct and a blood vessel (green double-arrow). Scale bars: 100 µm.
Fig. 3
Fig. 3 Phenotypical changes of rat mammary and human breast cells in cyan- and magenta-colored field cancerization, respectively. (a) Rat primary tumor cells with cyan-colored nuclei. (b) Rat epithelial cells in a mammary alveolus with cyan-colored nuclei. (c) Rat epithelial cells in a mammary duct with cyan-colored nuclei. (d) Rat endothelial cells of developing blood vessels with elongated cyan-colored nuclei. (e) Similar rat cells that line developed blood vessels. (f) Rat stromal cells in remote peri-tumoral field. (g) Normal rat mammary duct (cross-sectional view) lacking visible epithelial cells. (h) Normal rat mammary duct (lateral view) lacking visible epithelial cells. (i) Developing rat neo-vasculature (broken line) lacking visible endothelial cells. (j) Developed rat blood vessel lacking visible endothelial cells. (k) Human stromal cells in remote peri-tumoral field. (l) Normal human mammary duct (cross-sectional view) with yellow-magenta-colored epithelial cells. (m) Normal human mammary duct (lateral view) with yellow-magenta-colored epithelial cells. (n) Developing human blood vessel lacking visible endothelial cells. (o) Developed human blood vessel lacking visible endothelial cells. (p) Human primary tumor cells with a magenta-colored cytoplasm. (q) Human epithelial cells in a tumor region with a magenta-colored cytoplasm. (r) Human epithelial cells in a mammary duct with a magenta-colored cytoplasm (Visualization 1). (s) Human endothelial cells of developing blood capillaries with a magenta-colored cell body. (t) Connection of a magenta-colored blood capillary (broken box) with a larger magenta-colored blood vessel (Visualization 2). Images (b), (c), and (d) are from different depths of one field-of-view. Scale bars: 50 µm.
Fig. 4
Fig. 4 Wide-field tetra-modal imaging of cyan-colored field cancerization in carcinogen-inject rats. Images (a), (b), and (c) reflect the vicinity of mammary tumor boundary, tumor center, and the remote peri-tumoral field of a tumor in one rat, respectively, while image (d) reflects the vicinity of the tumor boundary in another rat for direct comparison with (a). Epithelial cells (arrowheads), endothelial cells lining yellow-colored blood vessels (double arrows), and numerous stromal cells in the peri-tumoral field share the same optical phenotype of cyan-colored nuclei with the primary tumor cells (broken box 1), illuminating a cyan-colored field cancerization beyond the primary tumor(s). D­­­ashed boxes 1, 2, and 3 are also plotted in Figs. 3(a), 3(b)-3(d), and 3(e), respectively. Scale bars: 100 µm.
Fig. 5
Fig. 5 Wide-field tetra-modal imaging of magenta-colored field cancerization in a cancer patient (Subject #388). Images (a), (b), and (c-d) reflect the vicinity of breast tumor boundary, tumor center, and the remote peri-tumoral fields of a tumor, respectively. Epithelial cells (arrow) and endothelial cells lining blood vessels (arrowheads) share the same optical phenotype of magenta-colored cytoplasm (or cell body) with the primary tumor cells (broken box 3), illuminating a magenta-colored field cancerization beyond the primary tumor(s). Dashed boxes 1, 2, 3, and 4 are also plotted in Figs. 3(s), 3(q), 3(p), and 3(k), respectively. Scale bars: 100 µm.
Fig. 6
Fig. 6 Wide-field and selective volumetric tetra-modal imaging of rejuvenated magenta-colored field cancerization by chemotherapeutically eliminating multifocal primary tumors in a cancer patient (Subject #393). (a) Wide-field tetra-modal image of the peri-tumoral field with root-like mammary ducts, with two regions of interest subjective to selective volumetric tetra-modal imaging (broken boxes). (b) Selective volumetric tetra-modal images at three depths showing branched mammary tubulogenesis with luminal epithelial cells (arrowhead) and myoepithelial cells (arrow), which intertwines with developing capillaries surrounded by magenta-colored stromal cells (region of white broken curve) (Visualization 3). (c) Selective volumetric tetra-modal images at three depths showing blood vessel development of a capillary (arrowhead) and a connected sprouting vessel (region of white broken curve) (Visualization 4). (d) main branch of mammary ducts with peripheral magenta-colored stromal cells (arrows) different from yellow-colored stromal cells. Scale bars: 100 µm.

Tables (3)

Tables Icon

Table 1 Representative slide-free imaging modalities for histology

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Table 2 Classified vital cells in mammary tissue with distinct optical phenotypes.

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Table 3 Stratification of breast cancer patients by magenta-colored field cancerization.

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