Abstract

Open-top light-sheet microscopy is a technique that can potentially enable rapid ex vivo inspection of large tissue surfaces and volumes. Here, we have optimized an open-top light-sheet (OTLS) microscope and image-processing workflow for the comprehensive examination of surgical margin surfaces, and have also developed a novel fluorescent analog of H&E staining that is robust for staining fresh unfixed tissues. Our tissue-staining method can be achieved within 2.5 minutes followed by OTLS microscopy of lumpectomy surfaces at a rate of up to 1.5 cm2/minute. An image atlas is presented to show that OTLS image quality surpasses that of intraoperative frozen sectioning and can approximate that of gold-standard H&E histology of formalin-fixed paraffin-embedded (FFPE) tissues. Qualitative evidence indicates that these intraoperative methods do not interfere with downstream post-operative H&E histology and immunohistochemistry. These results should facilitate the translation of OTLS microscopy for intraoperative guidance of lumpectomy and other surgical oncology procedures.

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

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  83. Y. Chen, W. Xie, A.K. Glaser, N.P. Reder, C. Mao, S.M. Dintzis, J.C. Vaughan and J. T.C. Liu, ” OTLS microscopy image shearing code,” figshare (2019), https://doi.org/10.6084/m9.figshare.7571861.v4.
  84. F. Aguet, D. Van De Ville, and M. Unser, “Model-based 2.5-d deconvolution for extended depth of field in brightfield microscopy,” IEEE Trans. Image Process. 17(7), 1144–1153 (2008).
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  85. Y. Chen, W. Xie, A.K. Glaser, N.P. Reder, C. Mao, S.M. Dintzis, J.C. Vaughan and J. T.C. Liu, ” False-coloring code for OTLS microscopy, ” figshare (2019), https://doi.org/10.6084/m9.figshare.7575692.v2.
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2018 (4)

T. Yoshitake, M. G. Giacomelli, L. M. Quintana, H. Vardeh, L. C. Cahill, B. E. Faulkner-Jones, J. L. Connolly, D. Do, and J. G. Fujimoto, “Rapid histopathological imaging of skin and breast cancer surgical specimens using immersion microscopy with ultraviolet surface excitation,” Sci. Rep. 8(1), 4476 (2018).
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S. Kang, Y. W. Wang, X. Xu, E. Navarro, K. M. Tichauer, and J. T. C. Liu, “Microscopic investigation of" topically applied nanoparticles for molecular imaging of fresh tissue surfaces,” J. Biophotonics 11(4), e201700246 (2018).
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M. G. Giacomelli, T. Yoshitake, L. C. Cahill, H. Vardeh, L. M. Quintana, B. E. Faulkner-Jones, J. Brooker, J. L. Connolly, and J. G. Fujimoto, “Multiscale nonlinear microscopy and widefield white light imaging enables rapid histological imaging of surgical specimen margins,” Biomed. Opt. Express 9(5), 2457–2475 (2018).
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L. C. Cahill, M. G. Giacomelli, T. Yoshitake, H. Vardeh, B. E. Faulkner-Jones, J. L. Connolly, C.-K. Sun, and J. G. Fujimoto, “Rapid virtual hematoxylin and eosin histology of breast tissue specimens using a compact fluorescence nonlinear microscope,” Lab. Invest. 98(1), 150–160 (2018).
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2017 (8)

Y. W. Wang, N. P. Reder, S. Kang, A. K. Glaser, Q. Yang, M. A. Wall, S. H. Javid, S. M. Dintzis, and J. T. C. Liu, “Raman-Encoded Molecular Imaging with Topically Applied SERS Nanoparticles for Intraoperative Guidance of Lumpectomy,” Cancer Res. 77(16), 4506–4516 (2017).
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F. Fereidouni, Z. T. Harmany, M. Tian, A. Todd, J. A. Kintner, J. D. McPherson, A. D. Borowsky, M. Lechpammer, J. Bishop, 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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S. Abeytunge, B. Larson, G. Peterson, M. Morrow, M. Rajadhyaksha, and M. P. Murray, “Evaluation of breast tissue with confocal strip-mosaicking microscopy: a test approach emulating pathology-like examination,” J. Biomed. Opt. 22(3), 034002 (2017).
[Crossref] [PubMed]

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(7), 0084 (2017).
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R. M. Power and J. Huisken, “Intraoperative histology: Lightning 3D histopathology,” Nat. Biomed. Eng. 1(7), 0101 (2017).
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K. Coffey, D. D’Alessio, D. M. Keating, and E. A. Morris, “Second-Opinion Review of Breast Imaging at a Cancer Center: Is It Worthwhile?” AJR Am. J. Roentgenol. 208(6), 1386–1391 (2017).
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S. A. Boppart, J. Q. Brown, C. S. Farah, E. Kho, L. Marcu, C. M. Saunders, and H. J. C. M. Sterenborg, “Label-free optical imaging technologies for rapid translation and use during intraoperative surgical and tumor margin assessment,” J. Biomed. Opt. 23(2), 1–10 (2017).
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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(5), e1602168 (2017).
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2016 (9)

E. F. Brachtel, N. B. Johnson, A. E. Huck, T. L. Rice-Stitt, M. G. Vangel, B. L. Smith, G. J. Tearney, and D. Kang, “Spectrally Encoded Confocal Microscopy for Diagnosing Breast Cancer in Excision and Margin Specimens,” Lab. Invest. 96(4), 459–467 (2016).
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H. Tu, Y. Liu, D. Turchinovich, M. Marjanovic, J. Lyngsø, J. Lægsgaard, E. J. Chaney, Y. Zhao, S. You, W. L. Wilson, B. Xu, M. Dantus, and S. A. Boppart, “Stain-free histopathology by programmable supercontinuum pulses,” Nat. Photonics 10(8), 534–540 (2016).
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M. Wang, D. B. Tulman, A. B. Sholl, H. Z. Kimbrell, S. H. Mandava, K. N. Elfer, S. Luethy, M. M. Maddox, W. Lai, B. R. Lee, and J. Q. Brown, “Gigapixel surface imaging of radical prostatectomy specimens for comprehensive detection of cancer-positive surgical margins using structured illumination microscopy,” Sci. Rep. 6(1), 27419 (2016).
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K. N. Elfer, A. B. Sholl, M. Wang, D. B. Tulman, S. H. Mandava, B. R. Lee, and J. Q. Brown, “DRAQ5 and Eosin (‘D&E’) as an Analog to Hematoxylin and Eosin for Rapid Fluorescence Histology of Fresh Tissues,” PLoS One 11(10), e0165530 (2016).
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Y. Wang, S. Kang, J. D. Doerksen, A. K. Glaser, and J. T. C. Liu, “Surgical Guidance via Multiplexed Molecular Imaging of Fresh Tissues Labeled with SERS-Coded Nanoparticles,” IEEE J. Sel. Top. Quantum Electron. 22(4), 154–164 (2016).
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Y. W. Wang, J. D. Doerksen, S. Kang, D. Walsh, Q. Yang, D. Hong, and J. T. C. Liu, “Multiplexed Molecular Imaging of Fresh Tissue Surfaces Enabled by Convection-Enhanced Topical Staining with SERS-Coded Nanoparticles,” Small 12(40), 5612–5621 (2016).
[Crossref] [PubMed]

Y. Wang, S. Kang, A. Khan, G. Ruttner, S. Y. Leigh, M. Murray, S. Abeytunge, G. Peterson, M. Rajadhyaksha, S. Dintzis, S. Javid, and J. T. C. Liu, “Quantitative molecular phenotyping with topically applied SERS nanoparticles for intraoperative guidance of breast cancer lumpectomy,” Sci. Rep. 6(1), 21242 (2016).
[Crossref] [PubMed]

M. G. Giacomelli, L. Husvogt, H. Vardeh, B. E. Faulkner-Jones, J. Hornegger, J. L. Connolly, and J. G. Fujimoto, “Virtual Hematoxylin and Eosin Transillumination Microscopy Using Epi-Fluorescence Imaging,” PLoS One 11(8), e0159337 (2016).
[Crossref] [PubMed]

S. Petroni, L. Caldarola, R. Scamarcio, F. Giotta, A. Latorre, A. Mangia, and G. Simone, “FISH testing of HER2 immunohistochemistry 1+ invasive breast cancer with unfavorable characteristics,” Oncol. Lett. 12(5), 3115–3122 (2016).
[Crossref] [PubMed]

2015 (5)

M. Wang, H. Z. Kimbrell, A. B. Sholl, D. B. Tulman, K. N. Elfer, T. C. Schlichenmeyer, B. R. Lee, M. Lacey, and J. Q. Brown, “High-resolution rapid diagnostic imaging of whole prostate biopsies using video-rate fluorescence structured illumination microscopy,” Cancer Res. 75(19), 4032–4041 (2015).
[Crossref] [PubMed]

E. S. Flores, M. Cordova, K. Kose, W. Phillips, A. Rossi, K. Nehal, and M. Rajadhyaksha, “Intraoperative imaging during Mohs surgery with reflectance confocal microscopy: initial clinical experience,” J. Biomed. Opt. 20(6), 061103 (2015).
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R. McGorty, H. Liu, D. Kamiyama, Z. Dong, S. Guo, and B. Huang, “Open-top selective plane illumination microscope for conventionally mounted specimens,” Opt. Express 23(12), 16142–16153 (2015).
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T. Osako, R. Nishimura, Y. Nishiyama, Y. Okumura, R. Tashima, M. Nakano, M. Fujisue, Y. Toyozumi, and N. Arima, “Efficacy of intraoperative entire-circumferential frozen section analysis of lumpectomy margins during breast-conserving surgery for breast cancer,” Int. J. Clin. Oncol. 20(6), 1093–1101 (2015).
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M. Moschetta, M. Telegrafo, T. Introna, L. Coi, L. Rella, V. Ranieri, A. Cirili, A. A. Stabile Ianora, and G. Angelelli, “Role of specimen US for predicting resection margin status in breast conserving therapy,” G. Chir. 36(5), 201–204 (2015).
[PubMed]

2014 (6)

M. Thill, K. Baumann, and J. Barinoff, “Intraoperative assessment of margins in breast conservative surgery--still in use?” J. Surg. Oncol. 110(1), 15–20 (2014).
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T. C. Schlichenmeyer, M. Wang, K. N. Elfer, and J. Q. Brown, “Video-rate structured illumination microscopy for high-throughput imaging of large tissue areas,” Biomed. Opt. Express 5(2), 366–377 (2014).
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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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F. H. Barakat, I. Sulaiman, and M. A. Sughayer, “Reliability of frozen section in breast sentinel lymph node examination,” Breast Cancer 21(5), 576–582 (2014).
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C. DeSantis, J. Ma, L. Bryan, and A. Jemal, “Breast cancer statistics, 2013,” CA Cancer J. Clin. 64(1), 52–62 (2014).
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Y. W. Wang, A. Khan, M. Som, D. Wang, Y. Chen, S. Y. Leigh, D. Meza, P. Z. McVeigh, B. C. Wilson, and J. T. C. Liu, “Rapid ratiometric biomarker detection with topically applied SERS nanoparticles,” Technology (Singap World Sci) 2(2), 118–132 (2014).
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2013 (8)

N. Hou and D. Huo, “A trend analysis of breast cancer incidence rates in the United States from 2000 to 2009 shows a recent increase,” Breast Cancer Res. Treat. 138(2), 633–641 (2013).
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M. Ramos, J. C. Díaz, T. Ramos, R. Ruano, M. Aparicio, M. Sancho, and J. M. González-Orús, “Ultrasound-guided excision combined with intraoperative assessment of gross macroscopic margins decreases the rate of reoperations for non-palpable invasive breast cancer,” Breast 22(4), 520–524 (2013).
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H. Eggemann, T. Ignatov, A. Beni, S. D. Costa, O. Ortmann, and A. Ignatov, “Intraoperative Ultrasound in the Treatment of Breast Cancer,” Geburtshilfe Frauenheilkd. 73(10), 1028–1034 (2013).
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F. O. Fahrbach, F. F. Voigt, B. Schmid, F. Helmchen, and J. Huisken, “Rapid 3D light-sheet microscopy with a tunable lens,” Opt. Express 21(18), 21010–21026 (2013).
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F. O. Fahrbach, V. Gurchenkov, K. Alessandri, P. Nassoy, and A. Rohrbach, “Light-sheet microscopy in thick media using scanned Bessel beams and two-photon fluorescence excitation,” Opt. Express 21(11), 13824–13839 (2013).
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S. Abeytunge, Y. Li, B. Larson, G. Peterson, E. Seltzer, R. Toledo-Crow, and M. Rajadhyaksha, “Confocal microscopy with strip mosaicing for rapid imaging over large areas of excised tissue,” J. Biomed. Opt. 18(6), 061227 (2013).
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V. Venugopal, M. Park, Y. Ashitate, F. Neacsu, F. Kettenring, J. V. Frangioni, S. P. Gangadharan, and S. Gioux, “Design and characterization of an optimized simultaneous color and near-infrared fluorescence rigid endoscopic imaging system,” J. Biomed. Opt. 18(12), 126018 (2013).
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S. C. Davis, S. L. Gibbs, J. R. Gunn, and B. W. Pogue, “Topical dual-stain difference imaging for rapid intra-operative tumor identification in fresh specimens,” Opt. Lett. 38(23), 5184–5187 (2013).
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2012 (7)

A. M. Laughney, V. Krishnaswamy, E. J. Rizzo, M. C. Schwab, R. J. Barth, B. W. Pogue, K. D. Paulsen, and W. A. Wells, “Scatter spectroscopic imaging distinguishes between breast pathologies in tissues relevant to surgical margin assessment,” Clin. Cancer Res. 18(22), 6315–6325 (2012).
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J. Eschbacher, N. L. Martirosyan, P. Nakaji, N. Sanai, M. C. Preul, K. A. Smith, S. W. Coons, and R. F. Spetzler, “In vivo intraoperative confocal microscopy for real-time histopathological imaging of brain tumors,” J. Neurosurg. 116(4), 854–860 (2012).
[Crossref] [PubMed]

D. Wang, Y. Chen, S. Y. Leigh, H. Haeberle, C. H. Contag, and J. T. C. Liu, “Microscopic Delineation of Medulloblastoma Margins in a Transgenic Mouse Model Using a Topically Applied VEGFR-1 Probe,” Transl. Oncol. 5(6), 408–414 (2012).
[Crossref] [PubMed]

S. J. Schnitt and M. Morrow, “Should intraoperative frozen section evaluation of breast lumpectomy margins become routine practice?” Am. J. Clin. Pathol. 138(5), 635–638 (2012).
[Crossref] [PubMed]

J. M. Jorns, D. Visscher, M. Sabel, T. Breslin, P. Healy, S. Daignaut, J. L. Myers, and A. J. Wu, “Intraoperative frozen section analysis of margins in breast conserving surgery significantly decreases reoperative rates: one-year experience at an ambulatory surgical center,” Am. J. Clin. Pathol. 138(5), 657–669 (2012).
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T. M. Bydlon, W. T. Barry, S. A. Kennedy, J. Q. Brown, J. E. Gallagher, L. G. Wilke, J. Geradts, and N. Ramanujam, “Advancing optical imaging for breast margin assessment: an analysis of excisional time, cautery, and patent blue dye on underlying sources of contrast,” PLoS One 7(12), e51418 (2012).
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R. Jeevan, D. A. Cromwell, M. Trivella, G. Lawrence, O. Kearins, J. Pereira, C. Sheppard, C. M. Caddy, and J. H. van der Meulen, “Reoperation rates after breast conserving surgery for breast cancer among women in England: retrospective study of hospital episode statistics,” BMJ 345(jul12 2), e4505 (2012).
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2011 (4)

L. Huo, “A practical approach to grossing breast specimens,” Ann. Diagn. Pathol. 15(4), 291–301 (2011).
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V. Krishnaswamy, A. M. Laughney, K. D. Paulsen, and B. W. Pogue, “Dark-field scanning in situ spectroscopy platform for broadband imaging of resected tissue,” Opt. Lett. 36(10), 1911–1913 (2011).
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N. Sanai, L. A. Snyder, N. J. Honea, S. W. Coons, J. M. Eschbacher, K. A. Smith, and R. F. Spetzler, “Intraoperative confocal microscopy in the visualization of 5-aminolevulinic acid fluorescence in low-grade gliomas,” J. Neurosurg. 115(4), 740–748 (2011).
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S. Abeytunge, Y. Li, B. Larson, R. Toledo-Crow, and M. Rajadhyaksha, “Rapid confocal imaging of large areas of excised tissue with strip mosaicing,” J. Biomed. Opt. 16(5), 050504 (2011).
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2009 (5)

J. K. Karen, D. S. Gareau, S. W. Dusza, M. Tudisco, M. Rajadhyaksha, and K. S. Nehal, “Detection of basal cell carcinomas in Mohs excisions with fluorescence confocal mosaicing microscopy,” Br. J. Dermatol. 160(6), 1242–1250 (2009).
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J. Huisken and D. Y. R. Stainier, “Selective plane illumination microscopy techniques in developmental biology,” Development 136(12), 1963–1975 (2009).
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R. G. Pleijhuis, M. Graafland, J. de Vries, J. Bart, J. S. de Jong, and G. M. van Dam, “Obtaining adequate surgical margins in breast-conserving therapy for patients with early-stage breast cancer: current modalities and future directions,” Ann. Surg. Oncol. 16(10), 2717–2730 (2009).
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F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
[Crossref] [PubMed]

S. Preibisch, S. Saalfeld, and P. Tomancak, “Globally optimal stitching of tiled 3D microscopic image acquisitions,” Bioinformatics 25(11), 1463–1465 (2009).
[Crossref] [PubMed]

2008 (4)

F. Aguet, D. Van De Ville, and M. Unser, “Model-based 2.5-d deconvolution for extended depth of field in brightfield microscopy,” IEEE Trans. Image Process. 17(7), 1144–1153 (2008).
[Crossref] [PubMed]

W. P. Weber, S. Engelberger, C. T. Viehl, R. Zanetti-Dallenbach, S. Kuster, S. Dirnhofer, D. Wruk, D. Oertli, and W. R. Marti, “Accuracy of frozen section analysis versus specimen radiography during breast-conserving surgery for nonpalpable lesions,” World J. Surg. 32(12), 2599–2606 (2008).
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L. Jacobs, “Positive margins: the challenge continues for breast surgeons,” Ann. Surg. Oncol. 15(5), 1271–1272 (2008).
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J. F. Waljee, E. S. Hu, L. A. Newman, and A. K. Alderman, “Predictors of re-excision among women undergoing breast-conserving surgery for cancer,” Ann. Surg. Oncol. 15(5), 1297–1303 (2008).
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2007 (5)

N. Cabioglu, K. K. Hunt, A. A. Sahin, H. M. Kuerer, G. V. Babiera, S. E. Singletary, G. J. Whitman, M. I. Ross, F. C. Ames, B. W. Feig, T. A. Buchholz, and F. Meric-Bernstam, “Role for intraoperative margin assessment in patients undergoing breast-conserving surgery,” Ann. Surg. Oncol. 14(4), 1458–1471 (2007).
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E. K. Valdes, S. K. Boolbol, J. M. Cohen, and S. M. Feldman, “Intra-operative touch preparation cytology; does it have a role in re-excision lumpectomy?” Ann. Surg. Oncol. 14(3), 1045–1050 (2007).
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C. J. Engelbrecht, K. Greger, E. G. Reynaud, U. Kržic, J. Colombelli, and E. H. K. Stelzer, “Three-dimensional laser microsurgery in light-sheet based microscopy (SPIM),” Opt. Express 15(10), 6420–6430 (2007).
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K. Greger, J. Swoger, and E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Rev. Sci. Instrum. 78(2), 023705 (2007).
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J. Huisken and D. Y. R. Stainier, “Even fluorescence excitation by multidirectional selective plane illumination microscopy (mSPIM),” Opt. Lett. 32(17), 2608–2610 (2007).
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2006 (1)

J. T. C. Liu, M. J. Mandella, S. Friedland, R. Soetikno, J. M. Crawford, C. H. Contag, G. S. Kino, and T. D. Wang, “Dual-axes confocal reflectance microscope for distinguishing colonic neoplasia,” J. Biomed. Opt. 11(5), 054019 (2006).
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2005 (4)

H. Inoue, S. E. Kudo, and A. Shiokawa, “Technology insight: Laser-scanning confocal microscopy and endocytoscopy for cellular observation of the gastrointestinal tract,” Nat. Clin. Pract. Gastroenterol. Hepatol. 2(1), 31–37 (2005).
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J. Skoch, A. Dunn, B. T. Hyman, and B. J. Bacskai, “Development of an optical approach for noninvasive imaging of Alzheimer’s disease pathology,” J. Biomed. Opt. 10(1), 011007 (2005).
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J. C. Cendán, D. Coco, and E. M. Copeland, “Accuracy of intraoperative frozen-section analysis of breast cancer lumpectomy-bed margins,” J. Am. Coll. Surg. 201(2), 194–198 (2005).
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K. C. Horst, M. C. Smitt, D. R. Goffinet, and R. W. Carlson, “Predictors of local recurrence after breast-conservation therapy,” Clin. Breast Cancer 5(6), 425–438 (2005).
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2004 (2)

E. Weinberg, C. Cox, E. Dupont, L. White, M. Ebert, H. Greenberg, N. Diaz, V. Vercel, B. Centeno, A. Cantor, and S. Nicosia, “Local recurrence in lumpectomy patients after imprint cytology margin evaluation,” Am. J. Surg. 188(4), 349–354 (2004).
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J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical Sectioning Deep Inside Live embryos by Selective Plane Illumination Microscopy,” Science 305(5686), 1007–1009 (2004).
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2002 (2)

B. Fisher, S. Anderson, J. Bryant, R. G. Margolese, M. Deutsch, E. R. Fisher, J. H. Jeong, and N. Wolmark, “Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer,” N. Engl. J. Med. 347(16), 1233–1241 (2002).
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A. J. Creager, J. A. Shaw, P. R. Young, and K. R. Geisinger, “Intraoperative Evaluation of Lumpectomy Margins by Imprint Cytology With Histologic Correlation: a Community Hospital Experience,” Arch. Pathol. Lab. Med. 126(7), 846–848 (2002).
[PubMed]

1999 (2)

R. S. Tuma, M. P. Beaudet, X. Jin, L. J. Jones, C. Y. Cheung, S. Yue, and V. L. Singer, “Characterization of SYBR Gold nucleic acid gel stain: a dye optimized for use with 300-nm ultraviolet transilluminators,” Anal. Biochem. 268(2), 278–288 (1999).
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T. W. Jacobs, A. M. Gown, H. Yaziji, M. J. Barnes, and S. J. Schnitt, “Comparison of fluorescence in situ hybridization and immunohistochemistry for the evaluation of HER-2/neu in breast cancer,” J. Clin. Oncol. 17(7), 1974–1982 (1999).
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1997 (1)

A. J. Guidi, J. L. Connolly, J. R. Harris, and S. J. Schnitt, “The relationship between shaved margin and inked margin status in breast excision specimens,” Cancer 79(8), 1568–1573 (1997).
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1996 (1)

I. Gage, S. J. Schnitt, A. J. Nixon, B. Silver, A. Recht, S. L. Troyan, T. Eberlein, S. M. Love, R. Gelman, J. R. Harris, and J. L. Connolly, “Pathologic margin involvement and the risk of recurrence in patients treated with breast-conserving therapy,” Cancer 78(9), 1921–1928 (1996).
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1995 (1)

J. A. Jacobson, D. N. Danforth, K. H. Cowan, T. d’Angelo, S. M. Steinberg, L. Pierce, M. E. Lippman, A. S. Lichter, E. Glatstein, and P. Okunieff, “Ten-year results of a comparison of conservation with mastectomy in the treatment of stage I and II breast cancer,” N. Engl. J. Med. 332(14), 907–911 (1995).
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1994 (1)

R. A. Graham, M. J. Homer, C. J. Sigler, H. Safaii, C. H. Schmid, D. J. Marchant, and T. J. Smith, “The efficacy of specimen radiography in evaluating the surgical margins of impalpable breast carcinoma,” AJR Am. J. Roentgenol. 162(1), 33–36 (1994).
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1991 (1)

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Y. Wang, S. Kang, A. Khan, G. Ruttner, S. Y. Leigh, M. Murray, S. Abeytunge, G. Peterson, M. Rajadhyaksha, S. Dintzis, S. Javid, and J. T. C. Liu, “Quantitative molecular phenotyping with topically applied SERS nanoparticles for intraoperative guidance of breast cancer lumpectomy,” Sci. Rep. 6(1), 21242 (2016).
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S. Abeytunge, Y. Li, B. Larson, G. Peterson, E. Seltzer, R. Toledo-Crow, and M. Rajadhyaksha, “Confocal microscopy with strip mosaicing for rapid imaging over large areas of excised tissue,” J. Biomed. Opt. 18(6), 061227 (2013).
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S. Abeytunge, Y. Li, B. Larson, R. Toledo-Crow, and M. Rajadhyaksha, “Rapid confocal imaging of large areas of excised tissue with strip mosaicing,” J. Biomed. Opt. 16(5), 050504 (2011).
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F. Aguet, D. Van De Ville, and M. Unser, “Model-based 2.5-d deconvolution for extended depth of field in brightfield microscopy,” IEEE Trans. Image Process. 17(7), 1144–1153 (2008).
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J. F. Waljee, E. S. Hu, L. A. Newman, and A. K. Alderman, “Predictors of re-excision among women undergoing breast-conserving surgery for cancer,” Ann. Surg. Oncol. 15(5), 1297–1303 (2008).
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M. Moschetta, M. Telegrafo, T. Introna, L. Coi, L. Rella, V. Ranieri, A. Cirili, A. A. Stabile Ianora, and G. Angelelli, “Role of specimen US for predicting resection margin status in breast conserving therapy,” G. Chir. 36(5), 201–204 (2015).
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R. G. Pleijhuis, M. Graafland, J. de Vries, J. Bart, J. S. de Jong, and G. M. van Dam, “Obtaining adequate surgical margins in breast-conserving therapy for patients with early-stage breast cancer: current modalities and future directions,” Ann. Surg. Oncol. 16(10), 2717–2730 (2009).
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M. Thill, K. Baumann, and J. Barinoff, “Intraoperative assessment of margins in breast conservative surgery--still in use?” J. Surg. Oncol. 110(1), 15–20 (2014).
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R. S. Tuma, M. P. Beaudet, X. Jin, L. J. Jones, C. Y. Cheung, S. Yue, and V. L. Singer, “Characterization of SYBR Gold nucleic acid gel stain: a dye optimized for use with 300-nm ultraviolet transilluminators,” Anal. Biochem. 268(2), 278–288 (1999).
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Bellafiore, F. J.

F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
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H. Eggemann, T. Ignatov, A. Beni, S. D. Costa, O. Ortmann, and A. Ignatov, “Intraoperative Ultrasound in the Treatment of Breast Cancer,” Geburtshilfe Frauenheilkd. 73(10), 1028–1034 (2013).
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F. Fereidouni, Z. T. Harmany, M. Tian, A. Todd, J. A. Kintner, J. D. McPherson, A. D. Borowsky, M. Lechpammer, J. Bishop, 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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Boolbol, S. K.

E. K. Valdes, S. K. Boolbol, J. M. Cohen, and S. M. Feldman, “Intra-operative touch preparation cytology; does it have a role in re-excision lumpectomy?” Ann. Surg. Oncol. 14(3), 1045–1050 (2007).
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Boppart, S. A.

S. A. Boppart, J. Q. Brown, C. S. Farah, E. Kho, L. Marcu, C. M. Saunders, and H. J. C. M. Sterenborg, “Label-free optical imaging technologies for rapid translation and use during intraoperative surgical and tumor margin assessment,” J. Biomed. Opt. 23(2), 1–10 (2017).
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H. Tu, Y. Liu, D. Turchinovich, M. Marjanovic, J. Lyngsø, J. Lægsgaard, E. J. Chaney, Y. Zhao, S. You, W. L. Wilson, B. Xu, M. Dantus, and S. A. Boppart, “Stain-free histopathology by programmable supercontinuum pulses,” Nat. Photonics 10(8), 534–540 (2016).
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F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
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F. Fereidouni, Z. T. Harmany, M. Tian, A. Todd, J. A. Kintner, J. D. McPherson, A. D. Borowsky, M. Lechpammer, J. Bishop, 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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Brachtel, E. F.

E. F. Brachtel, N. B. Johnson, A. E. Huck, T. L. Rice-Stitt, M. G. Vangel, B. L. Smith, G. J. Tearney, and D. Kang, “Spectrally Encoded Confocal Microscopy for Diagnosing Breast Cancer in Excision and Margin Specimens,” Lab. Invest. 96(4), 459–467 (2016).
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Breslin, T.

J. M. Jorns, D. Visscher, M. Sabel, T. Breslin, P. Healy, S. Daignaut, J. L. Myers, and A. J. Wu, “Intraoperative frozen section analysis of margins in breast conserving surgery significantly decreases reoperative rates: one-year experience at an ambulatory surgical center,” Am. J. Clin. Pathol. 138(5), 657–669 (2012).
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Brooker, J.

Brooker, J. S.

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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Brown, J. Q.

S. A. Boppart, J. Q. Brown, C. S. Farah, E. Kho, L. Marcu, C. M. Saunders, and H. J. C. M. Sterenborg, “Label-free optical imaging technologies for rapid translation and use during intraoperative surgical and tumor margin assessment,” J. Biomed. Opt. 23(2), 1–10 (2017).
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K. N. Elfer, A. B. Sholl, M. Wang, D. B. Tulman, S. H. Mandava, B. R. Lee, and J. Q. Brown, “DRAQ5 and Eosin (‘D&E’) as an Analog to Hematoxylin and Eosin for Rapid Fluorescence Histology of Fresh Tissues,” PLoS One 11(10), e0165530 (2016).
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M. Wang, H. Z. Kimbrell, A. B. Sholl, D. B. Tulman, K. N. Elfer, T. C. Schlichenmeyer, B. R. Lee, M. Lacey, and J. Q. Brown, “High-resolution rapid diagnostic imaging of whole prostate biopsies using video-rate fluorescence structured illumination microscopy,” Cancer Res. 75(19), 4032–4041 (2015).
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T. C. Schlichenmeyer, M. Wang, K. N. Elfer, and J. Q. Brown, “Video-rate structured illumination microscopy for high-throughput imaging of large tissue areas,” Biomed. Opt. Express 5(2), 366–377 (2014).
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T. M. Bydlon, W. T. Barry, S. A. Kennedy, J. Q. Brown, J. E. Gallagher, L. G. Wilke, J. Geradts, and N. Ramanujam, “Advancing optical imaging for breast margin assessment: an analysis of excisional time, cautery, and patent blue dye on underlying sources of contrast,” PLoS One 7(12), e51418 (2012).
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Bryant, J.

B. Fisher, S. Anderson, J. Bryant, R. G. Margolese, M. Deutsch, E. R. Fisher, J. H. Jeong, and N. Wolmark, “Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer,” N. Engl. J. Med. 347(16), 1233–1241 (2002).
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Buchholz, T. A.

N. Cabioglu, K. K. Hunt, A. A. Sahin, H. M. Kuerer, G. V. Babiera, S. E. Singletary, G. J. Whitman, M. I. Ross, F. C. Ames, B. W. Feig, T. A. Buchholz, and F. Meric-Bernstam, “Role for intraoperative margin assessment in patients undergoing breast-conserving surgery,” Ann. Surg. Oncol. 14(4), 1458–1471 (2007).
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Bydlon, T. M.

T. M. Bydlon, W. T. Barry, S. A. Kennedy, J. Q. Brown, J. E. Gallagher, L. G. Wilke, J. Geradts, and N. Ramanujam, “Advancing optical imaging for breast margin assessment: an analysis of excisional time, cautery, and patent blue dye on underlying sources of contrast,” PLoS One 7(12), e51418 (2012).
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Cabioglu, N.

N. Cabioglu, K. K. Hunt, A. A. Sahin, H. M. Kuerer, G. V. Babiera, S. E. Singletary, G. J. Whitman, M. I. Ross, F. C. Ames, B. W. Feig, T. A. Buchholz, and F. Meric-Bernstam, “Role for intraoperative margin assessment in patients undergoing breast-conserving surgery,” Ann. Surg. Oncol. 14(4), 1458–1471 (2007).
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Cable, A. E.

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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R. Jeevan, D. A. Cromwell, M. Trivella, G. Lawrence, O. Kearins, J. Pereira, C. Sheppard, C. M. Caddy, and J. H. van der Meulen, “Reoperation rates after breast conserving surgery for breast cancer among women in England: retrospective study of hospital episode statistics,” BMJ 345(jul12 2), e4505 (2012).
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Cahill, L. C.

T. Yoshitake, M. G. Giacomelli, L. M. Quintana, H. Vardeh, L. C. Cahill, B. E. Faulkner-Jones, J. L. Connolly, D. Do, and J. G. Fujimoto, “Rapid histopathological imaging of skin and breast cancer surgical specimens using immersion microscopy with ultraviolet surface excitation,” Sci. Rep. 8(1), 4476 (2018).
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L. C. Cahill, M. G. Giacomelli, T. Yoshitake, H. Vardeh, B. E. Faulkner-Jones, J. L. Connolly, C.-K. Sun, and J. G. Fujimoto, “Rapid virtual hematoxylin and eosin histology of breast tissue specimens using a compact fluorescence nonlinear microscope,” Lab. Invest. 98(1), 150–160 (2018).
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M. G. Giacomelli, T. Yoshitake, L. C. Cahill, H. Vardeh, L. M. Quintana, B. E. Faulkner-Jones, J. Brooker, J. L. Connolly, and J. G. Fujimoto, “Multiscale nonlinear microscopy and widefield white light imaging enables rapid histological imaging of surgical specimen margins,” Biomed. Opt. Express 9(5), 2457–2475 (2018).
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Caldarola, L.

S. Petroni, L. Caldarola, R. Scamarcio, F. Giotta, A. Latorre, A. Mangia, and G. Simone, “FISH testing of HER2 immunohistochemistry 1+ invasive breast cancer with unfavorable characteristics,” Oncol. Lett. 12(5), 3115–3122 (2016).
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Cantor, A.

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J. C. Cendán, D. Coco, and E. M. Copeland, “Accuracy of intraoperative frozen-section analysis of breast cancer lumpectomy-bed margins,” J. Am. Coll. Surg. 201(2), 194–198 (2005).
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Centeno, B.

E. Weinberg, C. Cox, E. Dupont, L. White, M. Ebert, H. Greenberg, N. Diaz, V. Vercel, B. Centeno, A. Cantor, and S. Nicosia, “Local recurrence in lumpectomy patients after imprint cytology margin evaluation,” Am. J. Surg. 188(4), 349–354 (2004).
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Chaney, E. J.

H. Tu, Y. Liu, D. Turchinovich, M. Marjanovic, J. Lyngsø, J. Lægsgaard, E. J. Chaney, Y. Zhao, S. You, W. L. Wilson, B. Xu, M. Dantus, and S. A. Boppart, “Stain-free histopathology by programmable supercontinuum pulses,” Nat. Photonics 10(8), 534–540 (2016).
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F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
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Chen, Y.

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(7), 0084 (2017).
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Cirili, A.

M. Moschetta, M. Telegrafo, T. Introna, L. Coi, L. Rella, V. Ranieri, A. Cirili, A. A. Stabile Ianora, and G. Angelelli, “Role of specimen US for predicting resection margin status in breast conserving therapy,” G. Chir. 36(5), 201–204 (2015).
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Coco, D.

J. C. Cendán, D. Coco, and E. M. Copeland, “Accuracy of intraoperative frozen-section analysis of breast cancer lumpectomy-bed margins,” J. Am. Coll. Surg. 201(2), 194–198 (2005).
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E. K. Valdes, S. K. Boolbol, J. M. Cohen, and S. M. Feldman, “Intra-operative touch preparation cytology; does it have a role in re-excision lumpectomy?” Ann. Surg. Oncol. 14(3), 1045–1050 (2007).
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M. Moschetta, M. Telegrafo, T. Introna, L. Coi, L. Rella, V. Ranieri, A. Cirili, A. A. Stabile Ianora, and G. Angelelli, “Role of specimen US for predicting resection margin status in breast conserving therapy,” G. Chir. 36(5), 201–204 (2015).
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Connolly, J. L.

M. G. Giacomelli, T. Yoshitake, L. C. Cahill, H. Vardeh, L. M. Quintana, B. E. Faulkner-Jones, J. Brooker, J. L. Connolly, and J. G. Fujimoto, “Multiscale nonlinear microscopy and widefield white light imaging enables rapid histological imaging of surgical specimen margins,” Biomed. Opt. Express 9(5), 2457–2475 (2018).
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L. C. Cahill, M. G. Giacomelli, T. Yoshitake, H. Vardeh, B. E. Faulkner-Jones, J. L. Connolly, C.-K. Sun, and J. G. Fujimoto, “Rapid virtual hematoxylin and eosin histology of breast tissue specimens using a compact fluorescence nonlinear microscope,” Lab. Invest. 98(1), 150–160 (2018).
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T. Yoshitake, M. G. Giacomelli, L. M. Quintana, H. Vardeh, L. C. Cahill, B. E. Faulkner-Jones, J. L. Connolly, D. Do, and J. G. Fujimoto, “Rapid histopathological imaging of skin and breast cancer surgical specimens using immersion microscopy with ultraviolet surface excitation,” Sci. Rep. 8(1), 4476 (2018).
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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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Figures (7)

Fig. 1
Fig. 1 Schematic of an open-top light-sheet (OTLS) microscope. The OTLS microscope utilizes a solid immersion lens (SIL) and thin oil film to provide wavefront- and index-matching of the illumination and collection beam paths into tissue at a 45-deg angle of incidence. This unique open-top configuration (inset) is versatile for imaging diverse clinical specimens with minimal constraints on size and geometry. The 0.03 illumination NA provides an extended depth of focus (~400 µm) to accommodate for tissue-surface irregularities, specimen tilt, and tissue debris.
Fig. 2
Fig. 2 Study design. Freshly excised human breast tissues were inked and bisected immediately after lumpectomy procedures. The bisected surface from one half of the specimen (control specimen) was processed for routine histology (H&E and IHC). The bisected surface from the other half (experimental specimen) was stained and imaged with OTLS microscopy (< 30 minutes), before being processed for routine histology. OTLS surface images were compared to archival H&E histology. In addition, histology images from the experimental and control specimens were compared to show that our tissue-staining and imaging techniques do not interfere with downstream H&E histology and IHC.
Fig. 3
Fig. 3 Image acquisition and processing of OTLS microscopy. (a) The dual-channel (nuclear and cytoplasmic channel) OTLS images occupy a combined height (h) of 128 vertical camera pixels (64 pixels per channel, or ~80 µm in tissues). The image height, h = 128 pixels, was selected to optimize the imaging speed while accommodating for surface irregularities, specimen tilt, and tissue debris. (b) Oblique (45-deg) light-sheet images are captured in succession at a sampling pitch of 1.25 μm along the primary tissue-scanning direction, x. The horizontal dimension of each image strip is w = 1.25 mm. (c) The raw light-sheet images are initially stored in a rectangular data cube. During post-processing, this data cube is sheared by 45 deg in the x-z plane to transform the data cube into a trapezoidal data volume, which accurately represents the geometry of the imaged tissue volume. (d) An extended-depth-of-field (EDF) algorithm [84] is applied to extract the irregular surface of the specimen. The two-channel surface-extracted image is then false-colored to resemble H&E histology using an algorithm modified from a recent publication [86]. (e) After false-color processing, adjacent image strips are registered and stitched using an ImageJ grid-stitching algorithm [87].
Fig. 4
Fig. 4 A comparison of the image quality between OTLS microscopy of eosin-stained (a) and ATTO 655 NHS-ester-stained (b) fresh breast tissue surfaces. When staining fresh specimens, eosin is not stably bound within the tissue and leaks out of the tissue during imaging (purple arrow), which generates a high background that deteriorates the image contrast. The image panels in (c) and (d) provide image quality comparisons between frozen-section histology with eosin staining, archival FFPE histology with eosin staining, OTLS microscopy with eosin staining, and OTLS microscopy with ATTO 655 NHS-ester staining. Results show that the ATTO 655 NHS ester provides improved contrast for visualizing tissue structures, such as collagen fibers, in comparison to eosin in fresh unfixed tissues. Adipocytes and strands of fibrous tissue with stromal cells remained intact after OTLS microscopy and slide-based “H&E” histology. However, the same tissue structures are heavily distorted in frozen-section “H&E” histology ((d), yellow arrow).
Fig. 5
Fig. 5 A fresh breast specimen (1 cm by 1cm by 0.5 cm, (a)) was first stained with SYBR Gold and ATTO 655 NHS ester followed by surface imaging with an OTLS microscope, (b). After OTLS microscopy, the same piece of tissue was submitted for archival FFPE histology (H&E), (c). Panels (d), (e) and (f) show benign breast lobules (red arrow), a duct (purple arrow) and a blood vessel within the adipose tissue (green arrow) that were identified from the OTLS surface image, respectively. The corresponding gold-standard H&E images displaying the same tissue features demonstrate that OTLS microscopy with the SYBR Gold and ATTO 655 NHS ester tissue-staining method can enable rapid and high-quality pathology (1.5 cm2/minute) of a large surgical specimen surface.
Fig. 6
Fig. 6 Various microarchitectural features were identified from the OTLS images, including (a) a benign breast lobule where the inset shows individual acini with identifiable lumens, (b) invasive ductal carcinoma (IDC) with Nottingham grade I and (c) IDC with Nottingham grade II, d) ductal carcinoma in situ with comedonecrosis.
Fig. 7
Fig. 7 (a) H&E histology and (b) IHC results (ER, PR, and HER2 expression) from different control specimens (untouched by OTLS microscopy methods) as compared to those from OTLS microscopy-processed counterparts, showing that the OTLS methods do not interfere with downstream post-operative H&E histology and IHC analysis.

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