Abstract

The ability to histologically assess surgical specimens in real-time is a long-standing challenge in cancer surgery, including applications such as breast conserving therapy (BCT). Up to 40% of women treated with BCT for breast cancer require a repeat surgery due to postoperative histological findings of close or positive surgical margins using conventional formalin fixed paraffin embedded histology. Imaging technologies such as nonlinear microscopy (NLM), combined with exogenous fluorophores can rapidly provide virtual H&E imaging of surgical specimens without requiring microtome sectioning, facilitating intraoperative assessment of margin status. However, the large volume of typical surgical excisions combined with the need for rapid assessment, make comprehensive cellular resolution margin assessment during surgery challenging. To address this limitation, we developed a multiscale, real-time microscope with variable magnification NLM and real-time, co-registered position display using a widefield white light imaging system. Margin assessment can be performed rapidly under operator guidance to image specific regions of interest located using widefield imaging. Using simulated surgical margins dissected from human breast excisions, we demonstrate that multi-centimeter margins can be comprehensively imaged at cellular resolution, enabling intraoperative margin assessment. These methods are consistent with pathology assessment performed using frozen section analysis (FSA), however NLM enables faster and more comprehensive assessment of surgical specimens because imaging can be performed without freezing and cryo-sectioning. Therefore, NLM methods have the potential to be applied to a wide range of intra-operative applications.

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

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2018 (3)

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).
[Crossref] [PubMed]

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).
[PubMed]

A. J. Guidi, J. A. Tworek, D. D. Mais, R. J. Souers, B. J. Blond, and R. W. Brown, “Breast Specimen Processing and Reporting With an Emphasis on Margin Evaluation,” Arch. Pathol. Lab Med.  142(4), 496–506 (2018).

2017 (6)

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), 34002 (2017).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

B. S. Nichols, A. Llopis, G. M. Palmer, S. S. McCachren, O. Senlik, D. Miller, M. A. Brooke, N. M. Jokerst, J. Geradts, R. Greenup, and N. Ramanujam, “Miniature spectral imaging device for wide-field quantitative functional imaging of the morphological landscape of breast tumor margins,” J. Biomed. Opt. 22(2), 026007 (2017).
[Crossref] [PubMed]

G. Thomas, T.-Q. Nguyen, I. J. Pence, B. Caldwell, M. E. O’Connor, J. Giltnane, M. E. Sanders, A. Grau, I. Meszoely, M. Hooks, M. C. Kelley, and A. Mahadevan-Jansen, “Evaluating feasibility of an automated 3-dimensional scanner using Raman spectroscopy for intraoperative breast margin assessment,” Sci. Rep. 7(1), 13548 (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,” Nature Biomedical Engineering 1(7), 84 (2017).
[Crossref]

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, 957–966 (2017).

2016 (8)

T. Yoshitake, M. G. Giacomelli, L. C. Cahill, D. B. Schmolze, H. Vardeh, B. E. Faulkner-Jones, J. L. Connolly, and J. G. Fujimoto, “Direct comparison between confocal and multiphoton microscopy for rapid histopathological evaluation of unfixed human breast tissue,” J. Biomed. Opt. 21(12), 126021 (2016).
[Crossref] [PubMed]

J. L. Mueller, J. E. Gallagher, R. Chitalia, M. Krieger, A. Erkanli, R. M. Willett, J. Geradts, and N. Ramanujam, “Rapid staining and imaging of subnuclear features to differentiate between malignant and benign breast tissues at a point-of-care setting,” J. Cancer Res. Clin. Oncol. 142(7), 1475–1486 (2016).
[Crossref] [PubMed]

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).
[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]

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).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

F. K. Lu, D. Calligaris, O. I. Olubiyi, I. Norton, W. Yang, S. Santagata, X. S. Xie, A. J. Golby, and N. Y. R. Agar, “Label-free neurosurgical pathology with stimulated Raman imaging,” Cancer Res. 76(12), 3451–3462 (2016).
[Crossref] [PubMed]

M. Morrow, K. J. Van Zee, L. J. Solin, N. Houssami, M. Chavez-MacGregor, J. R. Harris, J. Horton, S. Hwang, P. L. Johnson, M. L. Marinovich, S. J. Schnitt, I. Wapnir, and M. S. Moran, “Society of Surgical Oncology-American Society for Radiation Oncology-American Society of Clinical Oncology Consensus Guideline on Margins for Breast-Conserving Surgery With Whole-Breast Irradiation in Ductal Carcinoma in Situ,” Pract. Radiat. Oncol. 6(5), 287–295 (2016).
[Crossref] [PubMed]

2015 (4)

C. Longo, M. Ragazzi, S. Gardini, S. Piana, E. Moscarella, A. Lallas, M. Raucci, G. Argenziano, and G. Pellacani, “Ex vivo fluorescence confocal microscopy in conjunction with Mohs micrographic surgery for cutaneous squamous cell carcinoma,” J. Am. Acad. Dermatol. 73(2), 321–322 (2015).
[Crossref] [PubMed]

J. Dobbs, S. Krishnamurthy, M. Kyrish, A. P. Benveniste, W. Yang, and R. Richards-Kortum, “Confocal fluorescence microscopy for rapid evaluation of invasive tumor cellularity of inflammatory breast carcinoma core needle biopsies,” Breast Cancer Res. Treat. 149(1), 303–310 (2015).
[Crossref] [PubMed]

A. M. Zysk, K. Chen, E. Gabrielson, L. Tafra, E. A. May Gonzalez, J. K. Canner, E. B. Schneider, A. J. Cittadine, P. Scott Carney, S. A. Boppart, K. Tsuchiya, K. Sawyer, and L. K. Jacobs, “Intraoperative Assessment of Final Margins with a Handheld Optical Imaging Probe During Breast-Conserving Surgery May Reduce the Reoperation Rate: Results of a Multicenter Study,” Ann. Surg. Oncol. 22(10), 3356–3362 (2015).
[Crossref] [PubMed]

M. G. Giacomelli, Y. Sheikine, H. Vardeh, J. L. Connolly, and J. G. Fujimoto, “Rapid imaging of surgical breast excisions using direct temporal sampling two photon fluorescent lifetime imaging,” Biomed. Opt. Express 6(11), 4317–4325 (2015).
[Crossref] [PubMed]

2014 (4)

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(5), 455–468 (2014).
[PubMed]

M. S. Moran, S. J. Schnitt, A. E. Giuliano, J. R. Harris, S. A. Khan, J. Horton, S. Klimberg, M. Chavez-MacGregor, G. Freedman, N. Houssami, P. L. Johnson, M. Morrow, Society of Surgical OncologyAmerican Society for Radiation Oncology, “Society of Surgical Oncology-American Society for Radiation Oncology consensus guideline on margins for breast-conserving surgery with whole-breast irradiation in stages I and II invasive breast cancer,” J. Clin. Oncol. 32(14), 1507–1515 (2014).
[Crossref] [PubMed]

M. J. Baker, J. Trevisan, P. Bassan, R. Bhargava, H. J. Butler, K. M. Dorling, P. R. Fielden, S. W. Fogarty, N. J. Fullwood, K. A. Heys, C. Hughes, P. Lasch, P. L. Martin-Hirsch, B. Obinaju, G. D. Sockalingum, J. Sulé-Suso, R. J. Strong, M. J. Walsh, B. R. Wood, P. Gardner, and F. L. Martin, “Using Fourier transform IR spectroscopy to analyze biological materials,” Nat. Protoc. 9(8), 1771–1791 (2014).
[Crossref] [PubMed]

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]

2013 (1)

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).
[Crossref] [PubMed]

2012 (3)

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).
[Crossref] [PubMed]

T. Schlomm, P. Tennstedt, C. Huxhold, T. Steuber, G. Salomon, U. Michl, H. Heinzer, J. Hansen, L. Budäus, S. Steurer, C. Wittmer, S. Minner, A. Haese, G. Sauter, M. Graefen, and H. Huland, “Neurovascular structure-adjacent frozen-section examination (NeuroSAFE) increases nerve-sparing frequency and reduces positive surgical margins in open and robot-assisted laparoscopic radical prostatectomy: experience after 11,069 consecutive patients,” Eur. Urol. 62(2), 333–340 (2012).
[Crossref] [PubMed]

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. French, A. Chu, G. W. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS One 7(9), e43460 (2012).
[Crossref] [PubMed]

2011 (1)

D. M. Layfield, A. Agrawal, H. Roche, and R. I. Cutress, “Intraoperative assessment of sentinel lymph nodes in breast cancer,” Br. J. Surg. 98(1), 4–17 (2011).
[Crossref] [PubMed]

2010 (2)

S. Alkhateeb, S. Alibhai, N. Fleshner, A. Finelli, M. Jewett, A. Zlotta, M. Nesbitt, G. Lockwood, and J. Trachtenberg, “Impact of positive surgical margins after radical prostatectomy differs by disease risk group,” J. Urol. 183(1), 145–150 (2010).
[Crossref] [PubMed]

C. Zhou, D. W. D. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated optical coherence tomography and microscopy for ex vivo multiscale evaluation of human breast tissues,” Cancer Res. 70(24), 10071–10079 (2010).
[Crossref] [PubMed]

2009 (3)

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]

D. S. Gareau, J. K. Karen, S. W. Dusza, M. Tudisco, K. S. Nehal, and M. Rajadhyaksha, “Sensitivity and specificity for detecting basal cell carcinomas in Mohs excisions with confocal fluorescence mosaicing microscopy,” J. Biomed. Opt. 14(3), 034012 (2009).
[Crossref] [PubMed]

S. L. Blair, K. Thompson, J. Rococco, V. Malcarne, P. D. Beitsch, and D. W. Ollila, “Attaining negative margins in breast-conservation operations: is there a consensus among breast surgeons?” J. Am. Coll. Surg. 209(5), 608–613 (2009).
[Crossref] [PubMed]

2008 (2)

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).
[Crossref] [PubMed]

I. L. Nesvold, A. A. Dahl, E. Løkkevik, A. Marit Mengshoel, and S. D. Fosså, “Arm and shoulder morbidity in breast cancer patients after breast-conserving therapy versus mastectomy,” Acta Oncol. 47(5), 835–842 (2008).
[Crossref] [PubMed]

2007 (3)

T. P. Olson, J. Harter, A. Muñoz, D. M. Mahvi, and T. Breslin, “Frozen section analysis for intraoperative margin assessment during breast-conserving surgery results in low rates of re-excision and local recurrence,” Ann. Surg. Oncol. 14(10), 2953–2960 (2007).
[Crossref] [PubMed]

Y. G. Patel, K. S. Nehal, I. Aranda, Y. Li, A. C. Halpern, and M. Rajadhyaksha, “Confocal reflectance mosaicing of basal cell carcinomas in Mohs surgical skin excisions,” J. Biomed. Opt. 12(3), 034027 (2007).
[Crossref] [PubMed]

P.-L. Hsiung, D. R. Phatak, Y. Chen, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Benign and malignant lesions in the human breast depicted with ultrahigh resolution and three-dimensional optical coherence tomography,” Radiology 244(3), 865–874 (2007).
[Crossref] [PubMed]

2006 (1)

G. A. Cèfaro, D. Genovesi, R. Marchese, L. A. Ursini, E. Cianchetti, E. Ballone, and M. Di Nicola, “Predictors of local recurrence after conservative surgery and whole-breast irradiation,” Breast Cancer Res. Treat. 98(3), 329–335 (2006).
[Crossref] [PubMed]

2004 (2)

J. Engel, J. Kerr, A. Schlesinger-Raab, H. Sauer, and D. Holzel, “Quality of life following breast-conserving therapy or mastectomy: results of a 5-year prospective study,” Breast J. 10(3), 223–231 (2004).
[Crossref] [PubMed]

F. J. Fleming, A. D. Hill, E. W. Mc Dermott, A. O’Doherty, N. J. O’Higgins, and C. M. Quinn, “Intraoperative margin assessment and re-excision rate in breast conserving surgery,” Eur. J. Surg. Oncol. 30(3), 233–237 (2004).
[Crossref] [PubMed]

2003 (1)

J. J. Coen, A. G. Taghian, L. A. Kachnic, S. I. Assaad, and S. N. Powell, “Risk of lymphedema after regional nodal irradiation with breast conservation therapy,” Int. J. Radiat. Oncol. Biol. Phys. 55(5), 1209–1215 (2003).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

G. P. Swanson, K. Rynearson, and R. Symmonds, “Significance of margins of excision on breast cancer recurrence,” Am. J. Clin. Oncol. 25(5), 438–441 (2002).
[Crossref] [PubMed]

2000 (2)

M. R. Weiser, L. L. Montgomery, B. Susnik, L. K. Tan, P. I. Borgen, and H. S. Cody, “Is routine intraoperative frozen-section examination of sentinel lymph nodes in breast cancer worthwhile?” Ann. Surg. Oncol. 7(9), 651–655 (2000).
[Crossref] [PubMed]

J. A. van Dongen, A. C. Voogd, I. S. Fentiman, C. Legrand, R. J. Sylvester, D. Tong, E. van der Schueren, P. A. Helle, K. van Zijl, and H. Bartelink, “Long-term results of a randomized trial comparing breast-conserving therapy with mastectomy: European Organization for Research and Treatment of Cancer 10801 trial,” J. Natl. Cancer Inst. 92(14), 1143–1150 (2000).
[Crossref] [PubMed]

1998 (1)

J. L. Connolly, J. Boyages, A. J. Nixon, G. Peiró, I. Gage, B. Silver, A. Recht, J. R. Harris, and S. J. Schnitt, “Predictors of breast recurrence after conservative surgery and radiation therapy for invasive breast cancer,” Mod. Pathol. 11(2), 134–139 (1998).
[PubMed]

1997 (1)

D. A. Novis and R. J. Zarbo, “Interinstitutional comparison of frozen section turnaround time. A College of American Pathologists Q-Probes study of 32868 frozen sections in 700 hospitals,” Arch. Pathol. Lab. Med. 121(6), 559–567 (1997).
[PubMed]

1996 (1)

R. Arriagada, M. G. Lê, F. Rochard, G. Contesso, and Institut Gustave-Roussy Breast Cancer Group, “Conservative treatment versus mastectomy in early breast cancer: patterns of failure with 15 years of follow-up data,” J. Clin. Oncol. 14(5), 1558–1564 (1996).
[Crossref] [PubMed]

1986 (1)

D. Carter, “Margins of “lumpectomy” for breast cancer,” Hum. Pathol. 17(4), 330–332 (1986).
[Crossref] [PubMed]

Abeytunge, S.

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), 34002 (2017).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Agar, N. Y. R.

F. K. Lu, D. Calligaris, O. I. Olubiyi, I. Norton, W. Yang, S. Santagata, X. S. Xie, A. J. Golby, and N. Y. R. Agar, “Label-free neurosurgical pathology with stimulated Raman imaging,” Cancer Res. 76(12), 3451–3462 (2016).
[Crossref] [PubMed]

Agrawal, A.

D. M. Layfield, A. Agrawal, H. Roche, and R. I. Cutress, “Intraoperative assessment of sentinel lymph nodes in breast cancer,” Br. J. Surg. 98(1), 4–17 (2011).
[Crossref] [PubMed]

Aguirre, A. D.

C. Zhou, D. W. D. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated optical coherence tomography and microscopy for ex vivo multiscale evaluation of human breast tissues,” Cancer Res. 70(24), 10071–10079 (2010).
[Crossref] [PubMed]

P.-L. Hsiung, D. R. Phatak, Y. Chen, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Benign and malignant lesions in the human breast depicted with ultrahigh resolution and three-dimensional optical coherence tomography,” Radiology 244(3), 865–874 (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]

Alderman, A. K.

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).
[Crossref] [PubMed]

Alexandrov, Y.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. French, A. Chu, G. W. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS One 7(9), e43460 (2012).
[Crossref] [PubMed]

Alibhai, S.

S. Alkhateeb, S. Alibhai, N. Fleshner, A. Finelli, M. Jewett, A. Zlotta, M. Nesbitt, G. Lockwood, and J. Trachtenberg, “Impact of positive surgical margins after radical prostatectomy differs by disease risk group,” J. Urol. 183(1), 145–150 (2010).
[Crossref] [PubMed]

Alkhateeb, S.

S. Alkhateeb, S. Alibhai, N. Fleshner, A. Finelli, M. Jewett, A. Zlotta, M. Nesbitt, G. Lockwood, and J. Trachtenberg, “Impact of positive surgical margins after radical prostatectomy differs by disease risk group,” J. Urol. 183(1), 145–150 (2010).
[Crossref] [PubMed]

Anderson, S.

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).
[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(5), 455–468 (2014).
[PubMed]

Aranda, I.

Y. G. Patel, K. S. Nehal, I. Aranda, Y. Li, A. C. Halpern, and M. Rajadhyaksha, “Confocal reflectance mosaicing of basal cell carcinomas in Mohs surgical skin excisions,” J. Biomed. Opt. 12(3), 034027 (2007).
[Crossref] [PubMed]

Argenziano, G.

C. Longo, M. Ragazzi, S. Gardini, S. Piana, E. Moscarella, A. Lallas, M. Raucci, G. Argenziano, and G. Pellacani, “Ex vivo fluorescence confocal microscopy in conjunction with Mohs micrographic surgery for cutaneous squamous cell carcinoma,” J. Am. Acad. Dermatol. 73(2), 321–322 (2015).
[Crossref] [PubMed]

Arriagada, R.

R. Arriagada, M. G. Lê, F. Rochard, G. Contesso, and Institut Gustave-Roussy Breast Cancer Group, “Conservative treatment versus mastectomy in early breast cancer: patterns of failure with 15 years of follow-up data,” J. Clin. Oncol. 14(5), 1558–1564 (1996).
[Crossref] [PubMed]

Assaad, S. I.

J. J. Coen, A. G. Taghian, L. A. Kachnic, S. I. Assaad, and S. N. Powell, “Risk of lymphedema after regional nodal irradiation with breast conservation therapy,” Int. J. Radiat. Oncol. Biol. Phys. 55(5), 1209–1215 (2003).
[Crossref] [PubMed]

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(5), 455–468 (2014).
[PubMed]

Baker, M. J.

M. J. Baker, J. Trevisan, P. Bassan, R. Bhargava, H. J. Butler, K. M. Dorling, P. R. Fielden, S. W. Fogarty, N. J. Fullwood, K. A. Heys, C. Hughes, P. Lasch, P. L. Martin-Hirsch, B. Obinaju, G. D. Sockalingum, J. Sulé-Suso, R. J. Strong, M. J. Walsh, B. R. Wood, P. Gardner, and F. L. Martin, “Using Fourier transform IR spectroscopy to analyze biological materials,” Nat. Protoc. 9(8), 1771–1791 (2014).
[Crossref] [PubMed]

Ballone, E.

G. A. Cèfaro, D. Genovesi, R. Marchese, L. A. Ursini, E. Cianchetti, E. Ballone, and M. Di Nicola, “Predictors of local recurrence after conservative surgery and whole-breast irradiation,” Breast Cancer Res. Treat. 98(3), 329–335 (2006).
[Crossref] [PubMed]

Bartelink, H.

J. A. van Dongen, A. C. Voogd, I. S. Fentiman, C. Legrand, R. J. Sylvester, D. Tong, E. van der Schueren, P. A. Helle, K. van Zijl, and H. Bartelink, “Long-term results of a randomized trial comparing breast-conserving therapy with mastectomy: European Organization for Research and Treatment of Cancer 10801 trial,” J. Natl. Cancer Inst. 92(14), 1143–1150 (2000).
[Crossref] [PubMed]

Bassan, P.

M. J. Baker, J. Trevisan, P. Bassan, R. Bhargava, H. J. Butler, K. M. Dorling, P. R. Fielden, S. W. Fogarty, N. J. Fullwood, K. A. Heys, C. Hughes, P. Lasch, P. L. Martin-Hirsch, B. Obinaju, G. D. Sockalingum, J. Sulé-Suso, R. J. Strong, M. J. Walsh, B. R. Wood, P. Gardner, and F. L. Martin, “Using Fourier transform IR spectroscopy to analyze biological materials,” Nat. Protoc. 9(8), 1771–1791 (2014).
[Crossref] [PubMed]

Beitsch, P. D.

S. L. Blair, K. Thompson, J. Rococco, V. Malcarne, P. D. Beitsch, and D. W. Ollila, “Attaining negative margins in breast-conservation operations: is there a consensus among breast surgeons?” J. Am. Coll. Surg. 209(5), 608–613 (2009).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Benveniste, A. P.

J. Dobbs, S. Krishnamurthy, M. Kyrish, A. P. Benveniste, W. Yang, and R. Richards-Kortum, “Confocal fluorescence microscopy for rapid evaluation of invasive tumor cellularity of inflammatory breast carcinoma core needle biopsies,” Breast Cancer Res. Treat. 149(1), 303–310 (2015).
[Crossref] [PubMed]

Bhargava, R.

M. J. Baker, J. Trevisan, P. Bassan, R. Bhargava, H. J. Butler, K. M. Dorling, P. R. Fielden, S. W. Fogarty, N. J. Fullwood, K. A. Heys, C. Hughes, P. Lasch, P. L. Martin-Hirsch, B. Obinaju, G. D. Sockalingum, J. Sulé-Suso, R. J. Strong, M. J. Walsh, B. R. Wood, P. Gardner, and F. L. Martin, “Using Fourier transform IR spectroscopy to analyze biological materials,” Nat. Protoc. 9(8), 1771–1791 (2014).
[Crossref] [PubMed]

Bishop, J.

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, 957–966 (2017).

Blair, S. L.

S. L. Blair, K. Thompson, J. Rococco, V. Malcarne, P. D. Beitsch, and D. W. Ollila, “Attaining negative margins in breast-conservation operations: is there a consensus among breast surgeons?” J. Am. Coll. Surg. 209(5), 608–613 (2009).
[Crossref] [PubMed]

Blond, B. J.

A. J. Guidi, J. A. Tworek, D. D. Mais, R. J. Souers, B. J. Blond, and R. W. Brown, “Breast Specimen Processing and Reporting With an Emphasis on Margin Evaluation,” Arch. Pathol. Lab Med.  142(4), 496–506 (2018).

Boccara, C.

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(5), 455–468 (2014).
[PubMed]

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).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

A. M. Zysk, K. Chen, E. Gabrielson, L. Tafra, E. A. May Gonzalez, J. K. Canner, E. B. Schneider, A. J. Cittadine, P. Scott Carney, S. A. Boppart, K. Tsuchiya, K. Sawyer, and L. K. Jacobs, “Intraoperative Assessment of Final Margins with a Handheld Optical Imaging Probe During Breast-Conserving Surgery May Reduce the Reoperation Rate: Results of a Multicenter Study,” Ann. Surg. Oncol. 22(10), 3356–3362 (2015).
[Crossref] [PubMed]

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]

Borgen, P. I.

M. R. Weiser, L. L. Montgomery, B. Susnik, L. K. Tan, P. I. Borgen, and H. S. Cody, “Is routine intraoperative frozen-section examination of sentinel lymph nodes in breast cancer worthwhile?” Ann. Surg. Oncol. 7(9), 651–655 (2000).
[Crossref] [PubMed]

Borowsky, A. D.

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, 957–966 (2017).

Boyages, J.

J. L. Connolly, J. Boyages, A. J. Nixon, G. Peiró, I. Gage, B. Silver, A. Recht, J. R. Harris, and S. J. Schnitt, “Predictors of breast recurrence after conservative surgery and radiation therapy for invasive breast cancer,” Mod. Pathol. 11(2), 134–139 (1998).
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B. S. Nichols, A. Llopis, G. M. Palmer, S. S. McCachren, O. Senlik, D. Miller, M. A. Brooke, N. M. Jokerst, J. Geradts, R. Greenup, and N. Ramanujam, “Miniature spectral imaging device for wide-field quantitative functional imaging of the morphological landscape of breast tumor margins,” J. Biomed. Opt. 22(2), 026007 (2017).
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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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A. J. Guidi, J. A. Tworek, D. D. Mais, R. J. Souers, B. J. Blond, and R. W. Brown, “Breast Specimen Processing and Reporting With an Emphasis on Margin Evaluation,” Arch. Pathol. Lab Med.  142(4), 496–506 (2018).

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D. A. Novis and R. J. Zarbo, “Interinstitutional comparison of frozen section turnaround time. A College of American Pathologists Q-Probes study of 32868 frozen sections in 700 hospitals,” Arch. Pathol. Lab. Med. 121(6), 559–567 (1997).
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Figures (12)

Fig. 1
Fig. 1 Multiscale NLM system. Diagram of the NLM beam path including laser power controller, beam expander, laser interlock shutter, galvanometer-resonant scanner, scan/tube lens, filter cube and PMTs (left). Photograph of the instrument deployed at BIDMC (right).
Fig. 2
Fig. 2 Objective translator assembly shown integrated into the microscope (top left), separate from the microscope (bottom left), as assembled and installed (middle) and a ray diagram of the NLM system and objective translator (right).
Fig. 3
Fig. 3 Diagram of the widefield imaging system. Line illumination is provided by an LED array projected onto the specimen tray. A line scan camera and fold mirror are used to image the illuminated line as the specimen tray is translated through the camera focus.
Fig. 4
Fig. 4 Specimen tray. Rendering of the interchangeable specimen tray (left) and photograph of the tray with 6 inked, bread loaf breast specimens (right). The tray incorporates a lid with fill port as well as inset dividers that can be used to separate multiple small specimens.
Fig. 5
Fig. 5 Software user interface and controls used to image freshly excised, inked bread loafed surgical specimens. The virtual H&E display shows a terminal ductal lobule unit (TDLU) imaged at 20x magnification, while the white light microscopy shows a widefield image with the current imaging location adjacent to a simulated inked margin. The user can rapidly (< 1 second) switch the magnification, while a joystick and digital focus knob are used for X/Y and Z control, respectively. An LED indicator shows the laser interlock status, enabling the operator to see when the specimen is loaded and the laser armed.
Fig. 6
Fig. 6 Analog and digital data flow diagram separated into three phases of system operation.
Fig. 7
Fig. 7 Dewarping and stitching of live data to generate mosaics. By synchronously recording position data with each fast axis cycle, the true geometric position of all pixels in each image can be calculated and the resulting frames stitched into an undistorted mosaic.
Fig. 8
Fig. 8 Lateral (left) and axial (right) point spread function plots for the 5x (top) and 10x (bottom) objectives measured using sub-resolution fluorescent beads.
Fig. 9
Fig. 9 Comparison between 5x/0.25 NA and 10x/0.45 NA objectives at 1030 nm excitation wavelength using discarded superficial breast tissue excised during surgery for invasive ductal carcinoma. The biopsy site and skin are present along with large areas of fat and stroma (top left). Mosaic images viewed at low magnification show relatively limited difference between the two objectives (top center – 5x, top right – 10x), however zoomed views of the boxed regions show that cellular features are poorly resolved with the 5x/0.25 objective. In contrast, the structure of a blood vessel is readily identifiable with the 10x/0.45 objective. Scale bars: 1 cm (top) and 400 μm (bottom). Total area: 7.9 cm2. Full resolution image: http://imstore.mit.edu/system/Fig9.html.
Fig. 10
Fig. 10 Comparison between an NLM mosaic image of the specimen surface using the 10x / 0.45 NA objective and FFPE histology from approximately 300 μm below the surface of a breast surgical specimen with ductal carcinoma in situ. Scale bar: 2 mm. Total area: 2.2 cm2. Full resolution image: http://imstore.mit.edu/system/Fig10.html.
Fig. 11
Fig. 11 Comparison of mosaic and real-time imaging using normal human breast tissue inked to simulate a surgical margin. The widefield white light image (left) enables visualization of the tissue and regions of purple and blue ink on the simulated margins. Mosaic NLM (center) images the entire specimen face but required 487 seconds. In contrast, real-time assessment using the 10x objective required less than 45 seconds because the operator imaged only the margins using opportunistic averaging and did not image non-diagnostic regions such as adipose tissue. The lower scattering and absorption of 1030 nm excitation wavelength enabled imaging below thin layers of ink on the simulated margin. Scale bars: 2 mm. Total area: 3.9 cm2. Full resolution image: http://imstore.mit.edu/system/Fig11.html.
Fig. 12
Fig. 12 Comparison of real-time imaging using 5x/0.25 NA and 10x/0.45 NA objectives to assess an inked tissue specimen containing both normal tissue and invasive ductal carcinoma. Orange, yellow and green ink are grossly visible in the widefield image (bottom left), while each color is visible as fluorescence in one or both spectral channels in the NLM images. Both 10x and 5x objectives enable surveying the entire simulated margin in less than 1 minute, however the 5x objective is approximately 2x faster and can assess tissue further from the inked margins. Scale bars: 2 mm (top, left) and 400 μm (bottom right). Total specimen area: 4.0 cm2. Full resolution image: http://imstore.mit.edu/system/Fig12.html.

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