Abstract

Microscopic tumor cell foci left in a patient after surgery significantly increase the chance of cancer recurrence. However, fluorescence microscopes used for intraoperative navigation lack the necessary sensitivity for imaging microscopic disease and are too bulky to maneuver within the resection cavity. We have developed a scalable chip-scale fluorescence contact imager for detecting microscopic cancer in vivo and in real-time. The imager has been characterized under simulated in vivo conditions using ex vivo samples, providing strong evidence that our device can be used in vivo. Angle-selective gratings enhance the resolution of the imager without impacting its physical size. We demonstrate detection of cancer cell clusters containing as few as 25 HCC1569 breast cancer cells and 400 LNCaP prostate cancer cells with integration times of only 50 ms and 70 ms, respectively. A cell cluster recognition algorithm is used to achieve both a sensitivity and specificity of 92 % for HCC1569 cell samples, indicating the reliability of the imager. The signal-to-noise ratio (SNR) degradation with increased separation is only 1.5 dB at 250 μm. Blood scattering and absorption reduce the SNR by less than 2 dB for typical concentrations. Moreover, HER2+ breast cancer tissue taken from a patient is distinguished from normal breast tissue with an integration time of only 75 ms.

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

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M. Koch, J. S. de Jong, J. Glatz, P. Symvoulidis, L. E. Lamberts, A. L. L. Adams, M. E. G. Kranendonk, A. G. T. Terwisscha van Scheltinga, M. Aichler, L. Jansen, J. de Vries, M. N. Lub-de Hooge, C. P. Schrüder, A. Jorritsma-Smit, M. D. Linssen, E. de Boer, B. van der Vegt, W. B. Nagengast, S. G. Elias, S. Oliveira, A. J. Witkamp, W. P. T. M. Mali, E. Van der Wall, P. B. Garcia-Allende, P. J. van Diest, E. G. E. de Vries, A. Walch, G. M. van Dam, and V. Ntziachristos, “Threshold Analysis and Biodistribution of Fluorescently Labeled Bevacizumab in Human Breast Cancer,” Cancer Res.. 77(3), 623–631 (2017).
[Crossref]

L. Hong, H. Li, H. Yang, and K. Sengupta, “Fully Integrated Fluorescence Biosensors On-Chip Employing Multi-Functional Nanoplasmonic Optical Structures in CMOS,” IEEE J. Solid-State Circuits 52(9), 2388–2406 (2017).
[Crossref]

L. Hong and K. Sengupta, “Fully Integrated Optical Spectrometer in Visible and Near-IR in CMOS,” IEEE Transactions on Biomed. Circuits Syst. 11(6), 1176–1191 (2017).
[Crossref]

K. Ito, M. Mitsunaga, T. Nishimura, M. Saruta, T. Iwamoto, H. Kobayashi, and H. Tajiri, “Near-Infrared Photochemoimmunotherapy by Photoactivatable Bifunctional Antibody–Drug Conjugates Targeting Human Epidermal Growth Factor Receptor 2 Positive Cancer,” Bioconjugate Chem. 28(5), 1458–1469 (2017).
[Crossref]

2016 (6)

M. Garland, J. J. Yim, and M. Bogyo, “A Bright Future for Precision Medicine: Advances in Fluorescent Chemical Probe Design and Their Clinical Application,” Cell Chem. Biol. 23(1), 122–136 (2016).
[Crossref] [PubMed]

S. Türkcan, D. J. Naczynski, R. Nolley, L. S. Sasportas, D. M. Peehl, and G. Pratx, “Endoscopic detection of cancer with lensless radioluminescence imaging and machine vision,” Sci. Rep. 6, srep30737 (2016).

A. V. DSouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. 21(8), 080901 (2016).

E. de Boer, S. Samuel, D. N. French, J. M. Warram, T. R. Schoeb, E. L. Rosenthal, and K. R. Zinn, “Biodistribution Study of Intravenously Injected Cetuximab-IRDye700dx in Cynomolgus Macaques,” Mol Imaging Biol 8(2), 232–242 (2016).
[Crossref]

Y. Yoon, A. M. Mohs, M. C. Mancini, S. Nie, and H. Shim, “Combination of an Integrin-Targeting NIR Tracer and an Ultrasensitive Spectroscopic Device for Intraoperative Detection of Head and Neck Tumor Margins and Metastatic Lymph Nodes,” Tomography. 2(3), 215–222 (2016).
[Crossref] [PubMed]

M. Villiger, D. Lorenser, R. A. McLaughlin, B. C. Quirk, R. W. Kirk, B. E. Bouma, and D. D. Sampson, “Deep tissue volume imaging of birefringence through fibre-optic needle probes for the delineation of breast tumour,” Sci. Rep. 6, 28771 (2016).

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M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette, K. Saint-Arnaud, L. Bernstein, M.-C. Guiot, K. Petrecca, and F. Leblond, “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Medicine 7(274), 274ra19 (2015).
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S. B. Mondal, S. Gao, N. Zhu, G. P. Sudlow, K. Liang, A. Som, W. J. Akers, R. C. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular Goggle Augmented Imaging and Navigation System provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 512117 (2015).

E. L. Rosenthal, J. M. Warram, E. de Boer, T. K. Chung, M. L. Korb, M. Brandwein-Gensler, T. V. Strong, C. E. Schmalbach, A. B. Morlandt, G. Agarwal, Y. E. Hartman, W. R. Carroll, J. S. Richman, L. K. Clemons, L. M Nabell, and K. R. Zinn, “Safety and Tumor Specificity of Cetuximab-IRDye800 for Surgical Navigation in Head and Neck Cancer,” Clin Cancer Res. 21(16), 3658–3666 (2015).
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A. M. Zysk, K. Chen, E. Gabrielson, L. Tafra, E. A. M. Gonzalez, J. K. Canner, E. B. Schneider, A. J. Cittadine, P. S. 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).
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K. L. Kummerow, L. Du, D. F. Penson, Y. Shyr, and M. A. Hooks, “Nationwide Trends in Mastectomy for Early-Stage Breast Cancer,” JAMA Surg 150(1), 9–16 (2015).
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R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer statistics, 2015,” CA: A Cancer J. for Clin. 65(1), 5–29 (2015).

A. B. Chagpar, B. K. Killelea, T. N. Tsangaris, M. Butler, K. Stavris, F. Li, X. Yao, V. Bossuyt, M. Harigopal, D. R. Lannin, L. Pusztai, and N. R. Horowitz, “A Randomized, Controlled Trial of Cavity Shave Margins in Breast Cancer,” New Engl. J. Medicine 373(6), 503–510 (2015).
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K. Kourou, T. P. Exarchos, K. P. Exarchos, M. V. Karamouzis, and D. I. Fotiadis, “Machine learning applications in cancer prognosis and prediction,” Comput. Struct. Biotechnol. J. 13, 8–17 (2015).
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2014 (4)

D. Kuzum, H. Takano, E. Shim, J. C. Reed, H. Juul, A. G. Richardson, J. de Vries, H. Bink, M. A. Dichter, T. H. Lucas, D. A. Coulter, E. Cubukcu, and B. Litt, “Transparent and flexible low noise graphene electrodes for simultaneous electrophysiology and neuroimaging,” Nat. Commun. 5, 6259 (2014).
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L. G. Wilke, T. Czechura, C. Wang, B. Lapin, E. Liederbach, D. P. Winchester, and K. Yao, “Repeat Surgery After Breast Conservation for the Treatment of Stage 0 to II Breast Carcinoma: A Report From the National Cancer Data Base, 2004–2010,” JAMA Surg. 149(12), 1296–1305 (2014).
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T. A. Buchholz, M. R. Somerfield, J. J. Griggs, S. El-Eid, M. E. H. Hammond, G. H. Lyman, G. Mason, and L. A. Newman, “Margins for Breast-Conserving Surgery With Whole-Breast Irradiation in Stage I and II Invasive Breast Cancer: American Society of Clinical Oncology Endorsement of the Society of Surgical Oncology/American Society for Radiation Oncology Consensus Guideline,” J. Clin. Oncol. 32(14), 1502–1506 (2014).
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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, and M. Morrow, “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,” Int. J. Radiat. Oncol. 88(3), 553–564 (2014).
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2012 (1)

L. E. McCahill, R. M. Single, E. J. A. Bowles, H. S. Feigelson, T. A. James, T. Barney, J. M. Engel, and A. A. Onitilo, “Variability in Reexcision Following Breast Conservation Surgery,” JAMA 307(5), 467–475 (2012).
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2011 (4)

Y. Liu, A. Q. Bauer, W. J. Akers, G. Sudlow, K. Liang, D. Shen, M. Y. Berezin, J. P. Culver, and S. Achilefu, “Hands-free, wireless goggles for near-infrared fluorescence and real-time image-guided surgery,” Surgery 149(5), 689–698 (2011).
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G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat Med 17(10), 1315–1319 (2011).
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J. Viventi, D.-H. Kim, L. Vigeland, E. S. Frechette, J. A. Blanco, Y.-S. Kim, A. E. Avrin, V. R. Tiruvadi, S.-W. Hwang, A. C. Vanleer, D. F. Wulsin, K. Davis, C. E. Gelber, L. Palmer, J. Van der Spiegel, J. Wu, J. Xiao, Y. Huang, D. Contreras, J. A. Rogers, and B. Litt, “Flexible, foldable, actively multiplexed, high-density electrode array for mapping brain activity in vivo,” Nat. Neurosci. 14(12), 1599 (2011).
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C. Gutierrez and R. Schiff, “HER2: Biology, Detection, and Clinical Implications,” Arch. Pathol. & Lab. Medicine 135(1), 55–62 (2011).

2010 (3)

D. Shin, M. C. Pierce, A. M. Gillenwater, M. D. Williams, and R. R. Richards-Kortum, “A Fiber-Optic Fluorescence Microscope Using a Consumer-Grade Digital Camera for In Vivo Cellular Imaging,” PLoS ONE 5(6), e11218 (2010).
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J.-M. Nam, Y. Onodera, M. J. Bissell, and C. C. Park, “Breast Cancer Cells in Three-dimensional Culture Display an Enhanced Radioresponse after Coordinate Targeting of Integrin α5β1 and Fibronectin,” Cancer Res. 70(13), 5238–5248 (2010).
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A. M. Mohs, M. C. Mancini, S. Singhal, J. M. Provenzale, B. Leyland-Jones, M. D. Wang, and S. Nie, “Hand-held Spectroscopic Device for In Vivo and Intraoperative Tumor Detection: Contrast Enhancement, Detection Sensitivity, and Tissue Penetration,” Anal. Chem. 82(21), 9058–9065 (2010).
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2009 (3)

M. Ogawa, N. Kosaka, P. L. Choyke, and H. Kobayashi, “In vivo Molecular Imaging of Cancer with a Quenching Near-Infrared Fluorescent Probe Using Conjugates of Monoclonal Antibodies and Indocyanine Green,” Cancer Res. 69(4), 1268–1272 (2009).
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K. Gotoh, T. Yamada, O. Ishikawa, H. Takahashi, H. Eguchi, M. Yano, H. Ohigashi, Y. Tomita, Y. Miyamoto, and S. Imaoka, “A novel image-guided surgery of hepatocellular carcinoma by indocyanine green fluorescence imaging navigation,” J. Surg. Oncol. 100(1), 75–79 (2009).
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S. L. Troyan, V. Kianzad, S. L. Gibbs-Strauss, S. Gioux, A. Matsui, R. Oketokoun, L. Ngo, A. Khamene, F. Azar, and J. V. Frangioni, “The FLARE™ Intraoperative Near-Infrared Fluorescence Imaging System: A First-in-Human Clinical Trial in Breast Cancer Sentinel Lymph Node Mapping,” Annals Surg. Oncol. 16(10), 2943–2952 (2009).
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2008 (1)

M. McElroy, S. Kaushal, G. A. Luiken, M. A. Talamini, A. R. Moosa, R. M. Hoffman, and M. Bouvet, “Imaging of Primary and Metastatic Pancreatic Cancer Using a Fluorophore-Conjugated Anti-CA19-9 Antibody for Surgical Navigation,” World J Surg 32(6), 1057–1066 (2008).
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2007 (3)

H. Tada, H. Higuchi, T. M. Wanatabe, and N. Ohuchi, “In vivo Real-time Tracking of Single Quantum Dots Conjugated with Monoclonal Anti-HER2 Antibody in Tumors of Mice,” Cancer Res. 67(3), 1138–1144 (2007).
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A. J. Stephenson, P. T. Scardino, M. W. Kattan, T. M. Pisansky, K. M. Slawin, E. A. Klein, M. S. Anscher, J. M. Michalski, H. M. Sandler, D. W. Lin, J. D. Forman, M. J. Zelefsky, L. L. Kestin, C. G. Roehrborn, C. N. Catton, T. L. DeWeese, S. L. Liauw, R. K. Valicenti, D. A. Kuban, and A. Pollack, “Predicting the Outcome of Salvage Radiation Therapy for Recurrent Prostate Cancer After Radical Prostatectomy,” J. Clin. Oncol. 25(15), 2035–2041 (2007).
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M. A. Haider, T. H. van der Kwast, J. Tanguay, A. J. Evans, A.-T. Hashmi, G. Lockwood, and J. Trachtenberg, “Combined T2-Weighted and Diffusion-Weighted MRI for Localization of Prostate Cancer,” Am. J. Roentgenol. 189(2), 323–328 (2007).
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2006 (2)

J. W. Duparré and F. C. Wippermann, “Micro-optical artificial compound eyes,” Bioinspir. Biomim. 1(1), R1 (2006).
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C. C. Park, H. Zhang, M. Pallavicini, J. W. Gray, F. Baehner, C. J. Park, and M. J. Bissell, “β1 Integrin Inhibitory Antibody Induces Apoptosis of Breast Cancer Cells, Inhibits Growth, and Distinguishes Malignant from Normal Phenotype in Three Dimensional Cultures and In vivo,” Cancer Res. 66(3), 1526–1535 (2006).
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2005 (1)

Early Breast Cancer Trialists’ Collaborative Group (EBCTCG), “Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials,” The Lancet 366(9503), 2087–2106 (2005).
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2004 (2)

F. Sardanelli, G. M. Giuseppetti, P. Panizza, M. Bazzocchi, A. Fausto, G. Simonetti, V. Lattanzio, and A. Del Maschio, “Sensitivity of MRI Versus Mammography for Detecting Foci of Multifocal, Multicentric Breast Cancer in Fatty and Dense Breasts Using the Whole-Breast Pathologic Examination as a Gold Standard,” Am. J. Roentgenol. 183(4), 1149–1157 (2004).
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X. Gao, Y. Cui, R. M. Levenson, L. W. K. Chung, and S. Nie, “In vivo cancer targeting and imaging with semiconductor quantum dots,” Nat. Biotechnol. 22(8), 969–976, (2004).
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2003 (4)

J. A. Eastham, M. W. Kattan, E. Riedel, C. B. Begg, T. M. Wheeler, C. Gerigk, M. Gonen, V. Reuter, and P. T. Scardino, “Variations Among Individual Surgeons in the Rate of Positive Surgical Margins in Radical Prostatectomy Specimens,” J. Urol. 170(6), 2292–2295 (2003).
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J. V. Frangioni, “In vivo near-infrared fluorescence imaging,” Curr. Opin. Chem. Biol. 7(5), 626–634, (2003).
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R. Völkel, M. Eisner, and K. J. Weible, “Miniaturized imaging systems,” Microelectron. Eng. 67–68, 461–472 (2003).
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G. Agranov, V. Berezin, and R. H. Tsai, “Crosstalk and microlens study in a color CMOS image sensor,” IEEE Transactions on Electron Devices 50(1), 4–11 (2003).
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2002 (1)

S. E. Singletary, “Surgical margins in patients with early-stage breast cancer treated with breast conservation therapy,” The Am. J. Surg. 184(5), 383–393 (2002).
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2000 (1)

P. M. Smith-Jones, S. Vallabahajosula, S. J. Goldsmith, V. Navarro, C. J. Hunter, D. Bastidas, and N. H. Bander, “In Vitro Characterization of Radiolabeled Monoclonal Antibodies Specific for the Extracellular Domain of Prostate-specific Membrane Antigen,” Cancer Res. 60(18), 5237–5243 (2000).
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1998 (1)

J. A. Wieder and M. S. Soloway, “Incidence, Etiology, Location, Prevention and Treatment of Positive Surgical Margincs after Radical Prostatectomy for Prostate Cancer,” J. Urol. 160(2), 299–315 (1998).
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1989 (1)

F. P. Bolin, L. E. Preuss, R. C. Taylor, and R. J. Ference, “Refractive index of some mammalian tissues using a fiber optic cladding method,” Appl. Opt., AO 28(12), 2297–2303 (1989).
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Achilefu, S.

S. B. Mondal, S. Gao, N. Zhu, G. P. Sudlow, K. Liang, A. Som, W. J. Akers, R. C. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular Goggle Augmented Imaging and Navigation System provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 512117 (2015).

Y. Liu, A. Q. Bauer, W. J. Akers, G. Sudlow, K. Liang, D. Shen, M. Y. Berezin, J. P. Culver, and S. Achilefu, “Hands-free, wireless goggles for near-infrared fluorescence and real-time image-guided surgery,” Surgery 149(5), 689–698 (2011).
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Adams, A. L. L.

M. Koch, J. S. de Jong, J. Glatz, P. Symvoulidis, L. E. Lamberts, A. L. L. Adams, M. E. G. Kranendonk, A. G. T. Terwisscha van Scheltinga, M. Aichler, L. Jansen, J. de Vries, M. N. Lub-de Hooge, C. P. Schrüder, A. Jorritsma-Smit, M. D. Linssen, E. de Boer, B. van der Vegt, W. B. Nagengast, S. G. Elias, S. Oliveira, A. J. Witkamp, W. P. T. M. Mali, E. Van der Wall, P. B. Garcia-Allende, P. J. van Diest, E. G. E. de Vries, A. Walch, G. M. van Dam, and V. Ntziachristos, “Threshold Analysis and Biodistribution of Fluorescently Labeled Bevacizumab in Human Breast Cancer,” Cancer Res.. 77(3), 623–631 (2017).
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Agarwal, G.

E. L. Rosenthal, J. M. Warram, E. de Boer, T. K. Chung, M. L. Korb, M. Brandwein-Gensler, T. V. Strong, C. E. Schmalbach, A. B. Morlandt, G. Agarwal, Y. E. Hartman, W. R. Carroll, J. S. Richman, L. K. Clemons, L. M Nabell, and K. R. Zinn, “Safety and Tumor Specificity of Cetuximab-IRDye800 for Surgical Navigation in Head and Neck Cancer,” Clin Cancer Res. 21(16), 3658–3666 (2015).
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Agranov, G.

G. Agranov, V. Berezin, and R. H. Tsai, “Crosstalk and microlens study in a color CMOS image sensor,” IEEE Transactions on Electron Devices 50(1), 4–11 (2003).
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H. Rhodes, G. Agranov, C. Hong, U. Boettiger, R. Mauritzson, J. Ladd, I. Karasev, J. McKee, E. Jenkins, W. Quinlin, I. Patrick, J. Li, X. Fan, R. Panicacci, S. Smith, C. Mouli, and J. Bruce, “CMOS imager technology shrinks and image performance,” in “2004 IEEE Workshop on Microelectronics and Electron Devices,” (2004), 7–18.

Aichler, M.

M. Koch, J. S. de Jong, J. Glatz, P. Symvoulidis, L. E. Lamberts, A. L. L. Adams, M. E. G. Kranendonk, A. G. T. Terwisscha van Scheltinga, M. Aichler, L. Jansen, J. de Vries, M. N. Lub-de Hooge, C. P. Schrüder, A. Jorritsma-Smit, M. D. Linssen, E. de Boer, B. van der Vegt, W. B. Nagengast, S. G. Elias, S. Oliveira, A. J. Witkamp, W. P. T. M. Mali, E. Van der Wall, P. B. Garcia-Allende, P. J. van Diest, E. G. E. de Vries, A. Walch, G. M. van Dam, and V. Ntziachristos, “Threshold Analysis and Biodistribution of Fluorescently Labeled Bevacizumab in Human Breast Cancer,” Cancer Res.. 77(3), 623–631 (2017).
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Akers, W. J.

S. B. Mondal, S. Gao, N. Zhu, G. P. Sudlow, K. Liang, A. Som, W. J. Akers, R. C. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular Goggle Augmented Imaging and Navigation System provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 512117 (2015).

Y. Liu, A. Q. Bauer, W. J. Akers, G. Sudlow, K. Liang, D. Shen, M. Y. Berezin, J. P. Culver, and S. Achilefu, “Hands-free, wireless goggles for near-infrared fluorescence and real-time image-guided surgery,” Surgery 149(5), 689–698 (2011).
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Alander, J. T.

J. T. Alander, I. Kaartinen, A. Laakso, T. Pätilä, T. Spillmann, V. V. Tuchin, M. Venermo, and P. Välisuo, “A Review of Indocyanine Green Fluorescent Imaging in Surgery,” J. Biomed. Imaging, (2012).
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Anscher, M. S.

A. J. Stephenson, P. T. Scardino, M. W. Kattan, T. M. Pisansky, K. M. Slawin, E. A. Klein, M. S. Anscher, J. M. Michalski, H. M. Sandler, D. W. Lin, J. D. Forman, M. J. Zelefsky, L. L. Kestin, C. G. Roehrborn, C. N. Catton, T. L. DeWeese, S. L. Liauw, R. K. Valicenti, D. A. Kuban, and A. Pollack, “Predicting the Outcome of Salvage Radiation Therapy for Recurrent Prostate Cancer After Radical Prostatectomy,” J. Clin. Oncol. 25(15), 2035–2041 (2007).
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Anwar, M.

E. P. Papageorgiou, B. E. Boser, and M. Anwar, “An angle-selective CMOS imager with on-chip micro-collimators for blur reduction in near-field cell imaging,” in “2016 IEEE 29th International Conference on Micro Electro Mechanical Systems (MEMS),” (2016), pp. 337–340.

E. P. Papageorgiou, B. E. Boser, and M. Anwar, “Chip-scale fluorescence imager for in vivo microscopic cancer detection,” in “2017 Symposium on VLSI Circuits,” (2017), pp. C106–C107.

Arai, K.

N. Maeda, Y. S. Kim, Y. Hikosaka, T. Eshita, H. Kitada, K. Fujimoto, Y. Mizushima, K. Suzuki, T. Nakamura, A. Kawai, K. Arai, and T. Ohba, “Development of sub 10μm ultra-thinning technology using device wafers for 3D manufacturing of terabit memory,” in “2010 Symposium on VLSI Technology,” (2010), 105–106.

Arsinte, G.

J. Bogaerts, R. Lafaille, M. Borremans, J. Guo, B. Ceulemans, G. Meynants, N. Sarhangnejad, G. Arsinte, V. Statescu, and S. van der Groen, “105×65mm2 391mpixel CMOS image sensor with >78db dynamic range for airborne mapping applications,” in “ISSCC Digest of Technical Papers,” (2016), 114–115.

Arts, H. J. G.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat Med 17(10), 1315–1319 (2011).
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Avrin, A. E.

J. Viventi, D.-H. Kim, L. Vigeland, E. S. Frechette, J. A. Blanco, Y.-S. Kim, A. E. Avrin, V. R. Tiruvadi, S.-W. Hwang, A. C. Vanleer, D. F. Wulsin, K. Davis, C. E. Gelber, L. Palmer, J. Van der Spiegel, J. Wu, J. Xiao, Y. Huang, D. Contreras, J. A. Rogers, and B. Litt, “Flexible, foldable, actively multiplexed, high-density electrode array for mapping brain activity in vivo,” Nat. Neurosci. 14(12), 1599 (2011).
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Azar, F.

S. L. Troyan, V. Kianzad, S. L. Gibbs-Strauss, S. Gioux, A. Matsui, R. Oketokoun, L. Ngo, A. Khamene, F. Azar, and J. V. Frangioni, “The FLARE™ Intraoperative Near-Infrared Fluorescence Imaging System: A First-in-Human Clinical Trial in Breast Cancer Sentinel Lymph Node Mapping,” Annals Surg. Oncol. 16(10), 2943–2952 (2009).
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Baehner, F.

C. C. Park, H. Zhang, M. Pallavicini, J. W. Gray, F. Baehner, C. J. Park, and M. J. Bissell, “β1 Integrin Inhibitory Antibody Induces Apoptosis of Breast Cancer Cells, Inhibits Growth, and Distinguishes Malignant from Normal Phenotype in Three Dimensional Cultures and In vivo,” Cancer Res. 66(3), 1526–1535 (2006).
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Balalis, G. L.

A. Cousins, G. L. Balalis, S. K. Thompson, D. F. Morales, A. Mohtar, A. B. Wedding, and B. Thierry, “Novel Handheld Magnetometer Probe Based on Magnetic Tunnelling Junction Sensors for Intraoperative Sentinel Lymph Node Identification,” Sci. Rep. 5, 10842 (2015).

Bander, N. H.

P. M. Smith-Jones, S. Vallabahajosula, S. J. Goldsmith, V. Navarro, C. J. Hunter, D. Bastidas, and N. H. Bander, “In Vitro Characterization of Radiolabeled Monoclonal Antibodies Specific for the Extracellular Domain of Prostate-specific Membrane Antigen,” Cancer Res. 60(18), 5237–5243 (2000).
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Barney, T.

L. E. McCahill, R. M. Single, E. J. A. Bowles, H. S. Feigelson, T. A. James, T. Barney, J. M. Engel, and A. A. Onitilo, “Variability in Reexcision Following Breast Conservation Surgery,” JAMA 307(5), 467–475 (2012).
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Bart, J.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat Med 17(10), 1315–1319 (2011).
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Bastidas, D.

P. M. Smith-Jones, S. Vallabahajosula, S. J. Goldsmith, V. Navarro, C. J. Hunter, D. Bastidas, and N. H. Bander, “In Vitro Characterization of Radiolabeled Monoclonal Antibodies Specific for the Extracellular Domain of Prostate-specific Membrane Antigen,” Cancer Res. 60(18), 5237–5243 (2000).
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Bauer, A. Q.

Y. Liu, A. Q. Bauer, W. J. Akers, G. Sudlow, K. Liang, D. Shen, M. Y. Berezin, J. P. Culver, and S. Achilefu, “Hands-free, wireless goggles for near-infrared fluorescence and real-time image-guided surgery,” Surgery 149(5), 689–698 (2011).
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Bazzocchi, M.

F. Sardanelli, G. M. Giuseppetti, P. Panizza, M. Bazzocchi, A. Fausto, G. Simonetti, V. Lattanzio, and A. Del Maschio, “Sensitivity of MRI Versus Mammography for Detecting Foci of Multifocal, Multicentric Breast Cancer in Fatty and Dense Breasts Using the Whole-Breast Pathologic Examination as a Gold Standard,” Am. J. Roentgenol. 183(4), 1149–1157 (2004).
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Begg, C. B.

J. A. Eastham, M. W. Kattan, E. Riedel, C. B. Begg, T. M. Wheeler, C. Gerigk, M. Gonen, V. Reuter, and P. T. Scardino, “Variations Among Individual Surgeons in the Rate of Positive Surgical Margins in Radical Prostatectomy Specimens,” J. Urol. 170(6), 2292–2295 (2003).
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Berezin, M. Y.

Y. Liu, A. Q. Bauer, W. J. Akers, G. Sudlow, K. Liang, D. Shen, M. Y. Berezin, J. P. Culver, and S. Achilefu, “Hands-free, wireless goggles for near-infrared fluorescence and real-time image-guided surgery,” Surgery 149(5), 689–698 (2011).
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Berezin, V.

G. Agranov, V. Berezin, and R. H. Tsai, “Crosstalk and microlens study in a color CMOS image sensor,” IEEE Transactions on Electron Devices 50(1), 4–11 (2003).
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Bernstein, L.

M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette, K. Saint-Arnaud, L. Bernstein, M.-C. Guiot, K. Petrecca, and F. Leblond, “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Medicine 7(274), 274ra19 (2015).
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Bink, H.

D. Kuzum, H. Takano, E. Shim, J. C. Reed, H. Juul, A. G. Richardson, J. de Vries, H. Bink, M. A. Dichter, T. H. Lucas, D. A. Coulter, E. Cubukcu, and B. Litt, “Transparent and flexible low noise graphene electrodes for simultaneous electrophysiology and neuroimaging,” Nat. Commun. 5, 6259 (2014).
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Figures (8)

Fig. 1
Fig. 1 (a) Conventional fluorescence microscope. (b) In vitro contact imaging. (c) In vivo contact imaging using an image sensor with ASGs to recover the lost resolution due to light divergence. (d) Image sensor with ASGs bonded onto a PCB. (e) Optical filter epoxied using clear optical epoxy on top of image sensor with ASGs. Dark epoxy is used for electrical isolation.
Fig. 2
Fig. 2 Images of two locations of slides containing HCC1569 breast cancer 3D cell cultures. (a,b) Long, 1 s, integration time fluorescence microscope images. (c,d) Corresponding 50 ms images taken with the custom contact image sensor. (e) Histogram of HCC1569 and LNCaP cell clusters for SNR and size. The colorbar indicated how many cell clusters fall into each bin. HCC1569 clusters appear in the upper-left and LNCaP clusters appear in the lower-right. Integration times of 50 ms and 70 ms were used for HCC1569 and LNCaP samples, respectively. (f) Histogram showing SNR per decade calculated for each HCC1569 and LNCaP cluster imaged.
Fig. 3
Fig. 3 (a) Sensitivity and specificity when using the fully-automatic image recognition algorithm. For 340 μm offset radius, the sensitivity and specificity are both 85 %. (b) Sensitivity and specificity when using the semi-automatic recognition algorithm. Missed cancer cell clusters are manually identified in the custom sensor image. The sensitivity and specificity improve when using the semi-automated algorithm and for 280 μm offset radius, both sensitivity and specificity are 92 %.
Fig. 4
Fig. 4 (a) Test setup for measuring distance variation. (b1–g1) One hundred averaged 50 ms custom sensor images taken at increasing distance from 0.65 mm to 1.8 mm in 0.25 mm intervals. The maximum SNR in each image is noted. (b2–g2) Normalized versions of the images to more clearly visualize the degradation in imaging resolution with increasing distance. (h) 1 s integration time microscope image for reference.
Fig. 5
Fig. 5 (a) Test setup for measuring the effect of different dilutions of blood. (b1–g1) One hundred averaged 50 ms custom sensor images taken for a pure PBS (clear) solution, 100X, 30X, 10X, and 3X dilutions of blood in PBS, as well as undiluted blood. The maximum SNR in each image is noted. (b2–g2) The images are normalized in order to more clearly visualize the increased noise for solutions containing more blood. (h) 1 s integration time microscope image for reference.
Fig. 6
Fig. 6 Images of human HER2+ breast cancer tissue slices. (a) Raw 75 ms fluorescence microscope image. (b) Raw 75 ms custom sensor image. (c) Fluorescence microscope image filtered with 2D Gaussian filter with standard deviation 110 μm. (d) Custom image filtered with 2D Gaussian filter with standard deviation 110 μm. (e) 5 s integration time fluorescence microscope image for reference. (f1,g1) Two regions, labeled f and g in (e), were examined using hematoxylin and eosin (H&E) as shown in order to confirm tumor margin. (f2,g2) Higher magnification fluorescence images (red) are shown overlaid on DAPI stain images (blue) of the same regions.
Fig. 7
Fig. 7 (a) Raw custom sensor image. (b) Non-linearly scaled equalized custom sensor image. (c) Regions are identified with red and orange markers. (d) Regions are overlaid on the equalized image. (e) The clusters identified in the custom sensor image appear overlaid with the clusters that are identified in the microscope image using a similar procedure to the one described in (a–d) and illustrated in (f–i). (j) An overlay of the identified clusters on the microscope image for reference.
Fig. 8
Fig. 8 The cell clusters identified in the custom sensor image (red cross) and microscope image are compared. Clusters from the microscope image are classified as true positives (green square) if they fall within the capture radius of any cluster identified in the custom sensor image. Otherwise they are considered false negatives (light blue circle).

Equations (4)

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SNR log 10 ( N ) ,
SNR = 20 log 10 ( V pixel ¯ std ( V pixel ¯ ) ) ,
CR = OR + IR ,
IR = IF I ,