Distinguishing between whole cells and cell debris using surface plasmon coupled emission

Distinguishing between whole cells and cell debris is important in microscopy, e.g., in screening of pulmonary patients for infectious tuberculosis. We propose and theoretically demonstrate that whole cells and cell debris can be distinguished from the far-field pattern of surface plasmon coupled emission (SPCE) of a fluorescently-labeled sample placed on a thin metal layer. If fluorescently-labeled whole cells are placed on the metal film, SPCE takes place simultaneously at two or more different angles and creates two or more distinct rings in the far field. By contrast, if fluorescently-labeled cell debris are placed on the metal film, SPCE takes place at only one angle and creates one ring in the far-field. We find that the angular separation of the far-field rings is sufficiently distinct to use the presence of one or more rings to distinguish between whole cells and cell debris. The proposed technique has the potential for detection without the use of a microscope. © 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement OCIS codes: (170.3880) Medical and biological imaging; (180.2520) Fluorescence microscopy. References and links 1. M. A. King, “Detection of dead cells and measurement of cell killing by flow cytometry,” J. Immunol. Meth. 243, 155–166 (2000). 2. M. Shenkin, R. Babu, and R. Maiese, “Accurate assessment of cell count and viability with a flow cytometer,” Cytometer Part B 72B, 427–432 (2007). 3. J. P. Cobb, R. S. Hotchkiss, I. E. Karl, and T. G. Buchman, “Mechanisms of cell injury and death,” British J. of Anaesthesia 77, 3–10 (1996). 4. B. Hong and Y. Zu, “Detecting circulating tumor cells: Current challenges and new trends,” Theranostics 3, 377–394 (2013). 5. R. W. Smithwick, Laboratory Manual for Acid-Fast Microscopy (2nd ed., Centers for Disease Control and Prevention, Atlanta, GA, 1976). 6. M. Wilkinson, “Rapid automatic segmentation of fluorescent and phase-contrast images of bacteria,” in Fluorescence Microscopy and Fluorescent Probes, J. Slavik, ed. (Springer, 1996). 7. M. Wallwiener, S. Riethdorf, A. D. Hartkopf, C. Modugno, J. Nees, D. Madhavan, M. R. Sprick, S. Schott, C. Domschke, I. Baccelli, B. Schönfisch, B. Burwinkel, F. Marmé, J. Heil, C. Sohn, K. Pantel, A. Trumpp, and A. Schneeweiss, “Serial enumeration of circulating tumor cells predicts treatment response and prognosis in metastatic breast cancer: a prospective study in 393 patients,” BMC Cancer 14, 512 (2014). 8. J. P. Perez, N. Ybarra, F. Chagnon,M. Serban, S. Lee, J. Seuntjens, O. Lesur, and I. E. Naqa, “Tracking of mesenchymal stemcells with fluorescence endomicroscopy imaging in radiotherapy-induced lung injury,” Scientific Reports 7, 40748 (2017). 9. P. Terho and O. Lassila, “Novel method for cell debris removal in the flow cytometric cell cycle analysis using carboxy-fluorescein diacetate succinimidyl ester,” Cytometry Part A 69A, 552–554 (2006). 10. C. Bruni, L. Ferrante, G. Koch, C. Scoglio, and G. Starace, “A stochastic model for cell debris in flow cytometry,” J. of Theoretical Biology 161, 157–174 (1993). Vol. 9, No. 4 | 1 Apr 2018 | BIOMEDICAL OPTICS EXPRESS 1977 #315551 https://doi.org/10.1364/BOE.9.001977 Journal © 2018 Received 12 Dec 2017; revised 1 Mar 2018; accepted 20 Mar 2018; published 29 Mar 2018 11. K. de Jager, S. Fickling, S. Krishnan, and T. Douglas, “Automated fluorescence microscope for tuberculosis detection,” J. Med. Devices 8, 030943 (2014). 12. F. Stefani, K. Vasilev, N. Bocchio, N. Stoyanova, and M. Kreiter, “Surface-plasmon-mediated single-molecule fluorescence through a thin metallic film,” Phys. Rev. Lett. 94, 023005 (2005). 13. J. Borejdo, Z. Gryczynski, N. Calander, P. Muthu, and I. Gryczynski, “Application of surface plasmon coupled emission to study of muscle,” Biophys. J. 91, 2626–2635 (2006). 14. Q. Liu, S.-H. Cao, W.-P. Cai, X.-Q. Liu, Y.-H. Weng, K.-X. Xie, S.-X. Huo, and Y.-Q. Li, “Surface plasmon coupled emission in micrometer-scale cells: A leap from interface to bulk targets,” J. Phys. Chem. B, 119, 2921–2927 (2015). 15. J. R. Lakowicz, J. Malicka, I. Gryczynski, and Z. Gryczynski, “Directional surface plasmon-coupled emission: a new method for high sensitivity detection,” Biochem. and Biophys. Res. Commun. 307, 435–439 (2003). 16. J. R. Lakowicz, “Radiative decay engineering 3. Surface plasmon-coupled directional emission,” Aanal. Biochem. 324, 153–169 (2004). 17. S. E. Sund, J. A. Swanson, and D. Axelrod, “Cell membrane orientation visualized by polarized total internal reflection fluorescence,” Biophys. J. 77, 2266–2283 (1999). 18. A. L. Mattheyses, S. M. Simon, and J. Z. Rappoport, “Imaging with total internal reflection fluorescence microscopy for the cell biologist,” J. Cell Science 123, 3621–3628 (2010). 19. D. S. Johnson, J. K. Jaiswal, and S. Simon, “Total internal reflection fluorescence (TIRF) microscopy illuminator for improved imaging of cell surface events,” Current Protocols in Cytometry 61, 12.29.1–12.29.19 (2012). 20. I. Gryczynski, J. Malicka, Z. Gryczynski, and J. R. Lakowicz, “Radiative decay engineering 4. Experimental studies of surface plasmon-coupled directional emission,” Anal. Biochem. 324, 170–182 (2004). 21. N. Calander, “Surface plasmon-coupled emission and Fabry-Perot resonance in the sample layer: A theoretical approach,” J. Phys. Chem. 109, 13957–13963 (2005). 22. S. Z. Uddin, M. R. Tanvir, and M. A. Talukder, “A proposal and an analysis of an enhanced surface plasmon coupled emission structure for single molecule detection,” J. Appl. Phys. 119, 204701 (2016). 23. R. S. Sathish, Y. Kostov, and G. Rao, “Low-cost plastic plasmonic substrates for operation in aqueous environments,” Appl. Spectroscopy 64, 1234–1237 (2010). 24. X.-M. Wan, R. Gao, D.-F. Lu, and Z.-M. Qi, “Self-referenced directional enhanced Raman scattering using plasmon waveguide resonance for surface and bulk sensing,” Appl. Phys. Lett. 112, 041906 (2018). 25. K. Toma, M. Vala, P. Adam, J. Homola, W. Knoll, and J. Dostálek, “Compact surface plasmon-enhanced fluorescence biochip,” Opt. Express 21, 10121–10132 (2013). 26. K. Balaa, V. Devauges, Y. Goulam, V. Studer, S. L.-Fort, and Emmanuel Fort, “Live cell imaging with surface plasmon-mediated fluorescence microscopy,” In Proc. European Conference on Biomedical Optics, 736010 (2009). 27. I. Gryczynski, J. Malicka, K. Nowaczyk, Z. Gryczynski, and J. R. Lakowicz, “Waveguide-modulated surface plasmon-coupled emission of Nile blue in poly(vinyl alcohol) thin films,” Thin Solid Films 510, 15–20 (2006). 28. L. Novotny and B. Hecht, Principles of Nano-Optics (Cambridge University Press, 2012). 29. J. R. Lakowicz, Principles of Fluorescence Spectroscopy (Springer, 2007). 30. R. M. Anthony, A. H. J. Kolk, S. Kuijper, P. R. Klaster, “Light emitting diodes for auramine O fluorescence microscopic screening of Mycobacterium tuberculosis,” Int. J. Tuberculosis and Lung Disease 10, 1060–1062 (2006). 31. T. Yoshino, K. Takai, R. Negishi, T. Saeki, H. Kanbara, Y. Kikuhara, T. Matsunaga, and T. Tanaka, “Rapid imaging and detection of circulating tumor cells using a wide-field fluorescence imaging system,” Anal. Chimica Acta 969, 1–7 (2017). 32. D. Axelrod, “Total internal reflection fluorescence microscopy in cell biology,” Traffic 2 764–774, (2001). 33. A. S. Kristoffersen, S. R. Erga, B. Hamre, and Ø. Frette, “Testing fluorescence lifetime standards using two-photon excitation and time-domain instrumentation: Rhodamine B, coumarin 6 and lucifer yellow,” J. Fluorescence 24, 1015–1024 (2014). 34. S. A. Maier, Plasmonics: Fundamentals and Applications (Springer Science & Business Media, 2007). 35. D. N. Breslauer, R. N. Maamari, N. A. Switz, W. A. Lam, D. A. Fletcher, “Mobile phone based clinical microscopy for global health applications,” PLoS One 4, e6320 (2009). 36. W. Choi, C. F.-Yen, K. Badizadegan, S. Oh, N. Lue, R. R. Dasari, and M. S. Feld, “Tomographic phase microscopy,” Nat. Methods 4, 717–719 (2007). 37. P. Y. Liu, L. K. Chin, W. Ser, H. F. Chen, C.-M. Hsieh, C.-H. Lee, K.-B. Sung, T. C. Ayi, P. H. Yap, B. Liedberg, K. Wang, T. Bourouina, and Y. L.-Wang, “Cell refractive index for cell biology and disease diagnosis: past, present and future,” Lab on a Chip 16, 634–644 (2016). 38. K. Toma, H. Kano, and A. Offenhäusser, “Label-free measurement of cell-electrode cleft gap distance with high spatial resolution surface plasmon microscopy,” ACS Nano 8, 12612–12619 (2014). 39. J. Chang, P. Arbeláez, N. Switz, C. Reber, A. Tapley, J. L. Davis, A. Cattamanchi, D. Fletcher, and J. Malik, “Automated tuberculosis diagnosis using fluorescence images from a mobile microscope,” Med. Image Comput. and Comput.-Assist. Intervention 15, 345–352 (2012). 40. G. M. Cook, M. Berney, S. Gebhard, M. Heinemann, R. A. Cox, O. Danilchanka, and M. Niederweis, “Physiology of mycobacteria,” Adv. Microb. Phys. 55, 81–182, 318–319 (2009). 41. D. Gingell, O. Heavens, and J. Mellor, “General electromagnetic theory of total internal reflection fluorescence: The quantitative basis for mapping cell-substratum topography,” J. Cell Science 87, 677–693 (1987). 42. A. Anantharam, B. Onoa, R. H. Edwards, R. W. Holz, and D. Axelrod, “Localized topological changes of the plasma Vol. 9, No. 4 | 1 Apr 2018 | BIOMEDICAL OPTICS EXPRESS 1978