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Endoscopic Fluorescence Lifetime Imaging for In Vivo Intraoperative Diagnosis of Oral Carcinoma

Published online by Cambridge University Press:  23 May 2013

Yinghua Sun ,
Jennifer E. Phipps ,
Jeremy Meier ,
Nisa Hatami ,
Brian Poirier ,
Daniel S. Elson ,
D. Gregory Farwell  and
Laura Marcu
Yinghua Sun
Affiliation:
Department of Biomedical Engineering, University of California, Davis, CA 95616, USA
Jennifer E. Phipps
Affiliation:
Department of Biomedical Engineering, University of California, Davis, CA 95616, USA
Jeremy Meier
Affiliation:
Department of Otolaryngology-Head and Neck Surgery, University of California Davis, Sacramento, CA 95817, USA
Nisa Hatami
Affiliation:
Department of Biomedical Engineering, University of California, Davis, CA 95616, USA
Brian Poirier
Affiliation:
Department of Pathology, University of California Davis, Sacramento, CA 95817, USA
Daniel S. Elson
Affiliation:
Department of Surgery, Hamlyn Centre, Imperial College London, London SW7 2AZ, UK
D. Gregory Farwell
Affiliation:
Department of Otolaryngology-Head and Neck Surgery, University of California Davis, Sacramento, CA 95817, USA
Laura Marcu*
Affiliation:
Department of Biomedical Engineering, University of California, Davis, CA 95616, USA
*
*Corresponding author. E-mail: lmarcu@ucdavis.edu
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Abstract

A clinically compatible fluorescence lifetime imaging microscopy (FLIM) system was developed. The system was applied to intraoperative in vivo imaging of head and neck squamous cell carcinoma (HNSCC). The endoscopic FLIM prototype integrates a gated (down to 0.2 ns) intensifier imaging system and a fiber-bundle endoscope (0.5-mm-diameter, 10,000 fibers with a gradient index lens objective 0.5 NA, 4-mm field of view), which provides intraoperative access to the surgical field. Tissue autofluorescence was induced by a pulsed laser (337 nm, 700 ps pulse width) and collected in the 460 ± 25 nm spectral band. FLIM experiments were conducted at 26 anatomic sites in ten patients during head and neck cancer surgery. HNSCC exhibited a weaker florescence intensity (~50% less) when compared with healthy tissue and a shorter average lifetime (τHNSCC = 1.21 ± 0.04 ns) than the surrounding normal tissue (τN = 1.49 ± 0.06 ns). This work demonstrates the potential of FLIM for label-free head and neck tumor demarcation during intraoperative surgical procedures.

Keywords

fluorescence lifetime imaging microscopy (FLIM)tissue autofluorescenceendoscopyhead and neck squamous cell carcinoma (HNSCC)cancer diagnosisintraoperative diagnosis
Type
Omaha Imaging Symposium
Information
Microscopy and Microanalysis , Volume 19 , Issue 4 , August 2013 , pp. 791 - 798
Copyright
Copyright © Microscopy Society of America 2013 

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References

Andersson-Engels, S., Berg, R., Persson, A. & Svanberg, S. (1993). Multispectral tissue characterization with time-resolved detection of diffusely scattered white-light. Opt Lett 18, 1697–1699.CrossRefGoogle ScholarPubMed
Andersson-Engels, S., Johansson, J., Stenram, U., Svanberg, K. & Svanberg, S. (1990). Malignant tumour and atherosclerotic plaque diagnosis using laser induced fluorescence. IEEE J Quantum Electron 26, 2207–2217.CrossRefGoogle Scholar
Cubeddu, R., Comelli, D., D'Andrea, C., Taroni, P. & Valentini, G. (2002). Time-resolved fluorescence imaging in biology and medicine. J Phys D-Appl Phys 35, R61–R76.CrossRefGoogle Scholar
De Veld, D.C.G., Witjes, M.J.H., Sterenborg, H. & Roodenburg, J.L.N. (2005). The status of in vivo autofluorescence spectroscopy and imaging for oral oncology. Oral Oncol 41, 117–131.CrossRefGoogle ScholarPubMed
Elson, D.S., Jo, J.A. & Marcu, L. (2007). Miniaturized side-viewing imaging probe for fluorescence lifetime imaging (FLIM): Validation with fluorescence dyes, tissue structural proteins and tissue specimens. New J Phys 9, 127.CrossRefGoogle ScholarPubMed
Elson, D., Requejo-Isidro, J., Munro, I., Reavell, F., Siegel, J., Suhling, K., Tadrous, P., Benninger, R., Lanigan, P., McGinty, J., Talbot, C., Treanor, B., Webb, S., Sandison, A., Wallace, A., Davis, D., Lever, J., Neil, M., Phillips, D., Stamp, G. & French, P. (2004). Time-domain fluorescence lifetime imaging applied to biological tissue. Photoch Photobio Sci 3, 795–801.CrossRefGoogle ScholarPubMed
Jo, J.A., Fang, Q., Papaioannou, T., Baker, J.D., Dorafshar, A.H., Reil, T., Qiao, J.H., Fishbein, M.C., Freischlag, J.A. & Marcu, L. (2006). Laguerre-based method for analysis of time-resolved fluorescence data: Application to in-vivo characterization and diagnosis of atherosclerotic lesions. J Biomed Opt 11, 021004. CrossRefGoogle ScholarPubMed
Lakowicz, J.R. (2006). Principles of Fluorescence Spectroscopy, 3rd ed. New York: Kluwer Academic/Plenum Publishers.CrossRefGoogle Scholar
Liu, J., Sun, Y., Qi, J.Y. & Marcu, L. (2012). A novel method for fast and robust estimation of fluorescence decay dynamics using constrained least-squares deconvolution with Laguerre expansion. Phys Med Biol 57, 843–865.CrossRefGoogle Scholar
Marcu, L. (2012). Fluorescence lifetime techniques in medical applications. Ann Biomed Eng 40, 304–331.CrossRefGoogle ScholarPubMed
Marcu, L., Jo, J.A., Fang, Q., Papaioannou, T., Reil, T., Qiao, J.-H., Baker, J.D., Freischlag, J.A. & Fishbein, M.C. (2009). Detection of rupture-prone atherosclerotic plaques by time-resolved laser-induced fluorescence spectroscopy. Atherosclerosis 204, 156–164.CrossRefGoogle ScholarPubMed
Pavlova, I., Weber, C.R., Schwarz, R.A., Williams, M.D., Gillenwater, A.M. & Richards-Kortum, R. (2009). Fluorescence spectroscopy of oral tissue: Monte Carlo modeling with site-specific tissue properties. J Biomed Opt 14, 014009. CrossRefGoogle ScholarPubMed
Phipps, J., Sun, Y., Saroufeem, R., Hatami, N., Fishbein, M.C. & Marcu, L. (2011). Fluorescence lifetime imaging for the characterization of the biochemical composition of atherosclerotic plaques. J Biomed Opt 16, 096018. CrossRefGoogle ScholarPubMed
Ramanujam, N. (2000). Fluorescence spectroscopy in vivo . In Encyclopedia of Analytical Chemistry, Meyers, R. A. (Ed.), pp. 20–56. Chichester: John Wiley and Sons Ltd. Google Scholar
Richards-Kortum, R., Mitchell, M.F., Ramanujam, N., Mahadevan, A. & Thomsen, S. (1994). In vivo fluorescence spectroscopy: Potential for non-invasive, automated diagnosis of cervical intraepithelial neoplasia and use as a surrogate endpoint biomarker. J Cell Biochem Suppl 19, 111–119.Google ScholarPubMed
Richards-Kortum, R. & Sevick-Muraca, E.M. (1996). Quantitative optical spectroscopy for tissue diagnosis. Annu Rev Phys Chem 47, 555–606.CrossRefGoogle ScholarPubMed
Schwarz, R.A., Gao, W., Weber, C.R., Kurachi, C., Lee, J.J., El-Naggar, A.K., Richards-Kortum, R. & Gillenwater, A.M. (2009). Noninvasive evaluation of oral lesions using depth-sensitive optical spectroscopy. Cancer 115, 1669–1679.CrossRefGoogle ScholarPubMed
Skala, M.C., Riching, K.M., Gendron-Fitzpatrick, A., Eickhoff, J., Eliceiri, K.W., White, J.G. & Ramanujam, N. (2007). In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia. Proc Natl Acad Sci USA 104, 19494–19499.CrossRefGoogle ScholarPubMed
Sun, Y., Chaudhari, A.J., Lam, M., Xie, H., Yankelevich, D.R., Phipps, J., Liu, J., Fishbein, M.C., Cannata, J.M., Shung, K.K. & Marcu, L. (2011a). Multimodal characterization of compositional, structural and functional features of human atherosclerotic plaques. Biomed Opt Express 2, 2288–2298.CrossRefGoogle ScholarPubMed
Sun, Y., Phipps, J., Elson, D.S., Stoy, H., Tinling, S., Meier, J., Poirier, B., Chuang, F.S., Farwell, D.G. & Marcu, L. (2009). Fluorescence lifetime imaging microscopy: In vivo application to diagnosis of oral carcinoma. Opt Lett 34, 2081–2083.CrossRefGoogle ScholarPubMed
Sun, Y., Sun, Y., Stephens, D., Xie, H., Phipps, J., Saroufeem, R., Southard, J., Elson, D.S. & Marcu, L. (2011b). Dynamic tissue analysis using time- and wavelength-resolved fluorescence spectroscopy for atherosclerosis diagnosis. Opt Express 19, 3890–3901.CrossRefGoogle ScholarPubMed
Sun, Y., Xie, H.T., Liu, J., Lam, M., Chaudhari, A.J., Zhou, F.F., Bec, J., Yankelevich, D.R., Dobbie, A., Tinling, S.L., Gandour-Edwards, R.F., Monsky, W.L., Farwell, D.G. & Marcu, L. (2012). In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma. J Biomed Opt 17, 116003. CrossRefGoogle ScholarPubMed