Abstract

Optical imaging of tissue autofluorescence has the potential to provide rapid label-free screening and detection of surface tumors for clinical applications, including when combined with endoscopy. Quantitative imaging of intensity-based contrast is notoriously difficult and spectrally resolved imaging does not always provide sufficient contrast. We demonstrate that fluorescence lifetime imaging (FLIM) applied to intrinsic tissue autofluorescence can directly contrast a range of surface tissue tumors, including in gastrointestinal tissues, using compact, clinically deployable instrumentation achieving wide-field fluorescence lifetime images of unprecedented clarity. Statistically significant contrast is observed between cancerous and healthy colon tissue for FLIM with excitation at 355 nm. To illustrate the clinical potential, wide-field fluorescence lifetime images of unstained ex vivo tissue have been acquired at near video rate, which is an important step towards real-time FLIM for diagnostic and interoperative imaging, including for screening and image-guided biopsy applications.

©2010 Optical Society of America

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2009 (6)

W. L. Curvers, F. J. C. van den Broek, J. B. Reitsma, E. Dekker, and J. J. Bergman, “Systematic review of narrow-band imaging for the detection and differentiation of abnormalities in the esophagus and stomach (with video),” Gastrointest. Endosc. 69(2), 307–317 (2009).
[Crossref] [PubMed]

F. J. C. van den Broek, J. B. Reitsma, W. L. Curvers, P. Fockens, and E. Dekker, “Systematic review of narrow-band imaging for the detection and differentiation of neoplastic and nonneoplastic lesions in the colon (with videos),” Gastrointest. Endosc. 69(1), 124–135 (2009).
[Crossref] [PubMed]

G. W. Falk, “Autofluorescence endoscopy,” Gastrointest. Endosc. Clin. N. Am. 19(2), 209–220 (2009).
[Crossref] [PubMed]

F. J. C. van den Broek, P. Fockens, S. Van Eeden, M. A. Kara, J. C. H. Hardwick, J. B. Reitsma, and E. Dekker, “Clinical evaluation of endoscopic trimodal imaging for the detection and differentiation of colonic polyps,” Clin. Gastroenterol. Hepatol. 7(3), 288–295 (2009).
[Crossref] [PubMed]

E. Dimitrow, I. Riemann, A. Ehlers, M. J. Koehler, J. Norgauer, P. Elsner, K. König, and M. Kaatz, “Spectral fluorescence lifetime detection and selective melanin imaging by multiphoton laser tomography for melanoma diagnosis,” Exp. Dermatol. 18(6), 509–515 (2009).
[Crossref] [PubMed]

Y. Sun, J. Phipps, D. S. Elson, H. Stoy, S. Tinling, J. Meier, B. Poirier, F. S. Chuang, D. G. Farwell, and L. Marcu, “Fluorescence lifetime imaging microscopy: in vivo application to diagnosis of oral carcinoma,” Opt. Lett. 34(13), 2081–2083 (2009).
[Crossref] [PubMed]

2008 (5)

N. P. Galletly, J. McGinty, C. Dunsby, F. Teixeira, J. Requejo-Isidro, I. Munro, D. S. Elson, M. A. A. Neil, A. C. Chu, P. M. W. French, and G. W. Stamp, “Fluorescence lifetime imaging distinguishes basal cell carcinoma from surrounding uninvolved skin,” Br. J. Dermatol. 159(1), 152–161 (2008).
[Crossref] [PubMed]

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[Crossref] [PubMed]

T. Matsuda, Y. Saito, K. I. Fu, T. Uraoka, N. Kobayashi, T. Nakajima, H. Ikehara, Y. Mashimo, T. Shimoda, Y. Murakami, A. Parra-Blanco, T. Fujimori, and D. Saito, “Does autofluorescence imaging videoendoscopy system improve the colonoscopic polyp detection rate?--a pilot study,” Am. J. Gastroenterol. 103(8), 1926–1932 (2008).
[Crossref] [PubMed]

F. J. C. van den Broek, P. Fockens, S. van Eeden, J. B. Reitsma, J. C. H. Hardwick, P. C. F. Stokkers, and E. Dekker, “Endoscopic tri-modal imaging for surveillance in ulcerative colitis: randomised comparison of high-resolution endoscopy and autofluorescence imaging for neoplasia detection; and evaluation of narrow-band imaging for classification of lesions,” Gut 57(8), 1083–1089 (2008).
[Crossref] [PubMed]

M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13(4), 044030 (2008).
[Crossref] [PubMed]

2007 (4)

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. W. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
[Crossref] [PubMed]

S. R. Kantelhardt, J. Leppert, J. Krajewski, N. Petkus, E. Reusche, V. M. Tronnier, G. Hüttmann, and A. Giese, “Imaging of brain and brain tumor specimens by time-resolved multiphoton excitation microscopy ex vivo,” Neuro-oncol. 9(2), 103–112 (2007).
[Crossref] [PubMed]

R. Cicchi, D. Massi, S. Sestini, P. Carli, V. De Giorgi, T. Lotti, and F. S. Pavone, “Multidimensional non-linear laser imaging of Basal Cell Carcinoma,” Opt. Express 15(16), 10135–10148 (2007).
[Crossref] [PubMed]

2005 (5)

I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005).
[Crossref] [PubMed]

H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (2005).
[Crossref] [PubMed]

M. P. L. Bard, A. Amelink, M. Skurichina, M. den Bakker, S. A. Burgers, J. P. van Meerbeeck, R. P. W. Duin, J. G. J. V. Aerts, H. C. Hoogsteden, and H. J. C. M. Sterenborg, “Improving the specificity of fluorescence bronchoscopy for the analysis of neoplastic lesions of the bronchial tree by combination with optical spectroscopy: preliminary communication,” Lung Cancer 47(1), 41–47 (2005).
[Crossref] [PubMed]

H. M. Chen, C. P. Chiang, C. You, T. C. Hsiao, and C. Y. Wang, “Time-resolved autofluorescence spectroscopy for classifying normal and premalignant oral tissues,” Lasers Surg. Med. 37(1), 37–45 (2005).
[Crossref] [PubMed]

A. Esposito, T. Oggier, H. C. Gerritsen, F. Lustenberger, and F. S. Wouters, “All-solid-state lock-in imaging for wide-field fluorescence lifetime sensing,” Opt. Express 13(24), 9812–9821 (2005).
[Crossref] [PubMed]

2004 (2)

D. S. Elson, I. Munro, J. Requejo-Isidro, J. McGinty, C. Dunsby, N. Galletly, G. W. Stamp, M. A. A. Neil, M. J. Lever, P. A. Kellett, A. Dymoke-Bradshaw, J. Hares, and P. M. W. French, “Real-time time-domain fluorescence lifetime imaging including single-shot acquisition with a segmented optical image intensifier,” N. J. Phys. 6, 180 (2004).
[Crossref]

L. Marcu, J. A. Jo, P. V. Butte, W. H. Yong, B. K. Pikul, K. L. Black, and R. C. Thompson, “Fluorescence lifetime spectroscopy of glioblastoma multiforme,” Photochem. Photobiol. 80(1), 98–103 (2004).
[Crossref] [PubMed]

2003 (4)

K. Gono, K. Yamazaki, N. Doguchi, T. Nonami, T. Obi, M. Yamaguchi, N. Ohyama, H. Machida, Y. Sano, S. Yoshida, Y. Hamamoto, and T. Endo, “Endoscopic observation of tissue by narrowband illumination,” Opt. Rev. 10(4), 211–215 (2003).
[Crossref]

A. V. Agronskaia, L. Tertoolen, and H. C. Gerritsen, “High frame rate fluorescence lifetime imaging,” J. Phys. D Appl. Phys. 36(14), 1655–1662 (2003).
[Crossref]

P. J. Tadrous, J. Siegel, P. M. W. French, S. Shousha, N. Lalani, and G. W. H. Stamp, “Fluorescence lifetime imaging of unstained tissues: early results in human breast cancer,” J. Pathol. 199(3), 309–317 (2003).
[Crossref] [PubMed]

J. Siegel, D. S. Elson, S. E. D. Webb, K. C. Lee, A. Vlandas, G. L. Gambaruto, S. Lévêque-Fort, M. J. Lever, P. J. Tadrous, G. W. H. Stamp, A. L. Wallace, A. Sandison, T. F. Watson, F. Alvarez, and P. M. W. French, “Studying biological tissue with fluorescence lifetime imaging: microscopy, endoscopy, and complex decay profiles,” Appl. Opt. 42(16), 2995–3004 (2003).
[Crossref] [PubMed]

2002 (4)

R. S. Dacosta, B. C. Wilson, and N. E. Marcon, “New optical technologies for earlier endoscopic diagnosis of premalignant gastrointestinal lesions,” J. Gastroenterol. Hepatol. 17(Suppl), S85–S104 (2002).
[Crossref] [PubMed]

G. M. Palmer, C. L. Marshek, K. M. Vrotsos, and N. Ramanujam, “Optimal methods for fluorescence and diffuse reflectance measurements of tissue biopsy samples,” Lasers Surg. Med. 30(3), 191–200 (2002).
[Crossref] [PubMed]

R. Cubeddu, D. Comelli, C. D'Andrea, P. Taroni, and G. Valentini, “Time-resolved fluorescence imaging in biology and medicine,” J. Phys. D Appl. Phys. 35(9), R61–R76 (2002).
[Crossref]

K. Sokolov, M. Follen, and R. Richards-Kortum, “Optical spectroscopy for detection of neoplasia,” Curr. Opin. Chem. Biol. 6(5), 651–658 (2002).
[Crossref] [PubMed]

2001 (1)

K. C. Lee, J. Siegel, S. E. D. Webb, S. Lévêque-Fort, M. J. Cole, R. Jones, K. Dowling, M. J. Lever, and P. M. W. French, “Application of the stretched exponential function to fluorescence lifetime imaging,” Biophys. J. 81(3), 1265–1274 (2001).
[Crossref] [PubMed]

1999 (4)

J. Mizeret, T. Stepinac, M. Hansroul, A. Studzinski, H. van den Bergh, and G. Wagnières, “Instrumentation for real-time fluorescence lifetime imaging in endoscopy,” Rev. Sci. Instrum. 70(12), 4689–4701 (1999).
[Crossref]

T. D. Wang, J. M. Crawford, M. S. Feld, Y. Wang, I. Itzkan, and J. Van Dam, “In vivo identification of colonic dysplasia using fluorescence endoscopic imaging,” Gastrointest. Endosc. 49(4), 447–455 (1999).
[Crossref] [PubMed]

T. Glanzmann, J.-P. Ballini, H. van den Bergh, and G. Wagnières, “Time-resolved spectrofluorometer for clinical tissue characterization during endoscopy,” Rev. Sci. Instrum. 70(10), 4067–4077 (1999).
[Crossref]

P. I. H. Bastiaens and A. Squire, “Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell,” Trends Cell Biol. 9(2), 48–52 (1999).
[Crossref] [PubMed]

1998 (3)

M. A. Mycek, K. T. Schomacker, and N. S. Nishioka, “Colonic polyp differentiation using time-resolved autofluorescence spectroscopy,” Gastrointest. Endosc. 48(4), 390–394 (1998).
[Crossref] [PubMed]

K. Dowling, M. J. Dayel, M. J. Lever, P. M. W. French, J. D. Hares, and A. K. L. Dymoke-Bradshaw, “Fluorescence lifetime imaging with picosecond resolution for biomedical applications,” Opt. Lett. 23(10), 810–812 (1998).
[Crossref] [PubMed]

G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol. 68(5), 603–632 (1998).
[PubMed]

1997 (2)

I. J. Bigio and J. R. Mourant, “Ultraviolet and visible spectroscopies for tissue diagnostics: fluorescence spectroscopy and elastic-scattering spectroscopy,” Phys. Med. Biol. 42(5), 803–814 (1997).
[Crossref] [PubMed]

J. Mizeret, G. Wagnières, T. Stepinac, and H. Bergh, “Endoscopic tissue characterization by frequency-domain fluorescence lifetime imaging (FD-FLIM),” Lasers Med. Sci. 12(3), 209–217 (1997).
[Crossref]

1996 (1)

R. Richards-Kortum and E. Sevick-Muraca, “Quantitative optical spectroscopy for tissue diagnosis,” Annu. Rev. Phys. Chem. 47(1), 555–606 (1996).
[Crossref] [PubMed]

1995 (1)

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

1992 (2)

H. Schneckenburger and K. Konig, “Fluorescence Decay Kinetics and Imaging of Nad(P)H and Flavins as Metabolic Indicators,” Opt. Eng. 31(7), 1447–1451 (1992).
[Crossref]

A. Pradhan, B. B. Das, K. M. Yoo, J. Cleary, R. Prudente, E. Celmer, and R. R. Alfano, “Time-resolved UV photoexcited fluorescence kinetics from malignant and non-malignant human breast tissues,” Lasers in the Life Sciences 4, 225–234 (1992).

1991 (1)

S. Andersson-Engels, A. Elner, J. Johansson, S.-E. Karlsson, L. G. Salford, L.-G. Strömblad, K. Svanberg, and S. Svanberg, “Clinical Recording of Laser-induced Fluorescence Spectra for Evaluation of Tumour Demarcation Feasibility in Selected Clinical Specialities,” Lasers Med. Sci. 6(4), 415–424 (1991).
[Crossref]

1986 (1)

D. B. Tata, M. Foresti, J. Cordero, P. Tomashefsky, M. A. Alfano, and R. R. Alfano, “Fluorescence polarization spectroscopy and time-resolved fluorescence kinetics of native cancerous and normal rat kidney tissues,” Biophys. J. 50(3), 463–469 (1986).
[Crossref] [PubMed]

Aerts, J. G. J. V.

M. P. L. Bard, A. Amelink, M. Skurichina, M. den Bakker, S. A. Burgers, J. P. van Meerbeeck, R. P. W. Duin, J. G. J. V. Aerts, H. C. Hoogsteden, and H. J. C. M. Sterenborg, “Improving the specificity of fluorescence bronchoscopy for the analysis of neoplastic lesions of the bronchial tree by combination with optical spectroscopy: preliminary communication,” Lung Cancer 47(1), 41–47 (2005).
[Crossref] [PubMed]

Agronskaia, A. V.

A. V. Agronskaia, L. Tertoolen, and H. C. Gerritsen, “High frame rate fluorescence lifetime imaging,” J. Phys. D Appl. Phys. 36(14), 1655–1662 (2003).
[Crossref]

Alfano, M. A.

D. B. Tata, M. Foresti, J. Cordero, P. Tomashefsky, M. A. Alfano, and R. R. Alfano, “Fluorescence polarization spectroscopy and time-resolved fluorescence kinetics of native cancerous and normal rat kidney tissues,” Biophys. J. 50(3), 463–469 (1986).
[Crossref] [PubMed]

Alfano, R. R.

A. Pradhan, B. B. Das, K. M. Yoo, J. Cleary, R. Prudente, E. Celmer, and R. R. Alfano, “Time-resolved UV photoexcited fluorescence kinetics from malignant and non-malignant human breast tissues,” Lasers in the Life Sciences 4, 225–234 (1992).

D. B. Tata, M. Foresti, J. Cordero, P. Tomashefsky, M. A. Alfano, and R. R. Alfano, “Fluorescence polarization spectroscopy and time-resolved fluorescence kinetics of native cancerous and normal rat kidney tissues,” Biophys. J. 50(3), 463–469 (1986).
[Crossref] [PubMed]

Alvarez, F.

Amelink, A.

M. P. L. Bard, A. Amelink, M. Skurichina, M. den Bakker, S. A. Burgers, J. P. van Meerbeeck, R. P. W. Duin, J. G. J. V. Aerts, H. C. Hoogsteden, and H. J. C. M. Sterenborg, “Improving the specificity of fluorescence bronchoscopy for the analysis of neoplastic lesions of the bronchial tree by combination with optical spectroscopy: preliminary communication,” Lung Cancer 47(1), 41–47 (2005).
[Crossref] [PubMed]

Anand, P.

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. W. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
[Crossref] [PubMed]

Anand, U.

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. W. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
[Crossref] [PubMed]

Anders, A.

M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13(4), 044030 (2008).
[Crossref] [PubMed]

Andersson-Engels, S.

S. Andersson-Engels, A. Elner, J. Johansson, S.-E. Karlsson, L. G. Salford, L.-G. Strömblad, K. Svanberg, and S. Svanberg, “Clinical Recording of Laser-induced Fluorescence Spectra for Evaluation of Tumour Demarcation Feasibility in Selected Clinical Specialities,” Lasers Med. Sci. 6(4), 415–424 (1991).
[Crossref]

Babai, F.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

Balassy, A.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

Ballini, J.-P.

T. Glanzmann, J.-P. Ballini, H. van den Bergh, and G. Wagnières, “Time-resolved spectrofluorometer for clinical tissue characterization during endoscopy,” Rev. Sci. Instrum. 70(10), 4067–4077 (1999).
[Crossref]

Bard, M. P. L.

M. P. L. Bard, A. Amelink, M. Skurichina, M. den Bakker, S. A. Burgers, J. P. van Meerbeeck, R. P. W. Duin, J. G. J. V. Aerts, H. C. Hoogsteden, and H. J. C. M. Sterenborg, “Improving the specificity of fluorescence bronchoscopy for the analysis of neoplastic lesions of the bronchial tree by combination with optical spectroscopy: preliminary communication,” Lung Cancer 47(1), 41–47 (2005).
[Crossref] [PubMed]

Bastiaens, P. I. H.

P. I. H. Bastiaens and A. Squire, “Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell,” Trends Cell Biol. 9(2), 48–52 (1999).
[Crossref] [PubMed]

Benham, C. D.

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. W. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
[Crossref] [PubMed]

Bergh, H.

J. Mizeret, G. Wagnières, T. Stepinac, and H. Bergh, “Endoscopic tissue characterization by frequency-domain fluorescence lifetime imaging (FD-FLIM),” Lasers Med. Sci. 12(3), 209–217 (1997).
[Crossref]

Bergman, J. J.

W. L. Curvers, F. J. C. van den Broek, J. B. Reitsma, E. Dekker, and J. J. Bergman, “Systematic review of narrow-band imaging for the detection and differentiation of abnormalities in the esophagus and stomach (with video),” Gastrointest. Endosc. 69(2), 307–317 (2009).
[Crossref] [PubMed]

Bigio, I. J.

I. J. Bigio and J. R. Mourant, “Ultraviolet and visible spectroscopies for tissue diagnostics: fluorescence spectroscopy and elastic-scattering spectroscopy,” Phys. Med. Biol. 42(5), 803–814 (1997).
[Crossref] [PubMed]

Black, K. L.

L. Marcu, J. A. Jo, P. V. Butte, W. H. Yong, B. K. Pikul, K. L. Black, and R. C. Thompson, “Fluorescence lifetime spectroscopy of glioblastoma multiforme,” Photochem. Photobiol. 80(1), 98–103 (2004).
[Crossref] [PubMed]

Blanchard, L.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

Burgers, S. A.

M. P. L. Bard, A. Amelink, M. Skurichina, M. den Bakker, S. A. Burgers, J. P. van Meerbeeck, R. P. W. Duin, J. G. J. V. Aerts, H. C. Hoogsteden, and H. J. C. M. Sterenborg, “Improving the specificity of fluorescence bronchoscopy for the analysis of neoplastic lesions of the bronchial tree by combination with optical spectroscopy: preliminary communication,” Lung Cancer 47(1), 41–47 (2005).
[Crossref] [PubMed]

Butte, P. V.

L. Marcu, J. A. Jo, P. V. Butte, W. H. Yong, B. K. Pikul, K. L. Black, and R. C. Thompson, “Fluorescence lifetime spectroscopy of glioblastoma multiforme,” Photochem. Photobiol. 80(1), 98–103 (2004).
[Crossref] [PubMed]

Carli, P.

Celmer, E.

A. Pradhan, B. B. Das, K. M. Yoo, J. Cleary, R. Prudente, E. Celmer, and R. R. Alfano, “Time-resolved UV photoexcited fluorescence kinetics from malignant and non-malignant human breast tissues,” Lasers in the Life Sciences 4, 225–234 (1992).

Chen, H. M.

H. M. Chen, C. P. Chiang, C. You, T. C. Hsiao, and C. Y. Wang, “Time-resolved autofluorescence spectroscopy for classifying normal and premalignant oral tissues,” Lasers Surg. Med. 37(1), 37–45 (2005).
[Crossref] [PubMed]

Chiang, C. P.

H. M. Chen, C. P. Chiang, C. You, T. C. Hsiao, and C. Y. Wang, “Time-resolved autofluorescence spectroscopy for classifying normal and premalignant oral tissues,” Lasers Surg. Med. 37(1), 37–45 (2005).
[Crossref] [PubMed]

Chu, A. C.

N. P. Galletly, J. McGinty, C. Dunsby, F. Teixeira, J. Requejo-Isidro, I. Munro, D. S. Elson, M. A. A. Neil, A. C. Chu, P. M. W. French, and G. W. Stamp, “Fluorescence lifetime imaging distinguishes basal cell carcinoma from surrounding uninvolved skin,” Br. J. Dermatol. 159(1), 152–161 (2008).
[Crossref] [PubMed]

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. W. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
[Crossref] [PubMed]

Chuang, F. S.

Cicchi, R.

Cleary, J.

A. Pradhan, B. B. Das, K. M. Yoo, J. Cleary, R. Prudente, E. Celmer, and R. R. Alfano, “Time-resolved UV photoexcited fluorescence kinetics from malignant and non-malignant human breast tissues,” Lasers in the Life Sciences 4, 225–234 (1992).

Cole, M. J.

K. C. Lee, J. Siegel, S. E. D. Webb, S. Lévêque-Fort, M. J. Cole, R. Jones, K. Dowling, M. J. Lever, and P. M. W. French, “Application of the stretched exponential function to fluorescence lifetime imaging,” Biophys. J. 81(3), 1265–1274 (2001).
[Crossref] [PubMed]

Comelli, D.

R. Cubeddu, D. Comelli, C. D'Andrea, P. Taroni, and G. Valentini, “Time-resolved fluorescence imaging in biology and medicine,” J. Phys. D Appl. Phys. 35(9), R61–R76 (2002).
[Crossref]

Cordero, J.

D. B. Tata, M. Foresti, J. Cordero, P. Tomashefsky, M. A. Alfano, and R. R. Alfano, “Fluorescence polarization spectroscopy and time-resolved fluorescence kinetics of native cancerous and normal rat kidney tissues,” Biophys. J. 50(3), 463–469 (1986).
[Crossref] [PubMed]

Crawford, J. M.

T. D. Wang, J. M. Crawford, M. S. Feld, Y. Wang, I. Itzkan, and J. Van Dam, “In vivo identification of colonic dysplasia using fluorescence endoscopic imaging,” Gastrointest. Endosc. 49(4), 447–455 (1999).
[Crossref] [PubMed]

Cubeddu, R.

R. Cubeddu, D. Comelli, C. D'Andrea, P. Taroni, and G. Valentini, “Time-resolved fluorescence imaging in biology and medicine,” J. Phys. D Appl. Phys. 35(9), R61–R76 (2002).
[Crossref]

Curvers, W. L.

F. J. C. van den Broek, J. B. Reitsma, W. L. Curvers, P. Fockens, and E. Dekker, “Systematic review of narrow-band imaging for the detection and differentiation of neoplastic and nonneoplastic lesions in the colon (with videos),” Gastrointest. Endosc. 69(1), 124–135 (2009).
[Crossref] [PubMed]

W. L. Curvers, F. J. C. van den Broek, J. B. Reitsma, E. Dekker, and J. J. Bergman, “Systematic review of narrow-band imaging for the detection and differentiation of abnormalities in the esophagus and stomach (with video),” Gastrointest. Endosc. 69(2), 307–317 (2009).
[Crossref] [PubMed]

Dacosta, R. S.

R. S. Dacosta, B. C. Wilson, and N. E. Marcon, “New optical technologies for earlier endoscopic diagnosis of premalignant gastrointestinal lesions,” J. Gastroenterol. Hepatol. 17(Suppl), S85–S104 (2002).
[Crossref] [PubMed]

D'Andrea, C.

R. Cubeddu, D. Comelli, C. D'Andrea, P. Taroni, and G. Valentini, “Time-resolved fluorescence imaging in biology and medicine,” J. Phys. D Appl. Phys. 35(9), R61–R76 (2002).
[Crossref]

Das, B. B.

A. Pradhan, B. B. Das, K. M. Yoo, J. Cleary, R. Prudente, E. Celmer, and R. R. Alfano, “Time-resolved UV photoexcited fluorescence kinetics from malignant and non-malignant human breast tissues,” Lasers in the Life Sciences 4, 225–234 (1992).

Dayel, M. J.

De Beule, P. A. A.

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. W. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
[Crossref] [PubMed]

De Giorgi, V.

Dekker, E.

F. J. C. van den Broek, P. Fockens, S. Van Eeden, M. A. Kara, J. C. H. Hardwick, J. B. Reitsma, and E. Dekker, “Clinical evaluation of endoscopic trimodal imaging for the detection and differentiation of colonic polyps,” Clin. Gastroenterol. Hepatol. 7(3), 288–295 (2009).
[Crossref] [PubMed]

W. L. Curvers, F. J. C. van den Broek, J. B. Reitsma, E. Dekker, and J. J. Bergman, “Systematic review of narrow-band imaging for the detection and differentiation of abnormalities in the esophagus and stomach (with video),” Gastrointest. Endosc. 69(2), 307–317 (2009).
[Crossref] [PubMed]

F. J. C. van den Broek, J. B. Reitsma, W. L. Curvers, P. Fockens, and E. Dekker, “Systematic review of narrow-band imaging for the detection and differentiation of neoplastic and nonneoplastic lesions in the colon (with videos),” Gastrointest. Endosc. 69(1), 124–135 (2009).
[Crossref] [PubMed]

F. J. C. van den Broek, P. Fockens, S. van Eeden, J. B. Reitsma, J. C. H. Hardwick, P. C. F. Stokkers, and E. Dekker, “Endoscopic tri-modal imaging for surveillance in ulcerative colitis: randomised comparison of high-resolution endoscopy and autofluorescence imaging for neoplasia detection; and evaluation of narrow-band imaging for classification of lesions,” Gut 57(8), 1083–1089 (2008).
[Crossref] [PubMed]

den Bakker, M.

M. P. L. Bard, A. Amelink, M. Skurichina, M. den Bakker, S. A. Burgers, J. P. van Meerbeeck, R. P. W. Duin, J. G. J. V. Aerts, H. C. Hoogsteden, and H. J. C. M. Sterenborg, “Improving the specificity of fluorescence bronchoscopy for the analysis of neoplastic lesions of the bronchial tree by combination with optical spectroscopy: preliminary communication,” Lung Cancer 47(1), 41–47 (2005).
[Crossref] [PubMed]

Dimitrow, E.

E. Dimitrow, I. Riemann, A. Ehlers, M. J. Koehler, J. Norgauer, P. Elsner, K. König, and M. Kaatz, “Spectral fluorescence lifetime detection and selective melanin imaging by multiphoton laser tomography for melanoma diagnosis,” Exp. Dermatol. 18(6), 509–515 (2009).
[Crossref] [PubMed]

Doguchi, N.

K. Gono, K. Yamazaki, N. Doguchi, T. Nonami, T. Obi, M. Yamaguchi, N. Ohyama, H. Machida, Y. Sano, S. Yoshida, Y. Hamamoto, and T. Endo, “Endoscopic observation of tissue by narrowband illumination,” Opt. Rev. 10(4), 211–215 (2003).
[Crossref]

Dowling, K.

K. C. Lee, J. Siegel, S. E. D. Webb, S. Lévêque-Fort, M. J. Cole, R. Jones, K. Dowling, M. J. Lever, and P. M. W. French, “Application of the stretched exponential function to fluorescence lifetime imaging,” Biophys. J. 81(3), 1265–1274 (2001).
[Crossref] [PubMed]

K. Dowling, M. J. Dayel, M. J. Lever, P. M. W. French, J. D. Hares, and A. K. L. Dymoke-Bradshaw, “Fluorescence lifetime imaging with picosecond resolution for biomedical applications,” Opt. Lett. 23(10), 810–812 (1998).
[Crossref] [PubMed]

Duin, R. P. W.

M. P. L. Bard, A. Amelink, M. Skurichina, M. den Bakker, S. A. Burgers, J. P. van Meerbeeck, R. P. W. Duin, J. G. J. V. Aerts, H. C. Hoogsteden, and H. J. C. M. Sterenborg, “Improving the specificity of fluorescence bronchoscopy for the analysis of neoplastic lesions of the bronchial tree by combination with optical spectroscopy: preliminary communication,” Lung Cancer 47(1), 41–47 (2005).
[Crossref] [PubMed]

Dunsby, C.

N. P. Galletly, J. McGinty, C. Dunsby, F. Teixeira, J. Requejo-Isidro, I. Munro, D. S. Elson, M. A. A. Neil, A. C. Chu, P. M. W. French, and G. W. Stamp, “Fluorescence lifetime imaging distinguishes basal cell carcinoma from surrounding uninvolved skin,” Br. J. Dermatol. 159(1), 152–161 (2008).
[Crossref] [PubMed]

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. W. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
[Crossref] [PubMed]

I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005).
[Crossref] [PubMed]

D. S. Elson, I. Munro, J. Requejo-Isidro, J. McGinty, C. Dunsby, N. Galletly, G. W. Stamp, M. A. A. Neil, M. J. Lever, P. A. Kellett, A. Dymoke-Bradshaw, J. Hares, and P. M. W. French, “Real-time time-domain fluorescence lifetime imaging including single-shot acquisition with a segmented optical image intensifier,” N. J. Phys. 6, 180 (2004).
[Crossref]

Durocher, G.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

Dymoke-Bradshaw, A.

D. S. Elson, I. Munro, J. Requejo-Isidro, J. McGinty, C. Dunsby, N. Galletly, G. W. Stamp, M. A. A. Neil, M. J. Lever, P. A. Kellett, A. Dymoke-Bradshaw, J. Hares, and P. M. W. French, “Real-time time-domain fluorescence lifetime imaging including single-shot acquisition with a segmented optical image intensifier,” N. J. Phys. 6, 180 (2004).
[Crossref]

Dymoke-Bradshaw, A. K. L.

Ehlers, A.

E. Dimitrow, I. Riemann, A. Ehlers, M. J. Koehler, J. Norgauer, P. Elsner, K. König, and M. Kaatz, “Spectral fluorescence lifetime detection and selective melanin imaging by multiphoton laser tomography for melanoma diagnosis,” Exp. Dermatol. 18(6), 509–515 (2009).
[Crossref] [PubMed]

Eickhoff, J.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

Eliceiri, K. W.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
[Crossref] [PubMed]

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

Elner, A.

S. Andersson-Engels, A. Elner, J. Johansson, S.-E. Karlsson, L. G. Salford, L.-G. Strömblad, K. Svanberg, and S. Svanberg, “Clinical Recording of Laser-induced Fluorescence Spectra for Evaluation of Tumour Demarcation Feasibility in Selected Clinical Specialities,” Lasers Med. Sci. 6(4), 415–424 (1991).
[Crossref]

Elsner, P.

E. Dimitrow, I. Riemann, A. Ehlers, M. J. Koehler, J. Norgauer, P. Elsner, K. König, and M. Kaatz, “Spectral fluorescence lifetime detection and selective melanin imaging by multiphoton laser tomography for melanoma diagnosis,” Exp. Dermatol. 18(6), 509–515 (2009).
[Crossref] [PubMed]

Elson, D. S.

Y. Sun, J. Phipps, D. S. Elson, H. Stoy, S. Tinling, J. Meier, B. Poirier, F. S. Chuang, D. G. Farwell, and L. Marcu, “Fluorescence lifetime imaging microscopy: in vivo application to diagnosis of oral carcinoma,” Opt. Lett. 34(13), 2081–2083 (2009).
[Crossref] [PubMed]

N. P. Galletly, J. McGinty, C. Dunsby, F. Teixeira, J. Requejo-Isidro, I. Munro, D. S. Elson, M. A. A. Neil, A. C. Chu, P. M. W. French, and G. W. Stamp, “Fluorescence lifetime imaging distinguishes basal cell carcinoma from surrounding uninvolved skin,” Br. J. Dermatol. 159(1), 152–161 (2008).
[Crossref] [PubMed]

I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005).
[Crossref] [PubMed]

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T. D. Wang, J. M. Crawford, M. S. Feld, Y. Wang, I. Itzkan, and J. Van Dam, “In vivo identification of colonic dysplasia using fluorescence endoscopic imaging,” Gastrointest. Endosc. 49(4), 447–455 (1999).
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F. J. C. van den Broek, P. Fockens, S. van Eeden, J. B. Reitsma, J. C. H. Hardwick, P. C. F. Stokkers, and E. Dekker, “Endoscopic tri-modal imaging for surveillance in ulcerative colitis: randomised comparison of high-resolution endoscopy and autofluorescence imaging for neoplasia detection; and evaluation of narrow-band imaging for classification of lesions,” Gut 57(8), 1083–1089 (2008).
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N. P. Galletly, J. McGinty, C. Dunsby, F. Teixeira, J. Requejo-Isidro, I. Munro, D. S. Elson, M. A. A. Neil, A. C. Chu, P. M. W. French, and G. W. Stamp, “Fluorescence lifetime imaging distinguishes basal cell carcinoma from surrounding uninvolved skin,” Br. J. Dermatol. 159(1), 152–161 (2008).
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P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. W. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
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D. S. Elson, I. Munro, J. Requejo-Isidro, J. McGinty, C. Dunsby, N. Galletly, G. W. Stamp, M. A. A. Neil, M. J. Lever, P. A. Kellett, A. Dymoke-Bradshaw, J. Hares, and P. M. W. French, “Real-time time-domain fluorescence lifetime imaging including single-shot acquisition with a segmented optical image intensifier,” N. J. Phys. 6, 180 (2004).
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P. J. Tadrous, J. Siegel, P. M. W. French, S. Shousha, N. Lalani, and G. W. H. Stamp, “Fluorescence lifetime imaging of unstained tissues: early results in human breast cancer,” J. Pathol. 199(3), 309–317 (2003).
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J. Siegel, D. S. Elson, S. E. D. Webb, K. C. Lee, A. Vlandas, G. L. Gambaruto, S. Lévêque-Fort, M. J. Lever, P. J. Tadrous, G. W. H. Stamp, A. L. Wallace, A. Sandison, T. F. Watson, F. Alvarez, and P. M. W. French, “Studying biological tissue with fluorescence lifetime imaging: microscopy, endoscopy, and complex decay profiles,” Appl. Opt. 42(16), 2995–3004 (2003).
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K. C. Lee, J. Siegel, S. E. D. Webb, S. Lévêque-Fort, M. J. Cole, R. Jones, K. Dowling, M. J. Lever, and P. M. W. French, “Application of the stretched exponential function to fluorescence lifetime imaging,” Biophys. J. 81(3), 1265–1274 (2001).
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K. Dowling, M. J. Dayel, M. J. Lever, P. M. W. French, J. D. Hares, and A. K. L. Dymoke-Bradshaw, “Fluorescence lifetime imaging with picosecond resolution for biomedical applications,” Opt. Lett. 23(10), 810–812 (1998).
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[Crossref] [PubMed]

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. W. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
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Gendron-Fitzpatrick, A.

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F. J. C. van den Broek, P. Fockens, S. van Eeden, J. B. Reitsma, J. C. H. Hardwick, P. C. F. Stokkers, and E. Dekker, “Endoscopic tri-modal imaging for surveillance in ulcerative colitis: randomised comparison of high-resolution endoscopy and autofluorescence imaging for neoplasia detection; and evaluation of narrow-band imaging for classification of lesions,” Gut 57(8), 1083–1089 (2008).
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D. S. Elson, I. Munro, J. Requejo-Isidro, J. McGinty, C. Dunsby, N. Galletly, G. W. Stamp, M. A. A. Neil, M. J. Lever, P. A. Kellett, A. Dymoke-Bradshaw, J. Hares, and P. M. W. French, “Real-time time-domain fluorescence lifetime imaging including single-shot acquisition with a segmented optical image intensifier,” N. J. Phys. 6, 180 (2004).
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Heikal, A. A.

H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (2005).
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M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13(4), 044030 (2008).
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T. Matsuda, Y. Saito, K. I. Fu, T. Uraoka, N. Kobayashi, T. Nakajima, H. Ikehara, Y. Mashimo, T. Shimoda, Y. Murakami, A. Parra-Blanco, T. Fujimori, and D. Saito, “Does autofluorescence imaging videoendoscopy system improve the colonoscopic polyp detection rate?--a pilot study,” Am. J. Gastroenterol. 103(8), 1926–1932 (2008).
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P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
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T. D. Wang, J. M. Crawford, M. S. Feld, Y. Wang, I. Itzkan, and J. Van Dam, “In vivo identification of colonic dysplasia using fluorescence endoscopic imaging,” Gastrointest. Endosc. 49(4), 447–455 (1999).
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S. R. Kantelhardt, J. Leppert, J. Krajewski, N. Petkus, E. Reusche, V. M. Tronnier, G. Hüttmann, and A. Giese, “Imaging of brain and brain tumor specimens by time-resolved multiphoton excitation microscopy ex vivo,” Neuro-oncol. 9(2), 103–112 (2007).
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F. J. C. van den Broek, P. Fockens, S. Van Eeden, M. A. Kara, J. C. H. Hardwick, J. B. Reitsma, and E. Dekker, “Clinical evaluation of endoscopic trimodal imaging for the detection and differentiation of colonic polyps,” Clin. Gastroenterol. Hepatol. 7(3), 288–295 (2009).
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S. Andersson-Engels, A. Elner, J. Johansson, S.-E. Karlsson, L. G. Salford, L.-G. Strömblad, K. Svanberg, and S. Svanberg, “Clinical Recording of Laser-induced Fluorescence Spectra for Evaluation of Tumour Demarcation Feasibility in Selected Clinical Specialities,” Lasers Med. Sci. 6(4), 415–424 (1991).
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H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (2005).
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P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
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D. S. Elson, I. Munro, J. Requejo-Isidro, J. McGinty, C. Dunsby, N. Galletly, G. W. Stamp, M. A. A. Neil, M. J. Lever, P. A. Kellett, A. Dymoke-Bradshaw, J. Hares, and P. M. W. French, “Real-time time-domain fluorescence lifetime imaging including single-shot acquisition with a segmented optical image intensifier,” N. J. Phys. 6, 180 (2004).
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P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
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T. Matsuda, Y. Saito, K. I. Fu, T. Uraoka, N. Kobayashi, T. Nakajima, H. Ikehara, Y. Mashimo, T. Shimoda, Y. Murakami, A. Parra-Blanco, T. Fujimori, and D. Saito, “Does autofluorescence imaging videoendoscopy system improve the colonoscopic polyp detection rate?--a pilot study,” Am. J. Gastroenterol. 103(8), 1926–1932 (2008).
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E. Dimitrow, I. Riemann, A. Ehlers, M. J. Koehler, J. Norgauer, P. Elsner, K. König, and M. Kaatz, “Spectral fluorescence lifetime detection and selective melanin imaging by multiphoton laser tomography for melanoma diagnosis,” Exp. Dermatol. 18(6), 509–515 (2009).
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S. R. Kantelhardt, J. Leppert, J. Krajewski, N. Petkus, E. Reusche, V. M. Tronnier, G. Hüttmann, and A. Giese, “Imaging of brain and brain tumor specimens by time-resolved multiphoton excitation microscopy ex vivo,” Neuro-oncol. 9(2), 103–112 (2007).
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M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13(4), 044030 (2008).
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P. J. Tadrous, J. Siegel, P. M. W. French, S. Shousha, N. Lalani, and G. W. H. Stamp, “Fluorescence lifetime imaging of unstained tissues: early results in human breast cancer,” J. Pathol. 199(3), 309–317 (2003).
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I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005).
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Leppert, J.

S. R. Kantelhardt, J. Leppert, J. Krajewski, N. Petkus, E. Reusche, V. M. Tronnier, G. Hüttmann, and A. Giese, “Imaging of brain and brain tumor specimens by time-resolved multiphoton excitation microscopy ex vivo,” Neuro-oncol. 9(2), 103–112 (2007).
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Lever, M. J.

I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005).
[Crossref] [PubMed]

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[Crossref]

J. Siegel, D. S. Elson, S. E. D. Webb, K. C. Lee, A. Vlandas, G. L. Gambaruto, S. Lévêque-Fort, M. J. Lever, P. J. Tadrous, G. W. H. Stamp, A. L. Wallace, A. Sandison, T. F. Watson, F. Alvarez, and P. M. W. French, “Studying biological tissue with fluorescence lifetime imaging: microscopy, endoscopy, and complex decay profiles,” Appl. Opt. 42(16), 2995–3004 (2003).
[Crossref] [PubMed]

K. C. Lee, J. Siegel, S. E. D. Webb, S. Lévêque-Fort, M. J. Cole, R. Jones, K. Dowling, M. J. Lever, and P. M. W. French, “Application of the stretched exponential function to fluorescence lifetime imaging,” Biophys. J. 81(3), 1265–1274 (2001).
[Crossref] [PubMed]

K. Dowling, M. J. Dayel, M. J. Lever, P. M. W. French, J. D. Hares, and A. K. L. Dymoke-Bradshaw, “Fluorescence lifetime imaging with picosecond resolution for biomedical applications,” Opt. Lett. 23(10), 810–812 (1998).
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Lustenberger, F.

Machida, H.

K. Gono, K. Yamazaki, N. Doguchi, T. Nonami, T. Obi, M. Yamaguchi, N. Ohyama, H. Machida, Y. Sano, S. Yoshida, Y. Hamamoto, and T. Endo, “Endoscopic observation of tissue by narrowband illumination,” Opt. Rev. 10(4), 211–215 (2003).
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S. R. Kantelhardt, J. Leppert, J. Krajewski, N. Petkus, E. Reusche, V. M. Tronnier, G. Hüttmann, and A. Giese, “Imaging of brain and brain tumor specimens by time-resolved multiphoton excitation microscopy ex vivo,” Neuro-oncol. 9(2), 103–112 (2007).
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P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
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M. P. L. Bard, A. Amelink, M. Skurichina, M. den Bakker, S. A. Burgers, J. P. van Meerbeeck, R. P. W. Duin, J. G. J. V. Aerts, H. C. Hoogsteden, and H. J. C. M. Sterenborg, “Improving the specificity of fluorescence bronchoscopy for the analysis of neoplastic lesions of the bronchial tree by combination with optical spectroscopy: preliminary communication,” Lung Cancer 47(1), 41–47 (2005).
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F. J. C. van den Broek, P. Fockens, S. van Eeden, J. B. Reitsma, J. C. H. Hardwick, P. C. F. Stokkers, and E. Dekker, “Endoscopic tri-modal imaging for surveillance in ulcerative colitis: randomised comparison of high-resolution endoscopy and autofluorescence imaging for neoplasia detection; and evaluation of narrow-band imaging for classification of lesions,” Gut 57(8), 1083–1089 (2008).
[Crossref] [PubMed]

Stoy, H.

Strömblad, L.-G.

S. Andersson-Engels, A. Elner, J. Johansson, S.-E. Karlsson, L. G. Salford, L.-G. Strömblad, K. Svanberg, and S. Svanberg, “Clinical Recording of Laser-induced Fluorescence Spectra for Evaluation of Tumour Demarcation Feasibility in Selected Clinical Specialities,” Lasers Med. Sci. 6(4), 415–424 (1991).
[Crossref]

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J. Mizeret, T. Stepinac, M. Hansroul, A. Studzinski, H. van den Bergh, and G. Wagnières, “Instrumentation for real-time fluorescence lifetime imaging in endoscopy,” Rev. Sci. Instrum. 70(12), 4689–4701 (1999).
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Svanberg, K.

S. Andersson-Engels, A. Elner, J. Johansson, S.-E. Karlsson, L. G. Salford, L.-G. Strömblad, K. Svanberg, and S. Svanberg, “Clinical Recording of Laser-induced Fluorescence Spectra for Evaluation of Tumour Demarcation Feasibility in Selected Clinical Specialities,” Lasers Med. Sci. 6(4), 415–424 (1991).
[Crossref]

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S. Andersson-Engels, A. Elner, J. Johansson, S.-E. Karlsson, L. G. Salford, L.-G. Strömblad, K. Svanberg, and S. Svanberg, “Clinical Recording of Laser-induced Fluorescence Spectra for Evaluation of Tumour Demarcation Feasibility in Selected Clinical Specialities,” Lasers Med. Sci. 6(4), 415–424 (1991).
[Crossref]

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Taroni, P.

R. Cubeddu, D. Comelli, C. D'Andrea, P. Taroni, and G. Valentini, “Time-resolved fluorescence imaging in biology and medicine,” J. Phys. D Appl. Phys. 35(9), R61–R76 (2002).
[Crossref]

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D. B. Tata, M. Foresti, J. Cordero, P. Tomashefsky, M. A. Alfano, and R. R. Alfano, “Fluorescence polarization spectroscopy and time-resolved fluorescence kinetics of native cancerous and normal rat kidney tissues,” Biophys. J. 50(3), 463–469 (1986).
[Crossref] [PubMed]

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N. P. Galletly, J. McGinty, C. Dunsby, F. Teixeira, J. Requejo-Isidro, I. Munro, D. S. Elson, M. A. A. Neil, A. C. Chu, P. M. W. French, and G. W. Stamp, “Fluorescence lifetime imaging distinguishes basal cell carcinoma from surrounding uninvolved skin,” Br. J. Dermatol. 159(1), 152–161 (2008).
[Crossref] [PubMed]

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A. V. Agronskaia, L. Tertoolen, and H. C. Gerritsen, “High frame rate fluorescence lifetime imaging,” J. Phys. D Appl. Phys. 36(14), 1655–1662 (2003).
[Crossref]

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L. Marcu, J. A. Jo, P. V. Butte, W. H. Yong, B. K. Pikul, K. L. Black, and R. C. Thompson, “Fluorescence lifetime spectroscopy of glioblastoma multiforme,” Photochem. Photobiol. 80(1), 98–103 (2004).
[Crossref] [PubMed]

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D. B. Tata, M. Foresti, J. Cordero, P. Tomashefsky, M. A. Alfano, and R. R. Alfano, “Fluorescence polarization spectroscopy and time-resolved fluorescence kinetics of native cancerous and normal rat kidney tissues,” Biophys. J. 50(3), 463–469 (1986).
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M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13(4), 044030 (2008).
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S. R. Kantelhardt, J. Leppert, J. Krajewski, N. Petkus, E. Reusche, V. M. Tronnier, G. Hüttmann, and A. Giese, “Imaging of brain and brain tumor specimens by time-resolved multiphoton excitation microscopy ex vivo,” Neuro-oncol. 9(2), 103–112 (2007).
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T. Matsuda, Y. Saito, K. I. Fu, T. Uraoka, N. Kobayashi, T. Nakajima, H. Ikehara, Y. Mashimo, T. Shimoda, Y. Murakami, A. Parra-Blanco, T. Fujimori, and D. Saito, “Does autofluorescence imaging videoendoscopy system improve the colonoscopic polyp detection rate?--a pilot study,” Am. J. Gastroenterol. 103(8), 1926–1932 (2008).
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T. D. Wang, J. M. Crawford, M. S. Feld, Y. Wang, I. Itzkan, and J. Van Dam, “In vivo identification of colonic dysplasia using fluorescence endoscopic imaging,” Gastrointest. Endosc. 49(4), 447–455 (1999).
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T. Glanzmann, J.-P. Ballini, H. van den Bergh, and G. Wagnières, “Time-resolved spectrofluorometer for clinical tissue characterization during endoscopy,” Rev. Sci. Instrum. 70(10), 4067–4077 (1999).
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F. J. C. van den Broek, P. Fockens, S. van Eeden, J. B. Reitsma, J. C. H. Hardwick, P. C. F. Stokkers, and E. Dekker, “Endoscopic tri-modal imaging for surveillance in ulcerative colitis: randomised comparison of high-resolution endoscopy and autofluorescence imaging for neoplasia detection; and evaluation of narrow-band imaging for classification of lesions,” Gut 57(8), 1083–1089 (2008).
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F. J. C. van den Broek, P. Fockens, S. Van Eeden, M. A. Kara, J. C. H. Hardwick, J. B. Reitsma, and E. Dekker, “Clinical evaluation of endoscopic trimodal imaging for the detection and differentiation of colonic polyps,” Clin. Gastroenterol. Hepatol. 7(3), 288–295 (2009).
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F. J. C. van den Broek, P. Fockens, S. van Eeden, J. B. Reitsma, J. C. H. Hardwick, P. C. F. Stokkers, and E. Dekker, “Endoscopic tri-modal imaging for surveillance in ulcerative colitis: randomised comparison of high-resolution endoscopy and autofluorescence imaging for neoplasia detection; and evaluation of narrow-band imaging for classification of lesions,” Gut 57(8), 1083–1089 (2008).
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M. P. L. Bard, A. Amelink, M. Skurichina, M. den Bakker, S. A. Burgers, J. P. van Meerbeeck, R. P. W. Duin, J. G. J. V. Aerts, H. C. Hoogsteden, and H. J. C. M. Sterenborg, “Improving the specificity of fluorescence bronchoscopy for the analysis of neoplastic lesions of the bronchial tree by combination with optical spectroscopy: preliminary communication,” Lung Cancer 47(1), 41–47 (2005).
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Vrotsos, K. M.

G. M. Palmer, C. L. Marshek, K. M. Vrotsos, and N. Ramanujam, “Optimal methods for fluorescence and diffuse reflectance measurements of tissue biopsy samples,” Lasers Surg. Med. 30(3), 191–200 (2002).
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J. Mizeret, T. Stepinac, M. Hansroul, A. Studzinski, H. van den Bergh, and G. Wagnières, “Instrumentation for real-time fluorescence lifetime imaging in endoscopy,” Rev. Sci. Instrum. 70(12), 4689–4701 (1999).
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T. Glanzmann, J.-P. Ballini, H. van den Bergh, and G. Wagnières, “Time-resolved spectrofluorometer for clinical tissue characterization during endoscopy,” Rev. Sci. Instrum. 70(10), 4067–4077 (1999).
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J. Mizeret, G. Wagnières, T. Stepinac, and H. Bergh, “Endoscopic tissue characterization by frequency-domain fluorescence lifetime imaging (FD-FLIM),” Lasers Med. Sci. 12(3), 209–217 (1997).
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Wang, C. Y.

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T. D. Wang, J. M. Crawford, M. S. Feld, Y. Wang, I. Itzkan, and J. Van Dam, “In vivo identification of colonic dysplasia using fluorescence endoscopic imaging,” Gastrointest. Endosc. 49(4), 447–455 (1999).
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T. D. Wang, J. M. Crawford, M. S. Feld, Y. Wang, I. Itzkan, and J. Van Dam, “In vivo identification of colonic dysplasia using fluorescence endoscopic imaging,” Gastrointest. Endosc. 49(4), 447–455 (1999).
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Webb, S. E. D.

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H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (2005).
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G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol. 68(5), 603–632 (1998).
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P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, “Collagen density promotes mammary tumor initiation and progression,” BMC Med. 6(1), 11 (2008).
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L. Marcu, J. A. Jo, P. V. Butte, W. H. Yong, B. K. Pikul, K. L. Black, and R. C. Thompson, “Fluorescence lifetime spectroscopy of glioblastoma multiforme,” Photochem. Photobiol. 80(1), 98–103 (2004).
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A. Pradhan, B. B. Das, K. M. Yoo, J. Cleary, R. Prudente, E. Celmer, and R. R. Alfano, “Time-resolved UV photoexcited fluorescence kinetics from malignant and non-malignant human breast tissues,” Lasers in the Life Sciences 4, 225–234 (1992).

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K. Gono, K. Yamazaki, N. Doguchi, T. Nonami, T. Obi, M. Yamaguchi, N. Ohyama, H. Machida, Y. Sano, S. Yoshida, Y. Hamamoto, and T. Endo, “Endoscopic observation of tissue by narrowband illumination,” Opt. Rev. 10(4), 211–215 (2003).
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N. P. Galletly, J. McGinty, C. Dunsby, F. Teixeira, J. Requejo-Isidro, I. Munro, D. S. Elson, M. A. A. Neil, A. C. Chu, P. M. W. French, and G. W. Stamp, “Fluorescence lifetime imaging distinguishes basal cell carcinoma from surrounding uninvolved skin,” Br. J. Dermatol. 159(1), 152–161 (2008).
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E. Dimitrow, I. Riemann, A. Ehlers, M. J. Koehler, J. Norgauer, P. Elsner, K. König, and M. Kaatz, “Spectral fluorescence lifetime detection and selective melanin imaging by multiphoton laser tomography for melanoma diagnosis,” Exp. Dermatol. 18(6), 509–515 (2009).
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F. J. C. van den Broek, J. B. Reitsma, W. L. Curvers, P. Fockens, and E. Dekker, “Systematic review of narrow-band imaging for the detection and differentiation of neoplastic and nonneoplastic lesions in the colon (with videos),” Gastrointest. Endosc. 69(1), 124–135 (2009).
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F. J. C. van den Broek, P. Fockens, S. van Eeden, J. B. Reitsma, J. C. H. Hardwick, P. C. F. Stokkers, and E. Dekker, “Endoscopic tri-modal imaging for surveillance in ulcerative colitis: randomised comparison of high-resolution endoscopy and autofluorescence imaging for neoplasia detection; and evaluation of narrow-band imaging for classification of lesions,” Gut 57(8), 1083–1089 (2008).
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H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (2005).
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R. S. Dacosta, B. C. Wilson, and N. E. Marcon, “New optical technologies for earlier endoscopic diagnosis of premalignant gastrointestinal lesions,” J. Gastroenterol. Hepatol. 17(Suppl), S85–S104 (2002).
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A. V. Agronskaia, L. Tertoolen, and H. C. Gerritsen, “High frame rate fluorescence lifetime imaging,” J. Phys. D Appl. Phys. 36(14), 1655–1662 (2003).
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J. Mizeret, G. Wagnières, T. Stepinac, and H. Bergh, “Endoscopic tissue characterization by frequency-domain fluorescence lifetime imaging (FD-FLIM),” Lasers Med. Sci. 12(3), 209–217 (1997).
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G. M. Palmer, C. L. Marshek, K. M. Vrotsos, and N. Ramanujam, “Optimal methods for fluorescence and diffuse reflectance measurements of tissue biopsy samples,” Lasers Surg. Med. 30(3), 191–200 (2002).
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M. P. L. Bard, A. Amelink, M. Skurichina, M. den Bakker, S. A. Burgers, J. P. van Meerbeeck, R. P. W. Duin, J. G. J. V. Aerts, H. C. Hoogsteden, and H. J. C. M. Sterenborg, “Improving the specificity of fluorescence bronchoscopy for the analysis of neoplastic lesions of the bronchial tree by combination with optical spectroscopy: preliminary communication,” Lung Cancer 47(1), 41–47 (2005).
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Supplementary Material (1)

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Figures (7)

Fig. 1
Fig. 1

Equipment set-up for FLIM. The tissue sample is illuminated using a pulsed UV laser source carried via a fibre-optic cable to a diffuser. The emitted autofluorescence is imaged onto the GOI (which acts as a very fast shutter and an intensifier to amplify the weak fluorescence signal) and recorded by the CCD camera. Several time-gated images are recorded at different delays with respect to the excitation pulse. The resulting decay data is then analysed by fitting an exponential decay to the decay for each pixel in the field of view to generate a false-colour lifetime map of the image.

Fig. 2
Fig. 2

FLIM of a fresh hemicolectomy specimen containing a moderately differentiated colonic adenocarcinoma. (a) White light image of the macroscopic specimen (area of fluorescence imaging outlined). Scale bar (white) represents 2 cm. (b) H&E stained histological sections of the tumour. (c) Fluorescence integrated intensity image. (d, e) Intensity-weighted FLIM images. In (d) the lifetime is represented by a continuous spectrum colour scale while in (e) it is represented by a binary colour scale. (f) Lifetime distribution histograms calculated from the FLIM data.

Fig. 3
Fig. 3

FLIM of a fresh partial gastrectomy specimen containing a moderately differentiated intestinal-type adenocarcinoma. (a) White light image of the macroscopic specimen (area of fluorescence imaging outlined). (b) Fluorescence integrated intensity image. Scale bar (white) represents 1 cm. (c) Intensity-weighted false-colour FLIM image (lifetime represented by a continuous spectrum colour scale). (d) Intensity-weighted false-colour FLIM image (lifetime represented by a discrete binary colour scale). (e) Lifetime histogram from the normal and cancerous regions of interest.

Fig. 4
Fig. 4

FLIM of a freshly resected bladder containing a moderately differentiated squamous cell carcinoma. (a) White light image of the macroscopic specimen (area of fluorescence imaging outlined). (b) Fluorescence integrated intensity image. Scale bar (white) represents 1 cm. (c) Intensity-weighted false-colour FLIM image. (d) Histogram showing fluorescence lifetime distributions from normal and cancerous regions of interest.

Fig. 5
Fig. 5

(a) Graph showing difference in mean fluorescence intensity between the lesion ROI and normal tissue ROI for 18 colonic resections. (b) Plot of the mean difference in fluorescence lifetime between the lesion and normal ROIs. (c) AUC analysis of the fluorescence intensity data. (d) AUC analysis of the fluorescence lifetime data. Specimens 1-16 colonic tumours, 17-18 serrated adenomas.

Fig. 6
Fig. 6

FLIM of unfixed pancreas containing an area of pancreatic cancer. (a) Standard acquisition (25 time gates; decay curve fitted to data using an iterative WNLLS algorithm; update rate ~0.1 Hz). Scale bar (white) represents 5 mm. (b) Rapid lifetime determination acquisition (Media 1) update rate 7.7 Hz. (c) Histogram of lifetime values from (A) showing lifetimes for the cancer and normal regions of interest.

Fig. 7
Fig. 7

FLIM of an unfixed liver containing metastatic colorectal carcinoma and an area of radiofrequency ablation damage. (a) White light image of the specimen (area of fluorescence imaging indicated by rectangle). Scale bar (white) represents 2 cm. (b) Fluorescence intensity image. (c) FLIM map obtained with a single exponential fit. (d) Stretched exponential FLIM map and (e) heterogeneity images obtained with a stretched exponential fit. (f) Lifetime histogram generated from the stretched exponential fit demonstrating contrast between the three areas of the sample.

Tables (1)

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Table 1 Summary of fluorescence data from the 16 imaged adenocarcinomas. Errors are the standard deviation of the values across the 16 specimens. p-values were calculated using a Wilcoxon sign-rank test

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