Abstract

Combined non-linear imaging techniques were used to deeply image human ex-vivo fresh biopsies of bladder as well as to discriminate between healthy bladder mucosa and carcinoma in situ. Morphological examination by two-photon excited fluorescence and second-harmonic generation has shown a good agreement with corresponding common routine histology performed on the same samples. Tumor cells appeared slightly different in shape and with a smaller cellular-to-nuclear dimension ratio with respect to corresponding normal cells. Further differences between the two tissue types were found in both spectral emission and fluorescence lifetime distribution by performing temporal- and spectral- resolved analysis of fluorescence. This method may represent a promising tool to be used in a multi-photon endoscope, in a confocal endoscope or in a spectroscopic probe for in-vivo optical diagnosis of bladder cancer.

© 2010 OSA

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2009 (4)

W. W. Chin, P. S. P. Thong, R. Bhuvaneswari, K. C. Soo, P. W. S. Heng, and M. Olivo, “In-vivo optical detection of cancer using chlorin e6-polyvinylpyrrolidone induced fluorescence imaging and spectroscopy,” BMC Med. Imaging 9(1), 1–8 (2009).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

S. M. Zhuo, J. X. Chen, T. Luo, X. S. Jiang, and S. S. Xie, “Multiphoton microscopy of unstained bladder mucosa based on two-photon excited autofluorescence and second-harmonic generation,” Laser Phys. Lett. 6(1), 80–83 (2009).
[CrossRef]

R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol. 23(5), 861–867 (2009).
[CrossRef] [PubMed]

2008 (9)

M. E. Llewellyn, R. P. J. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454(7205), 784–788 (2008).
[PubMed]

Z. Yuan, Z. Wang, R. Pan, J. Liu, H. Cohen, and Y. Pan, “High-resolution imaging diagnosis and staging of bladder cancer: comparison between optical coherence tomography and high-frequency ultrasound,” J. Biomed. Opt. 13(5), 054007 (2008).
[CrossRef] [PubMed]

B. Hermes, F. Spöler, A. Naami, J. Bornemann, M. Först, J. Grosse, G. Jakse, and R. Knüchel, “Visualization of the basement membrane zone of the bladder by optical coherence tomography: feasibility of noninvasive evaluation of tumor invasion,” Urology 72(3), 677–681 (2008).
[CrossRef] [PubMed]

J. C. Kah, W. K. Lau, P. H. Tan, C. J. Sheppard, and M. Olivo, “Endoscopic image analysis of photosensitizer fluorescence as a promising noninvasive approach for pathological grading of bladder cancer in situ,” J. Biomed. Opt. 13(5), 054022 (2008).
[CrossRef] [PubMed]

E. L. Larsen, L. L. Randeberg, O. A. Gederaas, C. J. Arum, A. Hjelde, C. M. Zhao, D. Chen, H. E. Krokan, and L. O. Svaasand, “Monitoring of hexyl 5-aminolevulinate-induced photodynamic therapy in rat bladder cancer by optical spectroscopy,” J. Biomed. Opt. 13(4), 044031 (2008).
[CrossRef] [PubMed]

S. Berrahmoune, N. Fotinos, L. Bezdetnaya, N. Lange, J. C. Guedenet, F. Guillemin, and M. A. D’Hallewin, “Analysis of differential PDT effect in rat bladder tumor models according to concentrations of intravesical hexyl-aminolevulinate,” Photochem. Photobiol. Sci. 7(9), 1018–1024 (2008).
[CrossRef] [PubMed]

R. Cicchi, S. Sestini, V. De Giorgi, D. Massi, T. Lotti, and F. S. Pavone, “Non-linear laser imaging of skin lesions,” J. Biophoton. 1(1), 62–73 (2008).
[CrossRef]

J. Paoli, M. Smedh, A. M. Wennberg, and M. B. Ericson, “Multiphoton laser scanning microscopy on non-melanoma skin cancer: morphologic features for future non-invasive diagnostics,” J. Invest. Dermatol. 128(5), 1248–1255 (2008).
[CrossRef]

R. Cicchi, L. Sacconi, A. Jasaitis, R. P. O’Connor, D. Massi, S. Sestini, V. De Giorgi, T. Lotti, and F. S. Pavone, “Multidimensional custom-made non-linear microscope: from ex-vivo to in-vivo imaging,” Appl. Phys. B 92(3), 359–365 (2008).
[CrossRef]

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]

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
[CrossRef] [PubMed]

K. Steenkeste, S. Lécart, A. Deniset, P. Pernot, P. Eschwège, S. Ferlicot, S. Lévêque-Fort, R. Briandet, and M. P. Fontaine-Aupart, “Ex vivo fluorescence imaging of normal and malignant urothelial cells to enhance early diagnosis,” Photochem. Photobiol. 83(5), 1157–1166 (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]

2006 (2)

S. Y. Breusegem, M. Levi, and N. P. Barry, “Fluorescence correlation spectroscopy and fluorescence lifetime imaging microscopy,” Nephron, Exp. Nephrol. 103(2), e41–e49 (2006).
[CrossRef]

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
[CrossRef] [PubMed]

2005 (5)

L. H. Laiho, S. Pelet, T. M. Hancewicz, P. D. Kaplan, and P. T. C. So, “Two-photon 3-D mapping of ex vivo human skin endogenous fluorescence species based on fluorescence emission spectra,” J. Biomed. Opt. 10(2), 024016 (2005).
[CrossRef] [PubMed]

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

S. J. Lin, R. J. Wu, H. Y. Tan, W. Lo, W. C. Lin, T. H. Young, C. J. Hsu, J. S. Chen, S. H. Jee, and C. Y. Dong, “Evaluating cutaneous photoaging by use of multiphoton fluorescence and second-harmonic generation microscopy,” Opt. Lett. 30(17), 2275–2277 (2005).
[CrossRef] [PubMed]

D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
[CrossRef] [PubMed]

Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (2005).
[CrossRef] [PubMed]

2004 (1)

Y. Chen and A. Periasamy, “Characterization of two-photon excitation fluorescence lifetime imaging microscopy for protein localization,” Microsc. Res. Tech. 63(1), 72–80 (2004).
[CrossRef]

2003 (7)

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]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
[CrossRef] [PubMed]

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
[CrossRef] [PubMed]

F. Koenig, J. Knittel, L. Schnieder, M. George, M. Lein, and D. Schnorr, “Confocal laser scanning microscopy of urinary bladder after intravesical instillation of a fluorescent dye,” Urology 62(1), 158–161 (2003).
[CrossRef] [PubMed]

K. König and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt. 8(3), 432–439 (2003).
[CrossRef] [PubMed]

2002 (3)

D. Zaak, H. Stepp, R. Baumgartner, P. Schneede, R. Waidelich, D. Frimberger, A. Hartmann, R. Künchel, A. Hofstetter, and A. Hohla, “Ultraviolet-excited (308 nm) autofluorescence for bladder cancer detection,” Urology 60(6), 1029–1033 (2002).
[CrossRef] [PubMed]

J. C. Malone, A. F. Hood, T. Conley, J. Nürnberger, L. A. Baldridge, J. L. Clendenon, K. W. Dunn, and C. L. Phillips, “Three-dimensional imaging of human skin and mucosa by two-photon laser scanning microscopy,” J. Cutan. Pathol. 29(8), 453–458 (2002).
[CrossRef] [PubMed]

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

2000 (2)

P. J. Tadrous, “Methods for imaging the structure and function of living tissues and cells: 2. Fluorescence lifetime imaging,” J. Pathol. 191(3), 229–234 (2000).
[CrossRef] [PubMed]

N. Ramanujam, “Fluorescence spectroscopy of neoplastic and non-neoplastic tissues,” Neoplasia 2(1/2), 89–117 (2000).
[CrossRef] [PubMed]

1998 (3)

M. Anidjar, O. Cussenot, S. Avrillier, D. Ettori, P. Teillac, and A. Le Duc, “The role of laser-induced autofluorescence spectroscopy in bladder tumor detection. Dependence on the excitation wavelength,” Ann. N. Y. Acad. Sci. 838(1 ADVANCES IN O), 130–141 (1998).
[CrossRef] [PubMed]

B. R. Masters, P. T. C. So, and E. Gratton, “Optical biopsy of in vivo human skin: multi-photon excitation microscopy,” Lasers Med. Sci. 13(3), 196–203 (1998).
[CrossRef]

P. T. C. So, H. Kim, and I. E. Kochevar, “Two-Photon deep tissue ex vivo imaging of mouse dermal and subcutaneous structures,” Opt. Express 3(9), 339–350 (1998).
[CrossRef] [PubMed]

1996 (1)

F. Koenig, F. J. McGovern, A. F. Althausen, T. F. Deutsch, and K. T. Schomacker, “Laser induced autofluorescence diagnosis of bladder cancer,” J. Urol. 156(5), 1597–1601 (1996).
[CrossRef] [PubMed]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[CrossRef] [PubMed]

Althausen, A. F.

F. Koenig, F. J. McGovern, A. F. Althausen, T. F. Deutsch, and K. T. Schomacker, “Laser induced autofluorescence diagnosis of bladder cancer,” J. Urol. 156(5), 1597–1601 (1996).
[CrossRef] [PubMed]

Anidjar, M.

M. Anidjar, O. Cussenot, S. Avrillier, D. Ettori, P. Teillac, and A. Le Duc, “The role of laser-induced autofluorescence spectroscopy in bladder tumor detection. Dependence on the excitation wavelength,” Ann. N. Y. Acad. Sci. 838(1 ADVANCES IN O), 130–141 (1998).
[CrossRef] [PubMed]

Arum, C. J.

E. L. Larsen, L. L. Randeberg, O. A. Gederaas, C. J. Arum, A. Hjelde, C. M. Zhao, D. Chen, H. E. Krokan, and L. O. Svaasand, “Monitoring of hexyl 5-aminolevulinate-induced photodynamic therapy in rat bladder cancer by optical spectroscopy,” J. Biomed. Opt. 13(4), 044031 (2008).
[CrossRef] [PubMed]

Avrillier, S.

M. Anidjar, O. Cussenot, S. Avrillier, D. Ettori, P. Teillac, and A. Le Duc, “The role of laser-induced autofluorescence spectroscopy in bladder tumor detection. Dependence on the excitation wavelength,” Ann. N. Y. Acad. Sci. 838(1 ADVANCES IN O), 130–141 (1998).
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G. A. Sonn, S. N. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urol. 182(4), 1299–1305 (2009).
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S. M. Zhuo, J. X. Chen, T. Luo, X. S. Jiang, and S. S. Xie, “Multiphoton microscopy of unstained bladder mucosa based on two-photon excited autofluorescence and second-harmonic generation,” Laser Phys. Lett. 6(1), 80–83 (2009).
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D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
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G. A. Sonn, S. N. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urol. 182(4), 1299–1305 (2009).
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J. C. Kah, W. K. Lau, P. H. Tan, C. J. Sheppard, and M. Olivo, “Endoscopic image analysis of photosensitizer fluorescence as a promising noninvasive approach for pathological grading of bladder cancer in situ,” J. Biomed. Opt. 13(5), 054022 (2008).
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L. H. Laiho, S. Pelet, T. M. Hancewicz, P. D. Kaplan, and P. T. C. So, “Two-photon 3-D mapping of ex vivo human skin endogenous fluorescence species based on fluorescence emission spectra,” J. Biomed. Opt. 10(2), 024016 (2005).
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M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
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P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
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D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
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Kim, H.

Knittel, J.

F. Koenig, J. Knittel, L. Schnieder, M. George, M. Lein, and D. Schnorr, “Confocal laser scanning microscopy of urinary bladder after intravesical instillation of a fluorescent dye,” Urology 62(1), 158–161 (2003).
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B. Hermes, F. Spöler, A. Naami, J. Bornemann, M. Först, J. Grosse, G. Jakse, and R. Knüchel, “Visualization of the basement membrane zone of the bladder by optical coherence tomography: feasibility of noninvasive evaluation of tumor invasion,” Urology 72(3), 677–681 (2008).
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D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
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Koenig, F.

F. Koenig, J. Knittel, L. Schnieder, M. George, M. Lein, and D. Schnorr, “Confocal laser scanning microscopy of urinary bladder after intravesical instillation of a fluorescent dye,” Urology 62(1), 158–161 (2003).
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D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
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K. König and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt. 8(3), 432–439 (2003).
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D. Zaak, H. Stepp, R. Baumgartner, P. Schneede, R. Waidelich, D. Frimberger, A. Hartmann, R. Künchel, A. Hofstetter, and A. Hohla, “Ultraviolet-excited (308 nm) autofluorescence for bladder cancer detection,” Urology 60(6), 1029–1033 (2002).
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D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
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J. C. Kah, W. K. Lau, P. H. Tan, C. J. Sheppard, and M. Olivo, “Endoscopic image analysis of photosensitizer fluorescence as a promising noninvasive approach for pathological grading of bladder cancer in situ,” J. Biomed. Opt. 13(5), 054022 (2008).
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F. Koenig, J. Knittel, L. Schnieder, M. George, M. Lein, and D. Schnorr, “Confocal laser scanning microscopy of urinary bladder after intravesical instillation of a fluorescent dye,” Urology 62(1), 158–161 (2003).
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K. Steenkeste, S. Lécart, A. Deniset, P. Pernot, P. Eschwège, S. Ferlicot, S. Lévêque-Fort, R. Briandet, and M. P. Fontaine-Aupart, “Ex vivo fluorescence imaging of normal and malignant urothelial cells to enhance early diagnosis,” Photochem. Photobiol. 83(5), 1157–1166 (2007).
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Lin, W. C.

Liu, J.

Z. Yuan, Z. Wang, R. Pan, J. Liu, H. Cohen, and Y. Pan, “High-resolution imaging diagnosis and staging of bladder cancer: comparison between optical coherence tomography and high-frequency ultrasound,” J. Biomed. Opt. 13(5), 054007 (2008).
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M. E. Llewellyn, R. P. J. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454(7205), 784–788 (2008).
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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).
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S. M. Zhuo, J. X. Chen, T. Luo, X. S. Jiang, and S. S. Xie, “Multiphoton microscopy of unstained bladder mucosa based on two-photon excited autofluorescence and second-harmonic generation,” Laser Phys. Lett. 6(1), 80–83 (2009).
[CrossRef]

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G. A. Sonn, S. N. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urol. 182(4), 1299–1305 (2009).
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J. C. Malone, A. F. Hood, T. Conley, J. Nürnberger, L. A. Baldridge, J. L. Clendenon, K. W. Dunn, and C. L. Phillips, “Three-dimensional imaging of human skin and mucosa by two-photon laser scanning microscopy,” J. Cutan. Pathol. 29(8), 453–458 (2002).
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R. Cicchi, S. Sestini, V. De Giorgi, D. Massi, T. Lotti, and F. S. Pavone, “Non-linear laser imaging of skin lesions,” J. Biophoton. 1(1), 62–73 (2008).
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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).
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F. Koenig, F. J. McGovern, A. F. Althausen, T. F. Deutsch, and K. T. Schomacker, “Laser induced autofluorescence diagnosis of bladder cancer,” J. Urol. 156(5), 1597–1601 (1996).
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E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
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D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
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B. Hermes, F. Spöler, A. Naami, J. Bornemann, M. Först, J. Grosse, G. Jakse, and R. Knüchel, “Visualization of the basement membrane zone of the bladder by optical coherence tomography: feasibility of noninvasive evaluation of tumor invasion,” Urology 72(3), 677–681 (2008).
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W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
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J. C. Malone, A. F. Hood, T. Conley, J. Nürnberger, L. A. Baldridge, J. L. Clendenon, K. W. Dunn, and C. L. Phillips, “Three-dimensional imaging of human skin and mucosa by two-photon laser scanning microscopy,” J. Cutan. Pathol. 29(8), 453–458 (2002).
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R. Cicchi, L. Sacconi, A. Jasaitis, R. P. O’Connor, D. Massi, S. Sestini, V. De Giorgi, T. Lotti, and F. S. Pavone, “Multidimensional custom-made non-linear microscope: from ex-vivo to in-vivo imaging,” Appl. Phys. B 92(3), 359–365 (2008).
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W. W. Chin, P. S. P. Thong, R. Bhuvaneswari, K. C. Soo, P. W. S. Heng, and M. Olivo, “In-vivo optical detection of cancer using chlorin e6-polyvinylpyrrolidone induced fluorescence imaging and spectroscopy,” BMC Med. Imaging 9(1), 1–8 (2009).
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Z. Yuan, Z. Wang, R. Pan, J. Liu, H. Cohen, and Y. Pan, “High-resolution imaging diagnosis and staging of bladder cancer: comparison between optical coherence tomography and high-frequency ultrasound,” J. Biomed. Opt. 13(5), 054007 (2008).
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Pan, Y.

Z. Yuan, Z. Wang, R. Pan, J. Liu, H. Cohen, and Y. Pan, “High-resolution imaging diagnosis and staging of bladder cancer: comparison between optical coherence tomography and high-frequency ultrasound,” J. Biomed. Opt. 13(5), 054007 (2008).
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Pan, Y. T.

Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (2005).
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J. Paoli, M. Smedh, A. M. Wennberg, and M. B. Ericson, “Multiphoton laser scanning microscopy on non-melanoma skin cancer: morphologic features for future non-invasive diagnostics,” J. Invest. Dermatol. 128(5), 1248–1255 (2008).
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R. Cicchi, L. Sacconi, A. Jasaitis, R. P. O’Connor, D. Massi, S. Sestini, V. De Giorgi, T. Lotti, and F. S. Pavone, “Multidimensional custom-made non-linear microscope: from ex-vivo to in-vivo imaging,” Appl. Phys. B 92(3), 359–365 (2008).
[CrossRef]

R. Cicchi, S. Sestini, V. De Giorgi, D. Massi, T. Lotti, and F. S. Pavone, “Non-linear laser imaging of skin lesions,” J. Biophoton. 1(1), 62–73 (2008).
[CrossRef]

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]

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L. H. Laiho, S. Pelet, T. M. Hancewicz, P. D. Kaplan, and P. T. C. So, “Two-photon 3-D mapping of ex vivo human skin endogenous fluorescence species based on fluorescence emission spectra,” J. Biomed. Opt. 10(2), 024016 (2005).
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Y. Chen and A. Periasamy, “Characterization of two-photon excitation fluorescence lifetime imaging microscopy for protein localization,” Microsc. Res. Tech. 63(1), 72–80 (2004).
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K. Steenkeste, S. Lécart, A. Deniset, P. Pernot, P. Eschwège, S. Ferlicot, S. Lévêque-Fort, R. Briandet, and M. P. Fontaine-Aupart, “Ex vivo fluorescence imaging of normal and malignant urothelial cells to enhance early diagnosis,” Photochem. Photobiol. 83(5), 1157–1166 (2007).
[CrossRef] [PubMed]

Phillips, C. L.

J. C. Malone, A. F. Hood, T. Conley, J. Nürnberger, L. A. Baldridge, J. L. Clendenon, K. W. Dunn, and C. L. Phillips, “Three-dimensional imaging of human skin and mucosa by two-photon laser scanning microscopy,” J. Cutan. Pathol. 29(8), 453–458 (2002).
[CrossRef] [PubMed]

Pluen, A.

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
[CrossRef] [PubMed]

Popken, G.

D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
[CrossRef] [PubMed]

Provenzano, P. P.

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
[CrossRef] [PubMed]

Ramanujam, N.

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
[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]

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
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N. Ramanujam, “Fluorescence spectroscopy of neoplastic and non-neoplastic tissues,” Neoplasia 2(1/2), 89–117 (2000).
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E. L. Larsen, L. L. Randeberg, O. A. Gederaas, C. J. Arum, A. Hjelde, C. M. Zhao, D. Chen, H. E. Krokan, and L. O. Svaasand, “Monitoring of hexyl 5-aminolevulinate-induced photodynamic therapy in rat bladder cancer by optical spectroscopy,” J. Biomed. Opt. 13(4), 044031 (2008).
[CrossRef] [PubMed]

Riching, K. M.

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]

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
[CrossRef] [PubMed]

Riemann, I.

K. König and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt. 8(3), 432–439 (2003).
[CrossRef] [PubMed]

Sacconi, L.

R. Cicchi, L. Sacconi, A. Jasaitis, R. P. O’Connor, D. Massi, S. Sestini, V. De Giorgi, T. Lotti, and F. S. Pavone, “Multidimensional custom-made non-linear microscope: from ex-vivo to in-vivo imaging,” Appl. Phys. B 92(3), 359–365 (2008).
[CrossRef]

Schneede, P.

D. Zaak, H. Stepp, R. Baumgartner, P. Schneede, R. Waidelich, D. Frimberger, A. Hartmann, R. Künchel, A. Hofstetter, and A. Hohla, “Ultraviolet-excited (308 nm) autofluorescence for bladder cancer detection,” Urology 60(6), 1029–1033 (2002).
[CrossRef] [PubMed]

Schnieder, L.

F. Koenig, J. Knittel, L. Schnieder, M. George, M. Lein, and D. Schnorr, “Confocal laser scanning microscopy of urinary bladder after intravesical instillation of a fluorescent dye,” Urology 62(1), 158–161 (2003).
[CrossRef] [PubMed]

Schnitzer, M. J.

M. E. Llewellyn, R. P. J. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454(7205), 784–788 (2008).
[PubMed]

Schnorr, D.

F. Koenig, J. Knittel, L. Schnieder, M. George, M. Lein, and D. Schnorr, “Confocal laser scanning microscopy of urinary bladder after intravesical instillation of a fluorescent dye,” Urology 62(1), 158–161 (2003).
[CrossRef] [PubMed]

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Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (2005).
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E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–801 (2003).
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R. Cicchi, S. Sestini, V. De Giorgi, D. Massi, T. Lotti, and F. S. Pavone, “Non-linear laser imaging of skin lesions,” J. Biophoton. 1(1), 62–73 (2008).
[CrossRef]

R. Cicchi, L. Sacconi, A. Jasaitis, R. P. O’Connor, D. Massi, S. Sestini, V. De Giorgi, T. Lotti, and F. S. Pavone, “Multidimensional custom-made non-linear microscope: from ex-vivo to in-vivo imaging,” Appl. Phys. B 92(3), 359–365 (2008).
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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).
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Sheppard, C. J.

J. C. Kah, W. K. Lau, P. H. Tan, C. J. Sheppard, and M. Olivo, “Endoscopic image analysis of photosensitizer fluorescence as a promising noninvasive approach for pathological grading of bladder cancer in situ,” J. Biomed. Opt. 13(5), 054022 (2008).
[CrossRef] [PubMed]

Shousha, S.

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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Siegel, J.

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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Skala, M. C.

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
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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).
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Smedh, M.

J. Paoli, M. Smedh, A. M. Wennberg, and M. B. Ericson, “Multiphoton laser scanning microscopy on non-melanoma skin cancer: morphologic features for future non-invasive diagnostics,” J. Invest. Dermatol. 128(5), 1248–1255 (2008).
[CrossRef]

So, P. T. C.

L. H. Laiho, S. Pelet, T. M. Hancewicz, P. D. Kaplan, and P. T. C. So, “Two-photon 3-D mapping of ex vivo human skin endogenous fluorescence species based on fluorescence emission spectra,” J. Biomed. Opt. 10(2), 024016 (2005).
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G. A. Sonn, S. N. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urol. 182(4), 1299–1305 (2009).
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W. W. Chin, P. S. P. Thong, R. Bhuvaneswari, K. C. Soo, P. W. S. Heng, and M. Olivo, “In-vivo optical detection of cancer using chlorin e6-polyvinylpyrrolidone induced fluorescence imaging and spectroscopy,” BMC Med. Imaging 9(1), 1–8 (2009).
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B. Hermes, F. Spöler, A. Naami, J. Bornemann, M. Först, J. Grosse, G. Jakse, and R. Knüchel, “Visualization of the basement membrane zone of the bladder by optical coherence tomography: feasibility of noninvasive evaluation of tumor invasion,” Urology 72(3), 677–681 (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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K. Steenkeste, S. Lécart, A. Deniset, P. Pernot, P. Eschwège, S. Ferlicot, S. Lévêque-Fort, R. Briandet, and M. P. Fontaine-Aupart, “Ex vivo fluorescence imaging of normal and malignant urothelial cells to enhance early diagnosis,” Photochem. Photobiol. 83(5), 1157–1166 (2007).
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D. Zaak, H. Stepp, R. Baumgartner, P. Schneede, R. Waidelich, D. Frimberger, A. Hartmann, R. Künchel, A. Hofstetter, and A. Hohla, “Ultraviolet-excited (308 nm) autofluorescence for bladder cancer detection,” Urology 60(6), 1029–1033 (2002).
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W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[CrossRef] [PubMed]

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E. L. Larsen, L. L. Randeberg, O. A. Gederaas, C. J. Arum, A. Hjelde, C. M. Zhao, D. Chen, H. E. Krokan, and L. O. Svaasand, “Monitoring of hexyl 5-aminolevulinate-induced photodynamic therapy in rat bladder cancer by optical spectroscopy,” J. Biomed. Opt. 13(4), 044031 (2008).
[CrossRef] [PubMed]

Tadrous, P. J.

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]

P. J. Tadrous, “Methods for imaging the structure and function of living tissues and cells: 2. Fluorescence lifetime imaging,” J. Pathol. 191(3), 229–234 (2000).
[CrossRef] [PubMed]

Tan, G.

R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol. 23(5), 861–867 (2009).
[CrossRef] [PubMed]

Tan, H. Y.

Tan, P. H.

J. C. Kah, W. K. Lau, P. H. Tan, C. J. Sheppard, and M. Olivo, “Endoscopic image analysis of photosensitizer fluorescence as a promising noninvasive approach for pathological grading of bladder cancer in situ,” J. Biomed. Opt. 13(5), 054022 (2008).
[CrossRef] [PubMed]

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G. A. Sonn, S. N. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urol. 182(4), 1299–1305 (2009).
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M. Anidjar, O. Cussenot, S. Avrillier, D. Ettori, P. Teillac, and A. Le Duc, “The role of laser-induced autofluorescence spectroscopy in bladder tumor detection. Dependence on the excitation wavelength,” Ann. N. Y. Acad. Sci. 838(1 ADVANCES IN O), 130–141 (1998).
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Tewari, A. K.

R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol. 23(5), 861–867 (2009).
[CrossRef] [PubMed]

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W. W. Chin, P. S. P. Thong, R. Bhuvaneswari, K. C. Soo, P. W. S. Heng, and M. Olivo, “In-vivo optical detection of cancer using chlorin e6-polyvinylpyrrolidone induced fluorescence imaging and spectroscopy,” BMC Med. Imaging 9(1), 1–8 (2009).
[CrossRef] [PubMed]

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A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
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D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
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D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
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Vrotsos, K. M.

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
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D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
[CrossRef] [PubMed]

Waidelich, R.

D. Zaak, H. Stepp, R. Baumgartner, P. Schneede, R. Waidelich, D. Frimberger, A. Hartmann, R. Künchel, A. Hofstetter, and A. Hohla, “Ultraviolet-excited (308 nm) autofluorescence for bladder cancer detection,” Urology 60(6), 1029–1033 (2002).
[CrossRef] [PubMed]

Wang, Z.

Z. Yuan, Z. Wang, R. Pan, J. Liu, H. Cohen, and Y. Pan, “High-resolution imaging diagnosis and staging of bladder cancer: comparison between optical coherence tomography and high-frequency ultrasound,” J. Biomed. Opt. 13(5), 054007 (2008).
[CrossRef] [PubMed]

Wang, Z. G.

Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (2005).
[CrossRef] [PubMed]

Webb, W. W.

R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol. 23(5), 861–867 (2009).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[CrossRef] [PubMed]

Wennberg, A. M.

J. Paoli, M. Smedh, A. M. Wennberg, and M. B. Ericson, “Multiphoton laser scanning microscopy on non-melanoma skin cancer: morphologic features for future non-invasive diagnostics,” J. Invest. Dermatol. 128(5), 1248–1255 (2008).
[CrossRef]

White, J. G.

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. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
[CrossRef] [PubMed]

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Williams, R. M.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Witjes, F.

D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
[CrossRef] [PubMed]

Wu, R. J.

Xie, S. S.

S. M. Zhuo, J. X. Chen, T. Luo, X. S. Jiang, and S. S. Xie, “Multiphoton microscopy of unstained bladder mucosa based on two-photon excited autofluorescence and second-harmonic generation,” Laser Phys. Lett. 6(1), 80–83 (2009).
[CrossRef]

Yadav, R.

R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol. 23(5), 861–867 (2009).
[CrossRef] [PubMed]

Yan, L.

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Yeh, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

Young, T. H.

Yuan, Z.

Z. Yuan, Z. Wang, R. Pan, J. Liu, H. Cohen, and Y. Pan, “High-resolution imaging diagnosis and staging of bladder cancer: comparison between optical coherence tomography and high-frequency ultrasound,” J. Biomed. Opt. 13(5), 054007 (2008).
[CrossRef] [PubMed]

Zaak, D.

D. Zaak, H. Stepp, R. Baumgartner, P. Schneede, R. Waidelich, D. Frimberger, A. Hartmann, R. Künchel, A. Hofstetter, and A. Hohla, “Ultraviolet-excited (308 nm) autofluorescence for bladder cancer detection,” Urology 60(6), 1029–1033 (2002).
[CrossRef] [PubMed]

Zeylemaker, B.

D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
[CrossRef] [PubMed]

Zhao, C. M.

E. L. Larsen, L. L. Randeberg, O. A. Gederaas, C. J. Arum, A. Hjelde, C. M. Zhao, D. Chen, H. E. Krokan, and L. O. Svaasand, “Monitoring of hexyl 5-aminolevulinate-induced photodynamic therapy in rat bladder cancer by optical spectroscopy,” J. Biomed. Opt. 13(4), 044031 (2008).
[CrossRef] [PubMed]

Zhuo, S. M.

S. M. Zhuo, J. X. Chen, T. Luo, X. S. Jiang, and S. S. Xie, “Multiphoton microscopy of unstained bladder mucosa based on two-photon excited autofluorescence and second-harmonic generation,” Laser Phys. Lett. 6(1), 80–83 (2009).
[CrossRef]

Zipfel, W. R.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[CrossRef] [PubMed]

Zoumi, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

Ann. N. Y. Acad. Sci. (1)

M. Anidjar, O. Cussenot, S. Avrillier, D. Ettori, P. Teillac, and A. Le Duc, “The role of laser-induced autofluorescence spectroscopy in bladder tumor detection. Dependence on the excitation wavelength,” Ann. N. Y. Acad. Sci. 838(1 ADVANCES IN O), 130–141 (1998).
[CrossRef] [PubMed]

Appl. Phys. B (1)

R. Cicchi, L. Sacconi, A. Jasaitis, R. P. O’Connor, D. Massi, S. Sestini, V. De Giorgi, T. Lotti, and F. S. Pavone, “Multidimensional custom-made non-linear microscope: from ex-vivo to in-vivo imaging,” Appl. Phys. B 92(3), 359–365 (2008).
[CrossRef]

BMC Med. (1)

P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Med. 4(1), 38 (2006).
[CrossRef] [PubMed]

BMC Med. Imaging (1)

W. W. Chin, P. S. P. Thong, R. Bhuvaneswari, K. C. Soo, P. W. S. Heng, and M. Olivo, “In-vivo optical detection of cancer using chlorin e6-polyvinylpyrrolidone induced fluorescence imaging and spectroscopy,” BMC Med. Imaging 9(1), 1–8 (2009).
[CrossRef] [PubMed]

Cancer Res. (1)

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

J. Biomed. Opt. (6)

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
[CrossRef] [PubMed]

Z. Yuan, Z. Wang, R. Pan, J. Liu, H. Cohen, and Y. Pan, “High-resolution imaging diagnosis and staging of bladder cancer: comparison between optical coherence tomography and high-frequency ultrasound,” J. Biomed. Opt. 13(5), 054007 (2008).
[CrossRef] [PubMed]

J. C. Kah, W. K. Lau, P. H. Tan, C. J. Sheppard, and M. Olivo, “Endoscopic image analysis of photosensitizer fluorescence as a promising noninvasive approach for pathological grading of bladder cancer in situ,” J. Biomed. Opt. 13(5), 054022 (2008).
[CrossRef] [PubMed]

E. L. Larsen, L. L. Randeberg, O. A. Gederaas, C. J. Arum, A. Hjelde, C. M. Zhao, D. Chen, H. E. Krokan, and L. O. Svaasand, “Monitoring of hexyl 5-aminolevulinate-induced photodynamic therapy in rat bladder cancer by optical spectroscopy,” J. Biomed. Opt. 13(4), 044031 (2008).
[CrossRef] [PubMed]

K. König and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt. 8(3), 432–439 (2003).
[CrossRef] [PubMed]

L. H. Laiho, S. Pelet, T. M. Hancewicz, P. D. Kaplan, and P. T. C. So, “Two-photon 3-D mapping of ex vivo human skin endogenous fluorescence species based on fluorescence emission spectra,” J. Biomed. Opt. 10(2), 024016 (2005).
[CrossRef] [PubMed]

J. Biophoton. (1)

R. Cicchi, S. Sestini, V. De Giorgi, D. Massi, T. Lotti, and F. S. Pavone, “Non-linear laser imaging of skin lesions,” J. Biophoton. 1(1), 62–73 (2008).
[CrossRef]

J. Cutan. Pathol. (1)

J. C. Malone, A. F. Hood, T. Conley, J. Nürnberger, L. A. Baldridge, J. L. Clendenon, K. W. Dunn, and C. L. Phillips, “Three-dimensional imaging of human skin and mucosa by two-photon laser scanning microscopy,” J. Cutan. Pathol. 29(8), 453–458 (2002).
[CrossRef] [PubMed]

J. Endourol. (1)

R. Yadav, S. Mukherjee, M. Hermen, G. Tan, F. R. Maxfield, W. W. Webb, and A. K. Tewari, “Multiphoton microscopy of prostate and periprostatic neural tissue: a promising imaging technique for improving nerve-sparing prostatectomy,” J. Endourol. 23(5), 861–867 (2009).
[CrossRef] [PubMed]

J. Invest. Dermatol. (1)

J. Paoli, M. Smedh, A. M. Wennberg, and M. B. Ericson, “Multiphoton laser scanning microscopy on non-melanoma skin cancer: morphologic features for future non-invasive diagnostics,” J. Invest. Dermatol. 128(5), 1248–1255 (2008).
[CrossRef]

J. Pathol. (2)

P. J. Tadrous, “Methods for imaging the structure and function of living tissues and cells: 2. Fluorescence lifetime imaging,” J. Pathol. 191(3), 229–234 (2000).
[CrossRef] [PubMed]

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. Urol. (4)

F. Koenig, F. J. McGovern, A. F. Althausen, T. F. Deutsch, and K. T. Schomacker, “Laser induced autofluorescence diagnosis of bladder cancer,” J. Urol. 156(5), 1597–1601 (1996).
[CrossRef] [PubMed]

G. A. Sonn, S. N. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urol. 182(4), 1299–1305 (2009).
[CrossRef] [PubMed]

D. Jocham, F. Witjes, S. Wagner, B. Zeylemaker, J. van Moorselaar, M. O. Grimm, R. Muschter, G. Popken, F. König, R. Knüchel, and K. H. Kurth, “Improved detection and treatment of bladder cancer using hexaminolevulinate imaging: a prospective, phase III multicenter study,” J. Urol. 174(3), 862–866, discussion 866 (2005).
[CrossRef] [PubMed]

Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (2005).
[CrossRef] [PubMed]

Laser Phys. Lett. (1)

S. M. Zhuo, J. X. Chen, T. Luo, X. S. Jiang, and S. S. Xie, “Multiphoton microscopy of unstained bladder mucosa based on two-photon excited autofluorescence and second-harmonic generation,” Laser Phys. Lett. 6(1), 80–83 (2009).
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Lasers Med. Sci. (1)

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Figures (5)

Fig. 1
Fig. 1

Combined TPEF (green-coded) and SHG (blue-coded) images taken from human ex-vivo fresh biopsies of bladder and the corresponding histological images taken after H&E staining of the same sample. On the left: an optical section of healthy mucosa acquired at 25 μm depth (a), and the corresponding histological image (b); an optical section of HM / connective tissue border acquired at 55 μm depth (c) and the corresponding histological image (d). On the right: an optical section of CIS acquired at 25 μm depth (e), and the corresponding histological image (f); an optical section of CIS / connective tissue border acquired at 55 μm depth (g) and the corresponding histological image (h). Scale bars: 10 μm.

Fig. 2
Fig. 2

Histogram distribution of the cellular-to-nuclear area ratio (d) for CIS (in red) and for HM (in black), calculated by summing over images acquired in a 20-30 μm, on 5 samples of CIS and 5 samples of HM and over 10 cells per sample.

Fig. 3
Fig. 3

Two-photon emission spectra for CIS (red) and for HM (black), measured by summing the detected photon number over a region of 20 μm × 20 μm at a depth of 50-60 μm, and by averaging on 5 samples of CIS and 5 samples of HM, for 740 nm excitation (a), and for 890 nm excitation (b). Two examples of SAAID maps (c), calculated using Eq. (1), for both CIS and HM presented in a color-coded scale. Scale bars: 5 μm. SAAID distribution for CIS (red) and for HM (black) with the color-coded scale used in SAAID mapping superimposed (d), obtained by summing the calculated SAAID index over a region of 20 μm × 20 μm, and after averaging on 5 samples of CIS and 5 samples of HM.

Fig. 4
Fig. 4

MTPE images of HM acquired: at 740 nm excitation wavelength and detected in the 459 nm – 472 nm spectral range (a); at 890 nm excitation wavelength and detected in the 511 nm – 524 nm spectral range (b). Scale bars: 2 μm. Two examples of ROx maps (c), calculated using Eq. (2), for both CIS and HM presented in a color-coded scale. Scale bars: 5 μm. Red-Ox ratio distribution for CIS (red) and for HM (black) with the color-coded scale used in ROx mapping superimposed (d), obtained by summing the calculated ROx index over a region of 20 μm × 20 μm, and after averaging on 5 samples of CIS and 5 samples of HM.

Fig. 5
Fig. 5

TPEF image (a) and corresponding lifetime ratio map (b) acquired in HM sample at 25 μm. TPEF image (c) and corresponding lifetime ratio map (d) acquired in CIS at 25 μm depth. Scale bars: 10 μm. Excitation wavelength: 740 nm. Detection band: 430-490 nm. Lifetime components ratio distribution for CIS (red) and for HM (black) at 740 nm (e) and 890 nm (f) excitation wavelength, obtained by summing the parameter over a cellular region of 128 μm × 128 μm at a depth in the 20-30 μm range, and averaging on 5 samples of CIS and 5 samples of HM.

Equations (2)

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S A A I D = S H G T P E F S H G + T P E F .
R O x = F A D N A D H F A D + N A D H .

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