Abstract

This work reports a multimodal system for label-free tissue diagnosis combining fluorescence lifetime imaging (FLIm), ultrasound backscatter microscopy (UBM), and photoacoustic imaging (PAI). This system provides complementary biochemical, structural and functional features allowing for enhanced in vivo detection of oral carcinoma. Results from a hamster oral carcinoma model (normal, precancer and carcinoma) are presented demonstrating the ability of FLIm to delineate biochemical composition at the tissue surface, UBM and related radiofrequency parameters to identify disruptions in the tissue microarchitecture and PAI to map optical absorption associated with specific tissue morphology and physiology.

© 2013 OSA

Full Article  |  PDF Article

References

  • View by:
  • |
  • |
  • |

  1. R. Siegel, D. Naishadham, and A. Jemal, “Cancer statistics, 2013,” CA Cancer J. Clin.63(1), 11–30 (2013).
    [CrossRef] [PubMed]
  2. L. Martí-Bonmatí, R. Sopena, P. Bartumeus, and P. Sopena, “Multimodality imaging techniques,” Contrast Media Mol. Imaging5(4), 180–189 (2010).
    [CrossRef] [PubMed]
  3. Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
    [CrossRef] [PubMed]
  4. W. J. Hucker, C. M. Ripplinger, C. P. Fleming, V. V. Fedorov, A. M. Rollins, and I. R. Efimov, “Bimodal biophotonic imaging of the structure-function relationship in cardiac tissue,” J. Biomed. Opt.13(5), 054012 (2008).
    [CrossRef] [PubMed]
  5. M. Niedre and V. Ntziachristos, “Elucidating Structure and Function In Vivo With Hybrid Fluorescence and Magnetic Resonance Imaging,” Proc. IEEE96(3), 382–396 (2008).
    [CrossRef]
  6. V. Kalchenko, N. Madar-Balakirski, I. Meglinski, and A. Harmelin, “In vivo characterization of tumor and tumor vascular network using multi-modal imaging approach,” J Biophotonics4(9), 645–649 (2011).
    [PubMed]
  7. N. Howlader, A. M. Noone, M. Krapcho, N. Neyman, R. Aminou, S. F. Altekruse, C. L. Kosary, J. Ruhl, Z. Tatalovich, H. Cho, A. Mariotto, M. P. Eisner, D. R. Lewis, H. S. Chen, E. J. Feuer, and K. A. Cronin, eds., “SEER Cancer Statistics Review, 1975-2009 (Vintage 2009 Populations),” (National Cancer Institute., Bethesda, MD, 2012).
  8. Z. Rumboldt, T. A. Day, and M. Michel, “Imaging of oral cavity cancer,” Oral Oncol.42(9), 854–865 (2006).
    [CrossRef] [PubMed]
  9. B. M. Trotta, C. S. Pease, J. J. Rasamny, P. Raghavan, and S. Mukherjee, “Oral cavity and oropharyngeal squamous cell cancer: key imaging findings for staging and treatment planning,” Radiographics31(2), 339–354 (2011).
    [CrossRef] [PubMed]
  10. W. L. Lodder, H. J. Teertstra, I. B. Tan, F. A. Pameijer, L. E. Smeele, M. L. F. van Velthuysen, and M. W. M. van den Brekel, “Tumour thickness in oral cancer using an intra-oral ultrasound probe,” Eur. Radiol.21(1), 98–106 (2011).
    [CrossRef] [PubMed]
  11. M. Hagiwara, A. Nusbaum, and B. L. Schmidt, “MR Assessment of Oral Cavity Carcinomas,” Magn. Reson. Imaging Clin. N. Am.20(3), 473–494 (2012).
    [CrossRef] [PubMed]
  12. L. L. Simon and D. Rubinstein, “Imaging of oral cancer,” Otolaryngol. Clin. North Am.39(2), 307–317, vi (2006).
    [CrossRef] [PubMed]
  13. L. L. Myers, M. K. Wax, H. Nabi, G. T. Simpson, and D. Lamonica, “Positron Emission Tomography in the Evaluation of the N0 Neck,” Laryngoscope108(2), 232–236 (1998).
    [CrossRef] [PubMed]
  14. D. Shin, N. Vigneswaran, A. Gillenwater, and R. Richards-Kortum, “Advances in fluorescence imaging techniques to detect oral cancer and its precursors,” Future Oncol.6(7), 1143–1154 (2010).
    [CrossRef] [PubMed]
  15. J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
    [PubMed]
  16. W. G. Jung, J. Zhang, J. R. Chung, P. Wilder-Smith, M. Brenner, J. S. Nelson, and Z. P. Chen, “Advances in oral cancer detection using optical coherence tomography,” IEEE J Sel Top Quantum Electron.11(4), 811–817 (2005).
    [CrossRef]
  17. C.-K. Lee, T.-T. Chi, C.-T. Wu, M.-T. Tsai, C.-P. Chiang, and C.-C. Yang, “Diagnosis of oral precancer with optical coherence tomography,” Biomed. Opt. Express3(7), 1632–1646 (2012).
    [CrossRef] [PubMed]
  18. P.-C. Li, C.-R. C. Wang, D.-B. Shieh, C.-W. Wei, C.-K. Liao, C. Poe, S. Jhan, A.-A. Ding, and Y.-N. Wu, “In vivo photoacoustic molecular imaging with simultaneous multiple selective targeting using antibody-conjugated gold nanorods,” Opt. Express16(23), 18605–18615 (2008).
    [CrossRef] [PubMed]
  19. S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, and S. Emelianov, “Multiwavelength Photoacoustic Imaging and Plasmon Resonance Coupling of Gold Nanoparticles for Selective Detection of Cancer,” Nano Lett.9(8), 2825–2831 (2009).
    [CrossRef] [PubMed]
  20. M. H. Xu and L. H. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum.77(4), 041101 (2006).
    [CrossRef]
  21. M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
    [CrossRef] [PubMed]
  22. J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
    [CrossRef] [PubMed]
  23. 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]
  24. D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
    [CrossRef] [PubMed]
  25. 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]
  26. J. A. Jo, B. E. Applegate, J. Park, S. Shrestha, P. Pande, I. B. Gimenez-Conti, and J. L. Brandon, “In vivo simultaneous morphological and biochemical optical imaging of oral epithelial cancer,” IEEE. T Biomed. Eng. (N.Y.)57, 2596–2599 (2010).
  27. R. H. Spiro, A. G. Huvos, G. Y. Wong, J. D. Spiro, C. A. Gnecco, and E. W. Strong, “Predictive value of tumor thickness in squamous carcinoma confined to the tongue and floor of the mouth,” Am. J. Surg.152(4), 345–350 (1986).
    [CrossRef] [PubMed]
  28. S. H. Huang, D. Hwang, G. Lockwood, D. P. Goldstein, and B. O’Sullivan, “Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta-analysis of reported studies,” Cancer115(7), 1489–1497 (2009).
    [CrossRef] [PubMed]
  29. F. L. Lizzi, M. Greenebaum, E. J. Feleppa, M. Elbaum, and D. J. Coleman, “Theoretical framework for spectrum analysis in ultrasonic tissue characterization,” J. Acoust. Soc. Am.73(4), 1366–1373 (1983).
    [CrossRef] [PubMed]
  30. I. B. Gimenez-Conti and T. J. Slaga, “The Hamster Cheek Pouch Carcinogenesis Model,” J. Cell. Biochem. Suppl.17F(S17F), 83–90 (1993).
    [CrossRef] [PubMed]
  31. J. J. Salley, “Experimental Carcinogenesis in the Cheek Pouch of the Syrian Hamster,” J. Dent. Res.33(2), 253–262 (1954).
    [CrossRef] [PubMed]
  32. Y. H. Sun, Y. Sun, D. Stephens, H. T. Xie, J. Phipps, R. Saroufeem, J. Southard, D. S. Elson, and L. Marcu, “Dynamic tissue analysis using time- and wavelength-resolved fluorescence spectroscopy for atherosclerosis diagnosis,” Opt. Express19(5), 3890–3901 (2011).
    [CrossRef] [PubMed]
  33. Y. Sun, R. Liu, D. S. Elson, C. W. Hollars, J. A. Jo, J. Park, Y. Sun, and L. Marcu, “Simultaneous time- and wavelength-resolved fluorescence spectroscopy for near real-time tissue diagnosis,” Opt. Lett.33(6), 630–632 (2008).
    [CrossRef] [PubMed]
  34. J. Liu, Y. Sun, J. Qi, and L. Marcu, “A novel method for fast and robust estimation of fluorescence decay dynamics using constrained least-squares deconvolution with Laguerre expansion,” Phys. Med. Biol.57(4), 843–865 (2012).
    [CrossRef] [PubMed]
  35. K. C. B. 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]
  36. M. Y. Berezin and S. Achilefu, “Fluorescence lifetime measurements and biological imaging,” Chem. Rev.110(5), 2641–2684 (2010).
    [CrossRef] [PubMed]
  37. K. Sokolov, J. Galvan, A. Myakov, A. Lacy, R. Lotan, and R. Richards-Kortum, “Realistic three-dimensional epithelial tissue phantoms for biomedical optics,” J. Biomed. Opt.7(1), 148–156 (2002).
    [CrossRef] [PubMed]
  38. M. A. Hollingsworth and B. J. Swanson, “Mucins in cancer: protection and control of the cell surface,” Nat. Rev. Cancer4(1), 45–60 (2004).
    [CrossRef] [PubMed]
  39. V. P. Bhavanandan, N. J. Ringler, and D. C. Gowda, “Identification of the glycosidically bound sialic acid in mucin glycoproteins that reacts as “free sialic acid” in the Warren assay,” Glycobiology8(11), 1077–1086 (1998).
    [CrossRef] [PubMed]
  40. I. K. Cohen, C. W. Moncure, R. J. Witorsch, and R. F. Diegelmann, “Collagen Synthesis in Capsules Surrounding Dimethylbenzanthracene-induced Rat Breast Tumors and the Effect of Pretreatment with β-Aminopropionitrile,” Cancer Res.39(8), 2923–2927 (1979).
    [PubMed]
  41. V. Lutz, M. Sattler, S. Gallinat, H. Wenck, R. Poertner, and F. Fischer, “Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence,” Skin Res. Technol.18(2), 168–179 (2012).
    [CrossRef] [PubMed]

2013

R. Siegel, D. Naishadham, and A. Jemal, “Cancer statistics, 2013,” CA Cancer J. Clin.63(1), 11–30 (2013).
[CrossRef] [PubMed]

2012

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

M. Hagiwara, A. Nusbaum, and B. L. Schmidt, “MR Assessment of Oral Cavity Carcinomas,” Magn. Reson. Imaging Clin. N. Am.20(3), 473–494 (2012).
[CrossRef] [PubMed]

J. Liu, Y. Sun, J. Qi, and L. Marcu, “A novel method for fast and robust estimation of fluorescence decay dynamics using constrained least-squares deconvolution with Laguerre expansion,” Phys. Med. Biol.57(4), 843–865 (2012).
[CrossRef] [PubMed]

V. Lutz, M. Sattler, S. Gallinat, H. Wenck, R. Poertner, and F. Fischer, “Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence,” Skin Res. Technol.18(2), 168–179 (2012).
[CrossRef] [PubMed]

M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
[CrossRef] [PubMed]

C.-K. Lee, T.-T. Chi, C.-T. Wu, M.-T. Tsai, C.-P. Chiang, and C.-C. Yang, “Diagnosis of oral precancer with optical coherence tomography,” Biomed. Opt. Express3(7), 1632–1646 (2012).
[CrossRef] [PubMed]

2011

Y. H. Sun, Y. Sun, D. Stephens, H. T. Xie, J. Phipps, R. Saroufeem, J. Southard, D. S. Elson, and L. Marcu, “Dynamic tissue analysis using time- and wavelength-resolved fluorescence spectroscopy for atherosclerosis diagnosis,” Opt. Express19(5), 3890–3901 (2011).
[CrossRef] [PubMed]

V. Kalchenko, N. Madar-Balakirski, I. Meglinski, and A. Harmelin, “In vivo characterization of tumor and tumor vascular network using multi-modal imaging approach,” J Biophotonics4(9), 645–649 (2011).
[PubMed]

B. M. Trotta, C. S. Pease, J. J. Rasamny, P. Raghavan, and S. Mukherjee, “Oral cavity and oropharyngeal squamous cell cancer: key imaging findings for staging and treatment planning,” Radiographics31(2), 339–354 (2011).
[CrossRef] [PubMed]

W. L. Lodder, H. J. Teertstra, I. B. Tan, F. A. Pameijer, L. E. Smeele, M. L. F. van Velthuysen, and M. W. M. van den Brekel, “Tumour thickness in oral cancer using an intra-oral ultrasound probe,” Eur. Radiol.21(1), 98–106 (2011).
[CrossRef] [PubMed]

2010

L. Martí-Bonmatí, R. Sopena, P. Bartumeus, and P. Sopena, “Multimodality imaging techniques,” Contrast Media Mol. Imaging5(4), 180–189 (2010).
[CrossRef] [PubMed]

D. Shin, N. Vigneswaran, A. Gillenwater, and R. Richards-Kortum, “Advances in fluorescence imaging techniques to detect oral cancer and its precursors,” Future Oncol.6(7), 1143–1154 (2010).
[CrossRef] [PubMed]

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[CrossRef] [PubMed]

J. A. Jo, B. E. Applegate, J. Park, S. Shrestha, P. Pande, I. B. Gimenez-Conti, and J. L. Brandon, “In vivo simultaneous morphological and biochemical optical imaging of oral epithelial cancer,” IEEE. T Biomed. Eng. (N.Y.)57, 2596–2599 (2010).

J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
[CrossRef] [PubMed]

M. Y. Berezin and S. Achilefu, “Fluorescence lifetime measurements and biological imaging,” Chem. Rev.110(5), 2641–2684 (2010).
[CrossRef] [PubMed]

2009

S. H. Huang, D. Hwang, G. Lockwood, D. P. Goldstein, and B. O’Sullivan, “Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta-analysis of reported studies,” Cancer115(7), 1489–1497 (2009).
[CrossRef] [PubMed]

S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, and S. Emelianov, “Multiwavelength Photoacoustic Imaging and Plasmon Resonance Coupling of Gold Nanoparticles for Selective Detection of Cancer,” Nano Lett.9(8), 2825–2831 (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

Y. Sun, R. Liu, D. S. Elson, C. W. Hollars, J. A. Jo, J. Park, Y. Sun, and L. Marcu, “Simultaneous time- and wavelength-resolved fluorescence spectroscopy for near real-time tissue diagnosis,” Opt. Lett.33(6), 630–632 (2008).
[CrossRef] [PubMed]

P.-C. Li, C.-R. C. Wang, D.-B. Shieh, C.-W. Wei, C.-K. Liao, C. Poe, S. Jhan, A.-A. Ding, and Y.-N. Wu, “In vivo photoacoustic molecular imaging with simultaneous multiple selective targeting using antibody-conjugated gold nanorods,” Opt. Express16(23), 18605–18615 (2008).
[CrossRef] [PubMed]

W. J. Hucker, C. M. Ripplinger, C. P. Fleming, V. V. Fedorov, A. M. Rollins, and I. R. Efimov, “Bimodal biophotonic imaging of the structure-function relationship in cardiac tissue,” J. Biomed. Opt.13(5), 054012 (2008).
[CrossRef] [PubMed]

M. Niedre and V. Ntziachristos, “Elucidating Structure and Function In Vivo With Hybrid Fluorescence and Magnetic Resonance Imaging,” Proc. IEEE96(3), 382–396 (2008).
[CrossRef]

2007

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]

J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
[PubMed]

2006

L. L. Simon and D. Rubinstein, “Imaging of oral cancer,” Otolaryngol. Clin. North Am.39(2), 307–317, vi (2006).
[CrossRef] [PubMed]

Z. Rumboldt, T. A. Day, and M. Michel, “Imaging of oral cavity cancer,” Oral Oncol.42(9), 854–865 (2006).
[CrossRef] [PubMed]

M. H. Xu and L. H. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum.77(4), 041101 (2006).
[CrossRef]

2005

W. G. Jung, J. Zhang, J. R. Chung, P. Wilder-Smith, M. Brenner, J. S. Nelson, and Z. P. Chen, “Advances in oral cancer detection using optical coherence tomography,” IEEE J Sel Top Quantum Electron.11(4), 811–817 (2005).
[CrossRef]

2004

M. A. Hollingsworth and B. J. Swanson, “Mucins in cancer: protection and control of the cell surface,” Nat. Rev. Cancer4(1), 45–60 (2004).
[CrossRef] [PubMed]

2002

K. Sokolov, J. Galvan, A. Myakov, A. Lacy, R. Lotan, and R. Richards-Kortum, “Realistic three-dimensional epithelial tissue phantoms for biomedical optics,” J. Biomed. Opt.7(1), 148–156 (2002).
[CrossRef] [PubMed]

2001

K. C. B. 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]

1998

V. P. Bhavanandan, N. J. Ringler, and D. C. Gowda, “Identification of the glycosidically bound sialic acid in mucin glycoproteins that reacts as “free sialic acid” in the Warren assay,” Glycobiology8(11), 1077–1086 (1998).
[CrossRef] [PubMed]

L. L. Myers, M. K. Wax, H. Nabi, G. T. Simpson, and D. Lamonica, “Positron Emission Tomography in the Evaluation of the N0 Neck,” Laryngoscope108(2), 232–236 (1998).
[CrossRef] [PubMed]

1993

I. B. Gimenez-Conti and T. J. Slaga, “The Hamster Cheek Pouch Carcinogenesis Model,” J. Cell. Biochem. Suppl.17F(S17F), 83–90 (1993).
[CrossRef] [PubMed]

1986

R. H. Spiro, A. G. Huvos, G. Y. Wong, J. D. Spiro, C. A. Gnecco, and E. W. Strong, “Predictive value of tumor thickness in squamous carcinoma confined to the tongue and floor of the mouth,” Am. J. Surg.152(4), 345–350 (1986).
[CrossRef] [PubMed]

1983

F. L. Lizzi, M. Greenebaum, E. J. Feleppa, M. Elbaum, and D. J. Coleman, “Theoretical framework for spectrum analysis in ultrasonic tissue characterization,” J. Acoust. Soc. Am.73(4), 1366–1373 (1983).
[CrossRef] [PubMed]

1979

I. K. Cohen, C. W. Moncure, R. J. Witorsch, and R. F. Diegelmann, “Collagen Synthesis in Capsules Surrounding Dimethylbenzanthracene-induced Rat Breast Tumors and the Effect of Pretreatment with β-Aminopropionitrile,” Cancer Res.39(8), 2923–2927 (1979).
[PubMed]

1954

J. J. Salley, “Experimental Carcinogenesis in the Cheek Pouch of the Syrian Hamster,” J. Dent. Res.33(2), 253–262 (1954).
[CrossRef] [PubMed]

Achilefu, S.

M. Y. Berezin and S. Achilefu, “Fluorescence lifetime measurements and biological imaging,” Chem. Rev.110(5), 2641–2684 (2010).
[CrossRef] [PubMed]

Applegate, B. E.

J. A. Jo, B. E. Applegate, J. Park, S. Shrestha, P. Pande, I. B. Gimenez-Conti, and J. L. Brandon, “In vivo simultaneous morphological and biochemical optical imaging of oral epithelial cancer,” IEEE. T Biomed. Eng. (N.Y.)57, 2596–2599 (2010).

Bartumeus, P.

L. Martí-Bonmatí, R. Sopena, P. Bartumeus, and P. Sopena, “Multimodality imaging techniques,” Contrast Media Mol. Imaging5(4), 180–189 (2010).
[CrossRef] [PubMed]

Bec, J.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

Berezin, M. Y.

M. Y. Berezin and S. Achilefu, “Fluorescence lifetime measurements and biological imaging,” Chem. Rev.110(5), 2641–2684 (2010).
[CrossRef] [PubMed]

Bhattar, V. S.

M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
[CrossRef] [PubMed]

Bhavanandan, V. P.

V. P. Bhavanandan, N. J. Ringler, and D. C. Gowda, “Identification of the glycosidically bound sialic acid in mucin glycoproteins that reacts as “free sialic acid” in the Warren assay,” Glycobiology8(11), 1077–1086 (1998).
[CrossRef] [PubMed]

Brandon, J. L.

J. A. Jo, B. E. Applegate, J. Park, S. Shrestha, P. Pande, I. B. Gimenez-Conti, and J. L. Brandon, “In vivo simultaneous morphological and biochemical optical imaging of oral epithelial cancer,” IEEE. T Biomed. Eng. (N.Y.)57, 2596–2599 (2010).

Brenner, M.

W. G. Jung, J. Zhang, J. R. Chung, P. Wilder-Smith, M. Brenner, J. S. Nelson, and Z. P. Chen, “Advances in oral cancer detection using optical coherence tomography,” IEEE J Sel Top Quantum Electron.11(4), 811–817 (2005).
[CrossRef]

Chaudhari, A. J.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

Chen, Z. P.

W. G. Jung, J. Zhang, J. R. Chung, P. Wilder-Smith, M. Brenner, J. S. Nelson, and Z. P. Chen, “Advances in oral cancer detection using optical coherence tomography,” IEEE J Sel Top Quantum Electron.11(4), 811–817 (2005).
[CrossRef]

Chi, T.-T.

Chiang, C.-P.

Chuang, F. S.

Chung, J. R.

W. G. Jung, J. Zhang, J. R. Chung, P. Wilder-Smith, M. Brenner, J. S. Nelson, and Z. P. Chen, “Advances in oral cancer detection using optical coherence tomography,” IEEE J Sel Top Quantum Electron.11(4), 811–817 (2005).
[CrossRef]

Coffman, H.

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[CrossRef] [PubMed]

Cohen, I. K.

I. K. Cohen, C. W. Moncure, R. J. Witorsch, and R. F. Diegelmann, “Collagen Synthesis in Capsules Surrounding Dimethylbenzanthracene-induced Rat Breast Tumors and the Effect of Pretreatment with β-Aminopropionitrile,” Cancer Res.39(8), 2923–2927 (1979).
[PubMed]

Cole, M. J.

K. C. B. 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]

Coleman, D. J.

F. L. Lizzi, M. Greenebaum, E. J. Feleppa, M. Elbaum, and D. J. Coleman, “Theoretical framework for spectrum analysis in ultrasonic tissue characterization,” J. Acoust. Soc. Am.73(4), 1366–1373 (1983).
[CrossRef] [PubMed]

Day, T. A.

Z. Rumboldt, T. A. Day, and M. Michel, “Imaging of oral cavity cancer,” Oral Oncol.42(9), 854–865 (2006).
[CrossRef] [PubMed]

Diegelmann, R. F.

I. K. Cohen, C. W. Moncure, R. J. Witorsch, and R. F. Diegelmann, “Collagen Synthesis in Capsules Surrounding Dimethylbenzanthracene-induced Rat Breast Tumors and the Effect of Pretreatment with β-Aminopropionitrile,” Cancer Res.39(8), 2923–2927 (1979).
[PubMed]

Ding, A.-A.

Dobbie, A.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

Dowling, K.

K. C. B. 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]

Efimov, I. R.

W. J. Hucker, C. M. Ripplinger, C. P. Fleming, V. V. Fedorov, A. M. Rollins, and I. R. Efimov, “Bimodal biophotonic imaging of the structure-function relationship in cardiac tissue,” J. Biomed. Opt.13(5), 054012 (2008).
[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]

Elbaum, M.

F. L. Lizzi, M. Greenebaum, E. J. Feleppa, M. Elbaum, and D. J. Coleman, “Theoretical framework for spectrum analysis in ultrasonic tissue characterization,” J. Acoust. Soc. Am.73(4), 1366–1373 (1983).
[CrossRef] [PubMed]

Eliceiri, K. W.

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]

Elson, D. S.

Emelianov, S.

S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, and S. Emelianov, “Multiwavelength Photoacoustic Imaging and Plasmon Resonance Coupling of Gold Nanoparticles for Selective Detection of Cancer,” Nano Lett.9(8), 2825–2831 (2009).
[CrossRef] [PubMed]

Enepekides, D. J.

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[CrossRef] [PubMed]

Farwell, D. G.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
[CrossRef] [PubMed]

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[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]

Fedorov, V. V.

W. J. Hucker, C. M. Ripplinger, C. P. Fleming, V. V. Fedorov, A. M. Rollins, and I. R. Efimov, “Bimodal biophotonic imaging of the structure-function relationship in cardiac tissue,” J. Biomed. Opt.13(5), 054012 (2008).
[CrossRef] [PubMed]

Feleppa, E. J.

F. L. Lizzi, M. Greenebaum, E. J. Feleppa, M. Elbaum, and D. J. Coleman, “Theoretical framework for spectrum analysis in ultrasonic tissue characterization,” J. Acoust. Soc. Am.73(4), 1366–1373 (1983).
[CrossRef] [PubMed]

Fischer, F.

V. Lutz, M. Sattler, S. Gallinat, H. Wenck, R. Poertner, and F. Fischer, “Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence,” Skin Res. Technol.18(2), 168–179 (2012).
[CrossRef] [PubMed]

Fleming, C. P.

W. J. Hucker, C. M. Ripplinger, C. P. Fleming, V. V. Fedorov, A. M. Rollins, and I. R. Efimov, “Bimodal biophotonic imaging of the structure-function relationship in cardiac tissue,” J. Biomed. Opt.13(5), 054012 (2008).
[CrossRef] [PubMed]

French, P. M. W.

K. C. B. 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]

Gallinat, S.

V. Lutz, M. Sattler, S. Gallinat, H. Wenck, R. Poertner, and F. Fischer, “Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence,” Skin Res. Technol.18(2), 168–179 (2012).
[CrossRef] [PubMed]

Galvan, J.

K. Sokolov, J. Galvan, A. Myakov, A. Lacy, R. Lotan, and R. Richards-Kortum, “Realistic three-dimensional epithelial tissue phantoms for biomedical optics,” J. Biomed. Opt.7(1), 148–156 (2002).
[CrossRef] [PubMed]

Gandour-Edwards, R. F.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

Gendron-Fitzpatrick, A.

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]

Gillenwater, A.

D. Shin, N. Vigneswaran, A. Gillenwater, and R. Richards-Kortum, “Advances in fluorescence imaging techniques to detect oral cancer and its precursors,” Future Oncol.6(7), 1143–1154 (2010).
[CrossRef] [PubMed]

Gillenwater, A. M.

M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
[CrossRef] [PubMed]

Gimenez-Conti, I. B.

J. A. Jo, B. E. Applegate, J. Park, S. Shrestha, P. Pande, I. B. Gimenez-Conti, and J. L. Brandon, “In vivo simultaneous morphological and biochemical optical imaging of oral epithelial cancer,” IEEE. T Biomed. Eng. (N.Y.)57, 2596–2599 (2010).

I. B. Gimenez-Conti and T. J. Slaga, “The Hamster Cheek Pouch Carcinogenesis Model,” J. Cell. Biochem. Suppl.17F(S17F), 83–90 (1993).
[CrossRef] [PubMed]

Gnecco, C. A.

R. H. Spiro, A. G. Huvos, G. Y. Wong, J. D. Spiro, C. A. Gnecco, and E. W. Strong, “Predictive value of tumor thickness in squamous carcinoma confined to the tongue and floor of the mouth,” Am. J. Surg.152(4), 345–350 (1986).
[CrossRef] [PubMed]

Goldstein, D. P.

S. H. Huang, D. Hwang, G. Lockwood, D. P. Goldstein, and B. O’Sullivan, “Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta-analysis of reported studies,” Cancer115(7), 1489–1497 (2009).
[CrossRef] [PubMed]

Gowda, D. C.

V. P. Bhavanandan, N. J. Ringler, and D. C. Gowda, “Identification of the glycosidically bound sialic acid in mucin glycoproteins that reacts as “free sialic acid” in the Warren assay,” Glycobiology8(11), 1077–1086 (1998).
[CrossRef] [PubMed]

Greenebaum, M.

F. L. Lizzi, M. Greenebaum, E. J. Feleppa, M. Elbaum, and D. J. Coleman, “Theoretical framework for spectrum analysis in ultrasonic tissue characterization,” J. Acoust. Soc. Am.73(4), 1366–1373 (1983).
[CrossRef] [PubMed]

Hagiwara, M.

M. Hagiwara, A. Nusbaum, and B. L. Schmidt, “MR Assessment of Oral Cavity Carcinomas,” Magn. Reson. Imaging Clin. N. Am.20(3), 473–494 (2012).
[CrossRef] [PubMed]

Harmelin, A.

V. Kalchenko, N. Madar-Balakirski, I. Meglinski, and A. Harmelin, “In vivo characterization of tumor and tumor vascular network using multi-modal imaging approach,” J Biophotonics4(9), 645–649 (2011).
[PubMed]

Hatami, N.

J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
[CrossRef] [PubMed]

Hollars, C. W.

Hollingsworth, M. A.

M. A. Hollingsworth and B. J. Swanson, “Mucins in cancer: protection and control of the cell surface,” Nat. Rev. Cancer4(1), 45–60 (2004).
[CrossRef] [PubMed]

Huang, S. H.

S. H. Huang, D. Hwang, G. Lockwood, D. P. Goldstein, and B. O’Sullivan, “Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta-analysis of reported studies,” Cancer115(7), 1489–1497 (2009).
[CrossRef] [PubMed]

Hucker, W. J.

W. J. Hucker, C. M. Ripplinger, C. P. Fleming, V. V. Fedorov, A. M. Rollins, and I. R. Efimov, “Bimodal biophotonic imaging of the structure-function relationship in cardiac tissue,” J. Biomed. Opt.13(5), 054012 (2008).
[CrossRef] [PubMed]

Huvos, A. G.

R. H. Spiro, A. G. Huvos, G. Y. Wong, J. D. Spiro, C. A. Gnecco, and E. W. Strong, “Predictive value of tumor thickness in squamous carcinoma confined to the tongue and floor of the mouth,” Am. J. Surg.152(4), 345–350 (1986).
[CrossRef] [PubMed]

Hwang, D.

S. H. Huang, D. Hwang, G. Lockwood, D. P. Goldstein, and B. O’Sullivan, “Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta-analysis of reported studies,” Cancer115(7), 1489–1497 (2009).
[CrossRef] [PubMed]

James, C.

J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
[PubMed]

Jemal, A.

R. Siegel, D. Naishadham, and A. Jemal, “Cancer statistics, 2013,” CA Cancer J. Clin.63(1), 11–30 (2013).
[CrossRef] [PubMed]

Jhan, S.

Jo, J. A.

J. A. Jo, B. E. Applegate, J. Park, S. Shrestha, P. Pande, I. B. Gimenez-Conti, and J. L. Brandon, “In vivo simultaneous morphological and biochemical optical imaging of oral epithelial cancer,” IEEE. T Biomed. Eng. (N.Y.)57, 2596–2599 (2010).

Y. Sun, R. Liu, D. S. Elson, C. W. Hollars, J. A. Jo, J. Park, Y. Sun, and L. Marcu, “Simultaneous time- and wavelength-resolved fluorescence spectroscopy for near real-time tissue diagnosis,” Opt. Lett.33(6), 630–632 (2008).
[CrossRef] [PubMed]

Jones, R.

K. C. B. 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]

Joshi, P. P.

S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, and S. Emelianov, “Multiwavelength Photoacoustic Imaging and Plasmon Resonance Coupling of Gold Nanoparticles for Selective Detection of Cancer,” Nano Lett.9(8), 2825–2831 (2009).
[CrossRef] [PubMed]

Jung, W. G.

W. G. Jung, J. Zhang, J. R. Chung, P. Wilder-Smith, M. Brenner, J. S. Nelson, and Z. P. Chen, “Advances in oral cancer detection using optical coherence tomography,” IEEE J Sel Top Quantum Electron.11(4), 811–817 (2005).
[CrossRef]

Kah, J. C.

J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
[PubMed]

Kalchenko, V.

V. Kalchenko, N. Madar-Balakirski, I. Meglinski, and A. Harmelin, “In vivo characterization of tumor and tumor vascular network using multi-modal imaging approach,” J Biophotonics4(9), 645–649 (2011).
[PubMed]

Karpiouk, A.

S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, and S. Emelianov, “Multiwavelength Photoacoustic Imaging and Plasmon Resonance Coupling of Gold Nanoparticles for Selective Detection of Cancer,” Nano Lett.9(8), 2825–2831 (2009).
[CrossRef] [PubMed]

Kho, K. W.

J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
[PubMed]

Lacy, A.

K. Sokolov, J. Galvan, A. Myakov, A. Lacy, R. Lotan, and R. Richards-Kortum, “Realistic three-dimensional epithelial tissue phantoms for biomedical optics,” J. Biomed. Opt.7(1), 148–156 (2002).
[CrossRef] [PubMed]

Lam, M.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

Lamonica, D.

L. L. Myers, M. K. Wax, H. Nabi, G. T. Simpson, and D. Lamonica, “Positron Emission Tomography in the Evaluation of the N0 Neck,” Laryngoscope108(2), 232–236 (1998).
[CrossRef] [PubMed]

Larson, T.

S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, and S. Emelianov, “Multiwavelength Photoacoustic Imaging and Plasmon Resonance Coupling of Gold Nanoparticles for Selective Detection of Cancer,” Nano Lett.9(8), 2825–2831 (2009).
[CrossRef] [PubMed]

Lee, C. G.

J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
[PubMed]

Lee, C.-K.

Lee, J. J.

M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
[CrossRef] [PubMed]

Lee, K. C. B.

K. C. B. 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]

Lévêque-Fort, S.

K. C. B. 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]

Lever, M. J.

K. C. B. 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]

Li, P.-C.

Liao, C.-K.

Liu, J.

J. Liu, Y. Sun, J. Qi, and L. Marcu, “A novel method for fast and robust estimation of fluorescence decay dynamics using constrained least-squares deconvolution with Laguerre expansion,” Phys. Med. Biol.57(4), 843–865 (2012).
[CrossRef] [PubMed]

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

Liu, R.

Lizzi, F. L.

F. L. Lizzi, M. Greenebaum, E. J. Feleppa, M. Elbaum, and D. J. Coleman, “Theoretical framework for spectrum analysis in ultrasonic tissue characterization,” J. Acoust. Soc. Am.73(4), 1366–1373 (1983).
[CrossRef] [PubMed]

Lockwood, G.

S. H. Huang, D. Hwang, G. Lockwood, D. P. Goldstein, and B. O’Sullivan, “Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta-analysis of reported studies,” Cancer115(7), 1489–1497 (2009).
[CrossRef] [PubMed]

Lodder, W. L.

W. L. Lodder, H. J. Teertstra, I. B. Tan, F. A. Pameijer, L. E. Smeele, M. L. F. van Velthuysen, and M. W. M. van den Brekel, “Tumour thickness in oral cancer using an intra-oral ultrasound probe,” Eur. Radiol.21(1), 98–106 (2011).
[CrossRef] [PubMed]

Lotan, R.

K. Sokolov, J. Galvan, A. Myakov, A. Lacy, R. Lotan, and R. Richards-Kortum, “Realistic three-dimensional epithelial tissue phantoms for biomedical optics,” J. Biomed. Opt.7(1), 148–156 (2002).
[CrossRef] [PubMed]

Lutz, V.

V. Lutz, M. Sattler, S. Gallinat, H. Wenck, R. Poertner, and F. Fischer, “Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence,” Skin Res. Technol.18(2), 168–179 (2012).
[CrossRef] [PubMed]

Madar-Balakirski, N.

V. Kalchenko, N. Madar-Balakirski, I. Meglinski, and A. Harmelin, “In vivo characterization of tumor and tumor vascular network using multi-modal imaging approach,” J Biophotonics4(9), 645–649 (2011).
[PubMed]

Mallidi, S.

S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, and S. Emelianov, “Multiwavelength Photoacoustic Imaging and Plasmon Resonance Coupling of Gold Nanoparticles for Selective Detection of Cancer,” Nano Lett.9(8), 2825–2831 (2009).
[CrossRef] [PubMed]

Marcu, L.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

J. Liu, Y. Sun, J. Qi, and L. Marcu, “A novel method for fast and robust estimation of fluorescence decay dynamics using constrained least-squares deconvolution with Laguerre expansion,” Phys. Med. Biol.57(4), 843–865 (2012).
[CrossRef] [PubMed]

Y. H. Sun, Y. Sun, D. Stephens, H. T. Xie, J. Phipps, R. Saroufeem, J. Southard, D. S. Elson, and L. Marcu, “Dynamic tissue analysis using time- and wavelength-resolved fluorescence spectroscopy for atherosclerosis diagnosis,” Opt. Express19(5), 3890–3901 (2011).
[CrossRef] [PubMed]

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[CrossRef] [PubMed]

J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
[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]

Y. Sun, R. Liu, D. S. Elson, C. W. Hollars, J. A. Jo, J. Park, Y. Sun, and L. Marcu, “Simultaneous time- and wavelength-resolved fluorescence spectroscopy for near real-time tissue diagnosis,” Opt. Lett.33(6), 630–632 (2008).
[CrossRef] [PubMed]

Martí-Bonmatí, L.

L. Martí-Bonmatí, R. Sopena, P. Bartumeus, and P. Sopena, “Multimodality imaging techniques,” Contrast Media Mol. Imaging5(4), 180–189 (2010).
[CrossRef] [PubMed]

Meglinski, I.

V. Kalchenko, N. Madar-Balakirski, I. Meglinski, and A. Harmelin, “In vivo characterization of tumor and tumor vascular network using multi-modal imaging approach,” J Biophotonics4(9), 645–649 (2011).
[PubMed]

Meier, J.

Meier, J. D.

J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
[CrossRef] [PubMed]

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[CrossRef] [PubMed]

Michel, M.

Z. Rumboldt, T. A. Day, and M. Michel, “Imaging of oral cavity cancer,” Oral Oncol.42(9), 854–865 (2006).
[CrossRef] [PubMed]

Moncure, C. W.

I. K. Cohen, C. W. Moncure, R. J. Witorsch, and R. F. Diegelmann, “Collagen Synthesis in Capsules Surrounding Dimethylbenzanthracene-induced Rat Breast Tumors and the Effect of Pretreatment with β-Aminopropionitrile,” Cancer Res.39(8), 2923–2927 (1979).
[PubMed]

Mondrik, S.

M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
[CrossRef] [PubMed]

Monsky, W. L.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

Mukherjee, S.

B. M. Trotta, C. S. Pease, J. J. Rasamny, P. Raghavan, and S. Mukherjee, “Oral cavity and oropharyngeal squamous cell cancer: key imaging findings for staging and treatment planning,” Radiographics31(2), 339–354 (2011).
[CrossRef] [PubMed]

Myakov, A.

K. Sokolov, J. Galvan, A. Myakov, A. Lacy, R. Lotan, and R. Richards-Kortum, “Realistic three-dimensional epithelial tissue phantoms for biomedical optics,” J. Biomed. Opt.7(1), 148–156 (2002).
[CrossRef] [PubMed]

Myers, L. L.

L. L. Myers, M. K. Wax, H. Nabi, G. T. Simpson, and D. Lamonica, “Positron Emission Tomography in the Evaluation of the N0 Neck,” Laryngoscope108(2), 232–236 (1998).
[CrossRef] [PubMed]

Nabi, H.

L. L. Myers, M. K. Wax, H. Nabi, G. T. Simpson, and D. Lamonica, “Positron Emission Tomography in the Evaluation of the N0 Neck,” Laryngoscope108(2), 232–236 (1998).
[CrossRef] [PubMed]

Naishadham, D.

R. Siegel, D. Naishadham, and A. Jemal, “Cancer statistics, 2013,” CA Cancer J. Clin.63(1), 11–30 (2013).
[CrossRef] [PubMed]

Nelson, J. S.

W. G. Jung, J. Zhang, J. R. Chung, P. Wilder-Smith, M. Brenner, J. S. Nelson, and Z. P. Chen, “Advances in oral cancer detection using optical coherence tomography,” IEEE J Sel Top Quantum Electron.11(4), 811–817 (2005).
[CrossRef]

Niedre, M.

M. Niedre and V. Ntziachristos, “Elucidating Structure and Function In Vivo With Hybrid Fluorescence and Magnetic Resonance Imaging,” Proc. IEEE96(3), 382–396 (2008).
[CrossRef]

Ntziachristos, V.

M. Niedre and V. Ntziachristos, “Elucidating Structure and Function In Vivo With Hybrid Fluorescence and Magnetic Resonance Imaging,” Proc. IEEE96(3), 382–396 (2008).
[CrossRef]

Nusbaum, A.

M. Hagiwara, A. Nusbaum, and B. L. Schmidt, “MR Assessment of Oral Cavity Carcinomas,” Magn. Reson. Imaging Clin. N. Am.20(3), 473–494 (2012).
[CrossRef] [PubMed]

O’Sullivan, B.

S. H. Huang, D. Hwang, G. Lockwood, D. P. Goldstein, and B. O’Sullivan, “Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta-analysis of reported studies,” Cancer115(7), 1489–1497 (2009).
[CrossRef] [PubMed]

Olivo, M. C.

J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
[PubMed]

Pameijer, F. A.

W. L. Lodder, H. J. Teertstra, I. B. Tan, F. A. Pameijer, L. E. Smeele, M. L. F. van Velthuysen, and M. W. M. van den Brekel, “Tumour thickness in oral cancer using an intra-oral ultrasound probe,” Eur. Radiol.21(1), 98–106 (2011).
[CrossRef] [PubMed]

Pande, P.

J. A. Jo, B. E. Applegate, J. Park, S. Shrestha, P. Pande, I. B. Gimenez-Conti, and J. L. Brandon, “In vivo simultaneous morphological and biochemical optical imaging of oral epithelial cancer,” IEEE. T Biomed. Eng. (N.Y.)57, 2596–2599 (2010).

Park, J.

J. A. Jo, B. E. Applegate, J. Park, S. Shrestha, P. Pande, I. B. Gimenez-Conti, and J. L. Brandon, “In vivo simultaneous morphological and biochemical optical imaging of oral epithelial cancer,” IEEE. T Biomed. Eng. (N.Y.)57, 2596–2599 (2010).

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[CrossRef] [PubMed]

Y. Sun, R. Liu, D. S. Elson, C. W. Hollars, J. A. Jo, J. Park, Y. Sun, and L. Marcu, “Simultaneous time- and wavelength-resolved fluorescence spectroscopy for near real-time tissue diagnosis,” Opt. Lett.33(6), 630–632 (2008).
[CrossRef] [PubMed]

Pease, C. S.

B. M. Trotta, C. S. Pease, J. J. Rasamny, P. Raghavan, and S. Mukherjee, “Oral cavity and oropharyngeal squamous cell cancer: key imaging findings for staging and treatment planning,” Radiographics31(2), 339–354 (2011).
[CrossRef] [PubMed]

Phipps, J.

Pierce, M. C.

M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
[CrossRef] [PubMed]

Poe, C.

Poertner, R.

V. Lutz, M. Sattler, S. Gallinat, H. Wenck, R. Poertner, and F. Fischer, “Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence,” Skin Res. Technol.18(2), 168–179 (2012).
[CrossRef] [PubMed]

Poirier, B.

J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
[CrossRef] [PubMed]

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[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]

Qi, J.

J. Liu, Y. Sun, J. Qi, and L. Marcu, “A novel method for fast and robust estimation of fluorescence decay dynamics using constrained least-squares deconvolution with Laguerre expansion,” Phys. Med. Biol.57(4), 843–865 (2012).
[CrossRef] [PubMed]

Raghavan, P.

B. M. Trotta, C. S. Pease, J. J. Rasamny, P. Raghavan, and S. Mukherjee, “Oral cavity and oropharyngeal squamous cell cancer: key imaging findings for staging and treatment planning,” Radiographics31(2), 339–354 (2011).
[CrossRef] [PubMed]

Ramanujam, N.

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]

Rasamny, J. J.

B. M. Trotta, C. S. Pease, J. J. Rasamny, P. Raghavan, and S. Mukherjee, “Oral cavity and oropharyngeal squamous cell cancer: key imaging findings for staging and treatment planning,” Radiographics31(2), 339–354 (2011).
[CrossRef] [PubMed]

Richards-Kortum, R.

M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
[CrossRef] [PubMed]

D. Shin, N. Vigneswaran, A. Gillenwater, and R. Richards-Kortum, “Advances in fluorescence imaging techniques to detect oral cancer and its precursors,” Future Oncol.6(7), 1143–1154 (2010).
[CrossRef] [PubMed]

K. Sokolov, J. Galvan, A. Myakov, A. Lacy, R. Lotan, and R. Richards-Kortum, “Realistic three-dimensional epithelial tissue phantoms for biomedical optics,” J. Biomed. Opt.7(1), 148–156 (2002).
[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]

Ringler, N. J.

V. P. Bhavanandan, N. J. Ringler, and D. C. Gowda, “Identification of the glycosidically bound sialic acid in mucin glycoproteins that reacts as “free sialic acid” in the Warren assay,” Glycobiology8(11), 1077–1086 (1998).
[CrossRef] [PubMed]

Ripplinger, C. M.

W. J. Hucker, C. M. Ripplinger, C. P. Fleming, V. V. Fedorov, A. M. Rollins, and I. R. Efimov, “Bimodal biophotonic imaging of the structure-function relationship in cardiac tissue,” J. Biomed. Opt.13(5), 054012 (2008).
[CrossRef] [PubMed]

Rollins, A. M.

W. J. Hucker, C. M. Ripplinger, C. P. Fleming, V. V. Fedorov, A. M. Rollins, and I. R. Efimov, “Bimodal biophotonic imaging of the structure-function relationship in cardiac tissue,” J. Biomed. Opt.13(5), 054012 (2008).
[CrossRef] [PubMed]

Rubinstein, D.

L. L. Simon and D. Rubinstein, “Imaging of oral cancer,” Otolaryngol. Clin. North Am.39(2), 307–317, vi (2006).
[CrossRef] [PubMed]

Rumboldt, Z.

Z. Rumboldt, T. A. Day, and M. Michel, “Imaging of oral cavity cancer,” Oral Oncol.42(9), 854–865 (2006).
[CrossRef] [PubMed]

Salley, J. J.

J. J. Salley, “Experimental Carcinogenesis in the Cheek Pouch of the Syrian Hamster,” J. Dent. Res.33(2), 253–262 (1954).
[CrossRef] [PubMed]

Saroufeem, R.

Sattler, M.

V. Lutz, M. Sattler, S. Gallinat, H. Wenck, R. Poertner, and F. Fischer, “Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence,” Skin Res. Technol.18(2), 168–179 (2012).
[CrossRef] [PubMed]

Schmidt, B. L.

M. Hagiwara, A. Nusbaum, and B. L. Schmidt, “MR Assessment of Oral Cavity Carcinomas,” Magn. Reson. Imaging Clin. N. Am.20(3), 473–494 (2012).
[CrossRef] [PubMed]

Schwarz, R. A.

M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
[CrossRef] [PubMed]

Shen, Z. X.

J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
[PubMed]

Sheppard, R.

J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
[PubMed]

Shieh, D.-B.

Shin, D.

D. Shin, N. Vigneswaran, A. Gillenwater, and R. Richards-Kortum, “Advances in fluorescence imaging techniques to detect oral cancer and its precursors,” Future Oncol.6(7), 1143–1154 (2010).
[CrossRef] [PubMed]

Shrestha, S.

J. A. Jo, B. E. Applegate, J. Park, S. Shrestha, P. Pande, I. B. Gimenez-Conti, and J. L. Brandon, “In vivo simultaneous morphological and biochemical optical imaging of oral epithelial cancer,” IEEE. T Biomed. Eng. (N.Y.)57, 2596–2599 (2010).

Siegel, J.

K. C. B. 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]

Siegel, R.

R. Siegel, D. Naishadham, and A. Jemal, “Cancer statistics, 2013,” CA Cancer J. Clin.63(1), 11–30 (2013).
[CrossRef] [PubMed]

Simon, L. L.

L. L. Simon and D. Rubinstein, “Imaging of oral cancer,” Otolaryngol. Clin. North Am.39(2), 307–317, vi (2006).
[CrossRef] [PubMed]

Simpson, G. T.

L. L. Myers, M. K. Wax, H. Nabi, G. T. Simpson, and D. Lamonica, “Positron Emission Tomography in the Evaluation of the N0 Neck,” Laryngoscope108(2), 232–236 (1998).
[CrossRef] [PubMed]

Skala, M. C.

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]

Slaga, T. J.

I. B. Gimenez-Conti and T. J. Slaga, “The Hamster Cheek Pouch Carcinogenesis Model,” J. Cell. Biochem. Suppl.17F(S17F), 83–90 (1993).
[CrossRef] [PubMed]

Smeele, L. E.

W. L. Lodder, H. J. Teertstra, I. B. Tan, F. A. Pameijer, L. E. Smeele, M. L. F. van Velthuysen, and M. W. M. van den Brekel, “Tumour thickness in oral cancer using an intra-oral ultrasound probe,” Eur. Radiol.21(1), 98–106 (2011).
[CrossRef] [PubMed]

Sokolov, K.

S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, and S. Emelianov, “Multiwavelength Photoacoustic Imaging and Plasmon Resonance Coupling of Gold Nanoparticles for Selective Detection of Cancer,” Nano Lett.9(8), 2825–2831 (2009).
[CrossRef] [PubMed]

K. Sokolov, J. Galvan, A. Myakov, A. Lacy, R. Lotan, and R. Richards-Kortum, “Realistic three-dimensional epithelial tissue phantoms for biomedical optics,” J. Biomed. Opt.7(1), 148–156 (2002).
[CrossRef] [PubMed]

Soo, K. C.

J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
[PubMed]

Sopena, P.

L. Martí-Bonmatí, R. Sopena, P. Bartumeus, and P. Sopena, “Multimodality imaging techniques,” Contrast Media Mol. Imaging5(4), 180–189 (2010).
[CrossRef] [PubMed]

Sopena, R.

L. Martí-Bonmatí, R. Sopena, P. Bartumeus, and P. Sopena, “Multimodality imaging techniques,” Contrast Media Mol. Imaging5(4), 180–189 (2010).
[CrossRef] [PubMed]

Southard, J.

Spiro, J. D.

R. H. Spiro, A. G. Huvos, G. Y. Wong, J. D. Spiro, C. A. Gnecco, and E. W. Strong, “Predictive value of tumor thickness in squamous carcinoma confined to the tongue and floor of the mouth,” Am. J. Surg.152(4), 345–350 (1986).
[CrossRef] [PubMed]

Spiro, R. H.

R. H. Spiro, A. G. Huvos, G. Y. Wong, J. D. Spiro, C. A. Gnecco, and E. W. Strong, “Predictive value of tumor thickness in squamous carcinoma confined to the tongue and floor of the mouth,” Am. J. Surg.152(4), 345–350 (1986).
[CrossRef] [PubMed]

Stephens, D.

Stoy, H.

Strong, E. W.

R. H. Spiro, A. G. Huvos, G. Y. Wong, J. D. Spiro, C. A. Gnecco, and E. W. Strong, “Predictive value of tumor thickness in squamous carcinoma confined to the tongue and floor of the mouth,” Am. J. Surg.152(4), 345–350 (1986).
[CrossRef] [PubMed]

Sun, Y.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

J. Liu, Y. Sun, J. Qi, and L. Marcu, “A novel method for fast and robust estimation of fluorescence decay dynamics using constrained least-squares deconvolution with Laguerre expansion,” Phys. Med. Biol.57(4), 843–865 (2012).
[CrossRef] [PubMed]

Y. H. Sun, Y. Sun, D. Stephens, H. T. Xie, J. Phipps, R. Saroufeem, J. Southard, D. S. Elson, and L. Marcu, “Dynamic tissue analysis using time- and wavelength-resolved fluorescence spectroscopy for atherosclerosis diagnosis,” Opt. Express19(5), 3890–3901 (2011).
[CrossRef] [PubMed]

J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
[CrossRef] [PubMed]

J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
[CrossRef] [PubMed]

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[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]

Y. Sun, R. Liu, D. S. Elson, C. W. Hollars, J. A. Jo, J. Park, Y. Sun, and L. Marcu, “Simultaneous time- and wavelength-resolved fluorescence spectroscopy for near real-time tissue diagnosis,” Opt. Lett.33(6), 630–632 (2008).
[CrossRef] [PubMed]

Y. Sun, R. Liu, D. S. Elson, C. W. Hollars, J. A. Jo, J. Park, Y. Sun, and L. Marcu, “Simultaneous time- and wavelength-resolved fluorescence spectroscopy for near real-time tissue diagnosis,” Opt. Lett.33(6), 630–632 (2008).
[CrossRef] [PubMed]

Sun, Y. H.

Swanson, B. J.

M. A. Hollingsworth and B. J. Swanson, “Mucins in cancer: protection and control of the cell surface,” Nat. Rev. Cancer4(1), 45–60 (2004).
[CrossRef] [PubMed]

Tam, J.

S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, and S. Emelianov, “Multiwavelength Photoacoustic Imaging and Plasmon Resonance Coupling of Gold Nanoparticles for Selective Detection of Cancer,” Nano Lett.9(8), 2825–2831 (2009).
[CrossRef] [PubMed]

Tan, I. B.

W. L. Lodder, H. J. Teertstra, I. B. Tan, F. A. Pameijer, L. E. Smeele, M. L. F. van Velthuysen, and M. W. M. van den Brekel, “Tumour thickness in oral cancer using an intra-oral ultrasound probe,” Eur. Radiol.21(1), 98–106 (2011).
[CrossRef] [PubMed]

Teertstra, H. J.

W. L. Lodder, H. J. Teertstra, I. B. Tan, F. A. Pameijer, L. E. Smeele, M. L. F. van Velthuysen, and M. W. M. van den Brekel, “Tumour thickness in oral cancer using an intra-oral ultrasound probe,” Eur. Radiol.21(1), 98–106 (2011).
[CrossRef] [PubMed]

Tinling, S.

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[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]

Tinling, S. L.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

Trotta, B. M.

B. M. Trotta, C. S. Pease, J. J. Rasamny, P. Raghavan, and S. Mukherjee, “Oral cavity and oropharyngeal squamous cell cancer: key imaging findings for staging and treatment planning,” Radiographics31(2), 339–354 (2011).
[CrossRef] [PubMed]

Tsai, M.-T.

van den Brekel, M. W. M.

W. L. Lodder, H. J. Teertstra, I. B. Tan, F. A. Pameijer, L. E. Smeele, M. L. F. van Velthuysen, and M. W. M. van den Brekel, “Tumour thickness in oral cancer using an intra-oral ultrasound probe,” Eur. Radiol.21(1), 98–106 (2011).
[CrossRef] [PubMed]

van Velthuysen, M. L. F.

W. L. Lodder, H. J. Teertstra, I. B. Tan, F. A. Pameijer, L. E. Smeele, M. L. F. van Velthuysen, and M. W. M. van den Brekel, “Tumour thickness in oral cancer using an intra-oral ultrasound probe,” Eur. Radiol.21(1), 98–106 (2011).
[CrossRef] [PubMed]

Vigneswaran, N.

D. Shin, N. Vigneswaran, A. Gillenwater, and R. Richards-Kortum, “Advances in fluorescence imaging techniques to detect oral cancer and its precursors,” Future Oncol.6(7), 1143–1154 (2010).
[CrossRef] [PubMed]

Wang, C.-R. C.

Wang, L. H. V.

M. H. Xu and L. H. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum.77(4), 041101 (2006).
[CrossRef]

Wax, M. K.

L. L. Myers, M. K. Wax, H. Nabi, G. T. Simpson, and D. Lamonica, “Positron Emission Tomography in the Evaluation of the N0 Neck,” Laryngoscope108(2), 232–236 (1998).
[CrossRef] [PubMed]

Webb, S. E. D.

K. C. B. 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]

Wei, C.-W.

Wenck, H.

V. Lutz, M. Sattler, S. Gallinat, H. Wenck, R. Poertner, and F. Fischer, “Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence,” Skin Res. Technol.18(2), 168–179 (2012).
[CrossRef] [PubMed]

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]

Wilder-Smith, P.

W. G. Jung, J. Zhang, J. R. Chung, P. Wilder-Smith, M. Brenner, J. S. Nelson, and Z. P. Chen, “Advances in oral cancer detection using optical coherence tomography,” IEEE J Sel Top Quantum Electron.11(4), 811–817 (2005).
[CrossRef]

Williams, M. D.

M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
[CrossRef] [PubMed]

Witorsch, R. J.

I. K. Cohen, C. W. Moncure, R. J. Witorsch, and R. F. Diegelmann, “Collagen Synthesis in Capsules Surrounding Dimethylbenzanthracene-induced Rat Breast Tumors and the Effect of Pretreatment with β-Aminopropionitrile,” Cancer Res.39(8), 2923–2927 (1979).
[PubMed]

Wong, G. Y.

R. H. Spiro, A. G. Huvos, G. Y. Wong, J. D. Spiro, C. A. Gnecco, and E. W. Strong, “Predictive value of tumor thickness in squamous carcinoma confined to the tongue and floor of the mouth,” Am. J. Surg.152(4), 345–350 (1986).
[CrossRef] [PubMed]

Wu, C.-T.

Wu, Y.-N.

Xie, H.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
[CrossRef] [PubMed]

Xie, H. T.

Xu, M. H.

M. H. Xu and L. H. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum.77(4), 041101 (2006).
[CrossRef]

Yang, C.-C.

Yankelevich, D. R.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

Zhang, J.

W. G. Jung, J. Zhang, J. R. Chung, P. Wilder-Smith, M. Brenner, J. S. Nelson, and Z. P. Chen, “Advances in oral cancer detection using optical coherence tomography,” IEEE J Sel Top Quantum Electron.11(4), 811–817 (2005).
[CrossRef]

Zhou, F.

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

Am. J. Surg.

R. H. Spiro, A. G. Huvos, G. Y. Wong, J. D. Spiro, C. A. Gnecco, and E. W. Strong, “Predictive value of tumor thickness in squamous carcinoma confined to the tongue and floor of the mouth,” Am. J. Surg.152(4), 345–350 (1986).
[CrossRef] [PubMed]

Arch. Otolaryngol. Head Neck Surg.

D. G. Farwell, J. D. Meier, J. Park, Y. Sun, H. Coffman, B. Poirier, J. Phipps, S. Tinling, D. J. Enepekides, and L. Marcu, “Time-Resolved Fluorescence Spectroscopy as a Diagnostic Technique of Oral Carcinoma: Validation in the Hamster Buccal Pouch Model,” Arch. Otolaryngol. Head Neck Surg.136(2), 126–133 (2010).
[CrossRef] [PubMed]

Biomed. Opt. Express

Biophys. J.

K. C. B. 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]

CA Cancer J. Clin.

R. Siegel, D. Naishadham, and A. Jemal, “Cancer statistics, 2013,” CA Cancer J. Clin.63(1), 11–30 (2013).
[CrossRef] [PubMed]

Cancer

S. H. Huang, D. Hwang, G. Lockwood, D. P. Goldstein, and B. O’Sullivan, “Predictive value of tumor thickness for cervical lymph-node involvement in squamous cell carcinoma of the oral cavity: a meta-analysis of reported studies,” Cancer115(7), 1489–1497 (2009).
[CrossRef] [PubMed]

Cancer Prev. Res. (Phila.)

M. C. Pierce, R. A. Schwarz, V. S. Bhattar, S. Mondrik, M. D. Williams, J. J. Lee, R. Richards-Kortum, and A. M. Gillenwater, “Accuracy of in vivo multimodal optical imaging for detection of oral neoplasia,” Cancer Prev. Res. (Phila.)5(6), 801–809 (2012).
[CrossRef] [PubMed]

Cancer Res.

I. K. Cohen, C. W. Moncure, R. J. Witorsch, and R. F. Diegelmann, “Collagen Synthesis in Capsules Surrounding Dimethylbenzanthracene-induced Rat Breast Tumors and the Effect of Pretreatment with β-Aminopropionitrile,” Cancer Res.39(8), 2923–2927 (1979).
[PubMed]

Chem. Rev.

M. Y. Berezin and S. Achilefu, “Fluorescence lifetime measurements and biological imaging,” Chem. Rev.110(5), 2641–2684 (2010).
[CrossRef] [PubMed]

Contrast Media Mol. Imaging

L. Martí-Bonmatí, R. Sopena, P. Bartumeus, and P. Sopena, “Multimodality imaging techniques,” Contrast Media Mol. Imaging5(4), 180–189 (2010).
[CrossRef] [PubMed]

Eur. Radiol.

W. L. Lodder, H. J. Teertstra, I. B. Tan, F. A. Pameijer, L. E. Smeele, M. L. F. van Velthuysen, and M. W. M. van den Brekel, “Tumour thickness in oral cancer using an intra-oral ultrasound probe,” Eur. Radiol.21(1), 98–106 (2011).
[CrossRef] [PubMed]

Future Oncol.

D. Shin, N. Vigneswaran, A. Gillenwater, and R. Richards-Kortum, “Advances in fluorescence imaging techniques to detect oral cancer and its precursors,” Future Oncol.6(7), 1143–1154 (2010).
[CrossRef] [PubMed]

Glycobiology

V. P. Bhavanandan, N. J. Ringler, and D. C. Gowda, “Identification of the glycosidically bound sialic acid in mucin glycoproteins that reacts as “free sialic acid” in the Warren assay,” Glycobiology8(11), 1077–1086 (1998).
[CrossRef] [PubMed]

IEEE J Sel Top Quantum Electron.

W. G. Jung, J. Zhang, J. R. Chung, P. Wilder-Smith, M. Brenner, J. S. Nelson, and Z. P. Chen, “Advances in oral cancer detection using optical coherence tomography,” IEEE J Sel Top Quantum Electron.11(4), 811–817 (2005).
[CrossRef]

IEEE. T Biomed. Eng. (N.Y.)

J. A. Jo, B. E. Applegate, J. Park, S. Shrestha, P. Pande, I. B. Gimenez-Conti, and J. L. Brandon, “In vivo simultaneous morphological and biochemical optical imaging of oral epithelial cancer,” IEEE. T Biomed. Eng. (N.Y.)57, 2596–2599 (2010).

Int. J. Nanomedicine

J. C. Kah, K. W. Kho, C. G. Lee, C. James, R. Sheppard, Z. X. Shen, K. C. Soo, and M. C. Olivo, “Early diagnosis of oral cancer based on the surface plasmon resonance of gold nanoparticles,” Int. J. Nanomedicine2(4), 785–798 (2007).
[PubMed]

J Biophotonics

V. Kalchenko, N. Madar-Balakirski, I. Meglinski, and A. Harmelin, “In vivo characterization of tumor and tumor vascular network using multi-modal imaging approach,” J Biophotonics4(9), 645–649 (2011).
[PubMed]

J. Acoust. Soc. Am.

F. L. Lizzi, M. Greenebaum, E. J. Feleppa, M. Elbaum, and D. J. Coleman, “Theoretical framework for spectrum analysis in ultrasonic tissue characterization,” J. Acoust. Soc. Am.73(4), 1366–1373 (1983).
[CrossRef] [PubMed]

J. Biomed. Opt.

K. Sokolov, J. Galvan, A. Myakov, A. Lacy, R. Lotan, and R. Richards-Kortum, “Realistic three-dimensional epithelial tissue phantoms for biomedical optics,” J. Biomed. Opt.7(1), 148–156 (2002).
[CrossRef] [PubMed]

Y. Sun, H. Xie, J. Liu, M. Lam, A. J. Chaudhari, F. Zhou, J. Bec, D. R. Yankelevich, A. Dobbie, S. L. Tinling, R. F. Gandour-Edwards, W. L. Monsky, D. G. Farwell, and L. Marcu, “In vivo validation of a bimodal technique combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy for diagnosis of oral carcinoma,” J. Biomed. Opt.17(11), 116003 (2012).
[CrossRef] [PubMed]

W. J. Hucker, C. M. Ripplinger, C. P. Fleming, V. V. Fedorov, A. M. Rollins, and I. R. Efimov, “Bimodal biophotonic imaging of the structure-function relationship in cardiac tissue,” J. Biomed. Opt.13(5), 054012 (2008).
[CrossRef] [PubMed]

J. Cell. Biochem. Suppl.

I. B. Gimenez-Conti and T. J. Slaga, “The Hamster Cheek Pouch Carcinogenesis Model,” J. Cell. Biochem. Suppl.17F(S17F), 83–90 (1993).
[CrossRef] [PubMed]

J. Dent. Res.

J. J. Salley, “Experimental Carcinogenesis in the Cheek Pouch of the Syrian Hamster,” J. Dent. Res.33(2), 253–262 (1954).
[CrossRef] [PubMed]

Laryngoscope

L. L. Myers, M. K. Wax, H. Nabi, G. T. Simpson, and D. Lamonica, “Positron Emission Tomography in the Evaluation of the N0 Neck,” Laryngoscope108(2), 232–236 (1998).
[CrossRef] [PubMed]

Magn. Reson. Imaging Clin. N. Am.

M. Hagiwara, A. Nusbaum, and B. L. Schmidt, “MR Assessment of Oral Cavity Carcinomas,” Magn. Reson. Imaging Clin. N. Am.20(3), 473–494 (2012).
[CrossRef] [PubMed]

Nano Lett.

S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, and S. Emelianov, “Multiwavelength Photoacoustic Imaging and Plasmon Resonance Coupling of Gold Nanoparticles for Selective Detection of Cancer,” Nano Lett.9(8), 2825–2831 (2009).
[CrossRef] [PubMed]

Nat. Rev. Cancer

M. A. Hollingsworth and B. J. Swanson, “Mucins in cancer: protection and control of the cell surface,” Nat. Rev. Cancer4(1), 45–60 (2004).
[CrossRef] [PubMed]

Opt. Express

Opt. Lett.

Oral Oncol.

Z. Rumboldt, T. A. Day, and M. Michel, “Imaging of oral cavity cancer,” Oral Oncol.42(9), 854–865 (2006).
[CrossRef] [PubMed]

Otolaryngol. Clin. North Am.

L. L. Simon and D. Rubinstein, “Imaging of oral cancer,” Otolaryngol. Clin. North Am.39(2), 307–317, vi (2006).
[CrossRef] [PubMed]

Otolaryngol. Head Neck Surg.

J. D. Meier, H. Xie, Y. Sun, Y. Sun, N. Hatami, B. Poirier, L. Marcu, and D. G. Farwell, “Time-resolved laser-induced fluorescence spectroscopy as a diagnostic instrument in head and neck carcinoma,” Otolaryngol. Head Neck Surg.142(6), 838–844 (2010).
[CrossRef] [PubMed]

Phys. Med. Biol.

J. Liu, Y. Sun, J. Qi, and L. Marcu, “A novel method for fast and robust estimation of fluorescence decay dynamics using constrained least-squares deconvolution with Laguerre expansion,” Phys. Med. Biol.57(4), 843–865 (2012).
[CrossRef] [PubMed]

Proc. IEEE

M. Niedre and V. Ntziachristos, “Elucidating Structure and Function In Vivo With Hybrid Fluorescence and Magnetic Resonance Imaging,” Proc. IEEE96(3), 382–396 (2008).
[CrossRef]

Proc. Natl. Acad. Sci. U.S.A.

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]

Radiographics

B. M. Trotta, C. S. Pease, J. J. Rasamny, P. Raghavan, and S. Mukherjee, “Oral cavity and oropharyngeal squamous cell cancer: key imaging findings for staging and treatment planning,” Radiographics31(2), 339–354 (2011).
[CrossRef] [PubMed]

Rev. Sci. Instrum.

M. H. Xu and L. H. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum.77(4), 041101 (2006).
[CrossRef]

Skin Res. Technol.

V. Lutz, M. Sattler, S. Gallinat, H. Wenck, R. Poertner, and F. Fischer, “Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence,” Skin Res. Technol.18(2), 168–179 (2012).
[CrossRef] [PubMed]

Other

N. Howlader, A. M. Noone, M. Krapcho, N. Neyman, R. Aminou, S. F. Altekruse, C. L. Kosary, J. Ruhl, Z. Tatalovich, H. Cho, A. Mariotto, M. P. Eisner, D. R. Lewis, H. S. Chen, E. J. Feuer, and K. A. Cronin, eds., “SEER Cancer Statistics Review, 1975-2009 (Vintage 2009 Populations),” (National Cancer Institute., Bethesda, MD, 2012).

Cited By

OSA participates in CrossRef's Cited-By Linking service. Citing articles from OSA journals and other participating publishers are listed here.

Alert me when this article is cited.


Figures (8)

Fig. 1
Fig. 1

Schematic of the hybrid multimodal scanning FLIm, UBM and PAI system. The system consists of laser source(s), computer unit, FLIm subsystem, UBM/PAI subsystem and the multimodal scanning probe housing the ultrasound transducer, FLIm optical fiber and PAI fibers. Bottom right: (a) picture of the multimodal probe positioned above the hamster cheek pouch, and (b) magnified view of brace and petri-dish over reverted cheek pouch.

Fig. 2
Fig. 2

Normal hamster cheek tissue. FLIm images showing (a) intensity map, (b) average lifetime map, and (c) LC-1 map from two wavelength bands CH1 (390/40 nm) (top) and CH2 (450/45 nm) (bottom); (d) UBM B-mode image and (e) PAI B-mode image; (f) CH1 and (g) CH2 lifetime histogram over the entire imaged region; (h) Picture of hamster cheek with FLIm and PAI imaging region (blue box); (i) Masson’s Trichrome and (j) H&E histological section taken from the black dotted line in (h) and co-registered with UBM and PAI image. Magnified histology image is shown left to (i) and (j) corresponding to the region enclosed by black boxes. Black arrows in magnified trichrome section point to the different layers seen in tissue: E – Epithelium and sub-epithelium connective tissue, M – muscle fiber mucosa, A – adventitial connective tissue which can also be seen in the UBM image. The high intensity signal in the UBM image at the bottom is due to high reflection of ultrasound from the back of the cheek. High PAI signal intensity is seen in regions (white arrows, C, D) that correspond to blood vessels identified in histology (magnified H&E section, arrows C and D). Scale bars are 1 mm.

Fig. 3
Fig. 3

Hamster cheek tissue from precancer group. FLIm images showing fluorescence (a) intensity map, (b) average lifetime map, and (c) LC-1 map from two wavelength bands CH1 (390/40 nm) (top) and CH2 (450/45 nm) (bottom); (d) UBM B-mode image and (e) PAI B-mode image; (f) CH1 and (g) CH2 lifetime histogram showing two distinct lifetime distributions. (h) Picture of hamster cheek; (i) Masson’s Trichrome and (j) H&E histological section taken from the black dotted line in (h) and co-registered with UBM and PAI image. Magnified histology image is shown left to (i) and (j) corresponding to the region enclosed by black boxes. Black arrows in (j) Trichrome section point to A – collagen with muscle fibers, B – pulsatile diverticulum, C – lesion, D – collagen layers with blood vessels which can also be observed in UBM image with varying echogenicities. High PAI signal intensity is seen in regions (white arrows A and D, (e)) that correspond to blood vessels identified in histology (magnified H&E and trichrome section). Scale bars are 1 mm.

Fig. 4
Fig. 4

Hamster cheek tissue from carcinoma group. FLIm images showing fluorescence (a) intensity map, (b) average lifetime map, and (c) LC-1 map from two wavelength bands CH1 (390/40 nm) (top) and CH2 (450/45 nm) (bottom); (d) UBM B-mode image and (e) PAI B-mode image; (f) CH1 and (g) CH2 lifetime histogram showing two distinct lifetime distributions. (h) Picture of hamster cheek; (i) Masson’s Trichrome and (j) H&E histological section taken from the black dotted line cross-section in (h) and co-registered with UBM and PAI image. Magnified histology image is shown left to (i) and (j) corresponding to the region enclosed by black boxes. Histology sections show disruption of tissue structure which is seen in the UBM image as hypoechoic regions. Black arrows (magnified H&E section, A and B) show vascularization and large blood accumulation in the tumor region. High PAI signal intensity is seen in regions (white arrows A and B, (e)) that correspond to vascularization and blood accumulation identified in histology. Scale bars are 1 mm.

Fig. 5
Fig. 5

FLIm, PAI and histology results from a precancer animal case showing mucin accumulation around glands in tissue. 2-D maps of fluorescence (a) intensity and (b) lifetime from CH1 (390/40 nm) showing lowering of lifetime in the region (black arrow) where mucin accumulation is seen in (c) H&E histology section (magnified region shown on right). (d) PAI cross sectional image showing high signal intensity (white arrows, A and D) corresponding to region with vascularization and mucin accumulation as seen in (c) (black arrows).

Fig. 6
Fig. 6

UBM cross sectional images from (a) normal and (b) carcinoma case with corresponding co-registered H&E histology sections shown in (b) and (d) respectively. Tissue structural layers as seen in histology for normal case can also be seen in the UBM image. Similarly, loss of structural arrangement in tumor case is also observed in UBM image (c) which is confirmed in histology (d).

Fig. 7
Fig. 7

Average lifetime values and LC-1 histogram distribution for all normal (5), precancer (3) and invasive carcinoma (4) cases from CH1 (390/40 nm) and CH2 (450/45 nm) fluorescence emission. Data shown is from the entire imaged region.

Fig. 8
Fig. 8

UBM parameters computed from raw RF signals extracted from randomly selected regions of interest in UBM images representing normal, precancer and carcinoma treatments. (a) Backscatter coefficient function with standard deviation; histogram distribution of (b) Integrated backscatter (IB) computed from (a), and (c) Energy norm (E).

Equations (7)

Equations on this page are rendered with MathJax. Learn more.

y(k)= i=0 k I(ki)h(i) ,
h(k)= l=0 L1 c l b l (k;α) ,
τ avg = δt k kh(k) k h(k) .
B c (f)= S S (z,f) S R (z,f) ,
B c dB =10 log 10 | B c (f) | 2 ,
IB= 1 Δf Δf B c dB (f) df.
E= v. v T .

Metrics