Abstract

Optical spectroscopy has proven to be a powerful technique for studying neoplastic transformation in epithelial tissue. Since specific intra-layer precancerous changes originate in the stratified layers of the oral mucosa, layer-resolved analysis will likely improve both our understanding of the mechanism of premalignant transformation, and clinical diagnostic outcomes. However, the native fluorescence signal in linear spectroscopy typically originates from a multi-layered focal volume. In this study, nonlinear spectroscopy was exploited for in vivo layer-resolved discrimination between normal and dysplastic tissue for the first time. Our results revealed numerous intra-layer specific differences.

© 2012 OSA

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2011 (3)

P. Nankivell and H. Mehanna, “Oral dysplasia: biomarkers, treatment, and follow-up,” Curr. Oncol. Rep.13(2), 145–152 (2011).
[CrossRef] [PubMed]

N. J. Durr, C. T. Weisspfennig, B. A. Holfeld, and A. Ben-Yakar, “Maximum imaging depth of two-photon autofluorescence microscopy in epithelial tissues,” J. Biomed. Opt.16(2), 026008 (2011).
[CrossRef] [PubMed]

W. Zheng, D. Li, S. Li, Y. Zeng, Y. Yang, and J. Y. Qu, “Diagnostic value of nonlinear optical signals from collagen matrix in the detection of epithelial precancer,” Opt. Lett.36(18), 3620–3622 (2011).
[CrossRef] [PubMed]

2010 (3)

Z. Zheng-Fei, L. Han-Ping, G. Zhou-Yi, Z. Shuang-Mu, Y. Bi-Ying, and D. Xiao-Yuan, “Second-harmonic generation as a DNA malignancy indicator of prostate glandular epithelial cells,” Chinese Phys. B19(4), 049501 (2010).
[CrossRef]

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]

L. Qiu, D. K. Pleskow, R. Chuttani, E. Vitkin, J. Leyden, N. Ozden, S. Itani, L. Guo, A. Sacks, J. D. Goldsmith, M. D. Modell, E. B. Hanlon, I. Itzkan, and L. T. Perelman, “Multispectral scanning during endoscopy guides biopsy of dysplasia in Barrett’s esophagus,” Nat. Med.16(5), 603–606, 1p, 606 (2010).
[CrossRef] [PubMed]

2009 (1)

H. M. Mehanna, T. Rattay, J. Smith, and C. C. McConkey, “Treatment and follow-up of oral dysplasia—a systematic review and meta-analysis,” Head Neck31(12), 1600–1609 (2009).
[CrossRef] [PubMed]

2008 (2)

R. A. Schwarz, W. Gao, D. Daye, M. D. Williams, R. Richards-Kortum, and A. M. Gillenwater, “Autofluorescence and diffuse reflectance spectroscopy of oral epithelial tissue using a depth-sensitive fiber-optic probe,” Appl. Opt.47(6), 825–834 (2008).
[CrossRef] [PubMed]

I. Pavlova, M. Williams, A. El-Naggar, R. Richards-Kortum, and A. Gillenwater, “Understanding the biological basis of autofluorescence imaging for oral cancer detection: high-resolution fluorescence microscopy in viable tissue,” Clin. Cancer Res.14(8), 2396–2404 (2008).
[CrossRef] [PubMed]

2007 (5)

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]

S. Zhuo, J. Chen, X. Jiang, S. Xie, R. Chen, N. Cao, Q. Zou, and S. Xiong, “The layered-resolved microstructure and spectroscopy of mouse oral mucosa using multiphoton microscopy,” Phys. Med. Biol.52(16), 4967–4980 (2007).
[CrossRef] [PubMed]

J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit esophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys.9(7), 212 (2007).
[CrossRef]

P. M. Speight, “Update on oral epithelial dysplasia and progression to cancer,” Head Neck Pathol.1(1), 61–66 (2007).
[CrossRef] [PubMed]

J. A. Palero, H. S. de Bruijn, A. van der Ploeg van den Heuvel, H. J. C. M. Sterenborg, and H. C. Gerritsen, “Spectrally resolved multiphoton imaging of in vivo and excised mouse skin tissues,” Biophys. J.93(3), 992–1007 (2007).
[CrossRef] [PubMed]

2006 (5)

O. Kujan, R. J. Oliver, A. Khattab, S. A. Roberts, N. Thakker, and P. Sloan, “Evaluation of a new binary system of grading oral epithelial dysplasia for prediction of malignant transformation,” Oral Oncol.42(10), 987–993 (2006).
[CrossRef] [PubMed]

J. E. Bouquot, P. M. Speight, and P. M. Farthing, “Epithelial dysplasia of the oral mucosa-Diagnostic problems and prognostic features,” Curr. Diagn. Pathol.12(1), 11–21 (2006).
[CrossRef]

J. A. Evans, J. M. Poneros, B. E. Bouma, J. Bressner, E. F. Halpern, M. Shishkov, G. Y. Lauwers, M. Mino-Kenudson, N. S. Nishioka, and G. J. Tearney, “Optical coherence tomography to identify intramucosal carcinoma and high-grade dysplasia in Barrett’s esophagus,” Clin. Gastroenterol. Hepatol.4(1), 38–43 (2006).
[CrossRef] [PubMed]

J. A. Palero, H. S. de Bruijn, A. van der Ploeg-van den Heuvel, H. J. C. M. Sterenborg, and H. C. Gerritsen, “In vivo nonlinear spectral imaging in mouse skin,” Opt. Express14(10), 4395–4402 (2006).
[CrossRef] [PubMed]

L. B. Lovat, K. Johnson, G. D. Mackenzie, B. R. Clark, M. R. Novelli, S. Davies, M. O’Donovan, C. Selvasekar, S. M. Thorpe, D. Pickard, R. C. Fitzgerald, T. Fearn, I. J. Bigio, and S. G. Bown, “Elastic scattering spectroscopy accurately detects high grade dysplasia and cancer in Barrett’s oesophagus,” Gut55(8), 1078–1083 (2006).
[CrossRef] [PubMed]

2005 (3)

A. Pena, M. Strupler, T. Boulesteix, and M. Schanne-Klein, “Spectroscopic analysis of keratin endogenous signal for skin multiphoton microscopy,” Opt. Express13(16), 6268–6274 (2005).
[CrossRef] [PubMed]

D. C. G. De Veld, M. J. Witjes, H. J. Sterenborg, and J. L. Roodenburg, “The status of in vivo autofluorescence spectroscopy and imaging for oral oncology,” Oral Oncol.41(2), 117–131 (2005).
[CrossRef] [PubMed]

M. C. Skala, J. M. Squirrell, K. M. Vrotsos, J. C. Eickhoff, A. Gendron-Fitzpatrick, K. W. Eliceiri, and N. Ramanujam, “Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues,” Cancer Res.65(4), 1180–1186 (2005).
[CrossRef] [PubMed]

2004 (3)

2003 (2)

T. J. Pfefer, L. S. Matchette, A. M. Ross, and M. N. Ediger, “Selective detection of fluorophore layers in turbid media: the role of fiber-optic probe design,” Opt. Lett.28(2), 120–122 (2003).
[CrossRef] [PubMed]

A. Uppal and P. K. Gupta, “Measurement of NADH concentration in normal and malignant human tissues from breast and oral cavity,” Biotechnol. Appl. Biochem.37(1), 45–50 (2003).
[CrossRef] [PubMed]

2002 (3)

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]

S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J.82(5), 2811–2825 (2002).
[CrossRef] [PubMed]

B. W. Neville and T. A. Day, “Oral cancer and precancerous lesions,” CA Cancer J. Clin.52(4), 195–215 (2002).
[CrossRef] [PubMed]

2001 (1)

G. Zuccaro, N. Gladkova, J. Vargo, F. Feldchtein, E. Zagaynova, D. Conwell, G. Falk, J. Goldblum, J. Dumot, J. Ponsky, G. Gelikonov, B. Davros, E. Donchenko, and J. Richter, “Optical coherence tomography of the esophagus and proximal stomach in health and disease,” Am. J. Gastroenterol.96(9), 2633–2639 (2001).
[CrossRef] [PubMed]

2000 (2)

L. Coghlan, U. Utzinger, R. Drezek, D. Heintzelmann, A. Zuluaga, C. Brookner, R. Richards-Kortum, I. Gimenez-Conti, and M. Follen, “Optimal fluorescence excitation wavelengths for detection of squamous intra-epithelial neoplasia: results from an animal model,” Opt. Express7(12), 436–446 (2000).
[CrossRef] [PubMed]

D. L. Heintzelman, U. Utzinger, H. Fuchs, A. Zuluaga, K. Gossage, A. M. Gillenwater, R. Jacob, B. Kemp, and R. R. Richards-Kortum, “Optimal excitation wavelengths for in vivo detection of oral neoplasia using fluorescence spectroscopy,” Photochem. Photobiol.72(1), 103–113 (2000).
[CrossRef] [PubMed]

1999 (1)

C. Y. Wang, H. K. Chiang, C. T. Chen, C. P. Chiang, Y. S. Kuo, and S. N. Chow, “Diagnosis of oral cancer by light-induced autofluorescence spectroscopy using double excitation wavelengths,” Oral Oncol.35(2), 144–150 (1999).
[CrossRef] [PubMed]

1998 (2)

A. Gillenwater, R. Jacob, R. Ganeshappa, B. Kemp, A. K. El-Naggar, J. L. Palmer, G. Clayman, M. F. Mitchell, and R. Richards-Kortum, “Noninvasive diagnosis of oral neoplasia based on fluorescence spectroscopy and native tissue autofluorescence,” Arch. Otolaryngol. Head Neck Surg.124(11), 1251–1258 (1998).
[PubMed]

J. A. Gardecki and M. Maroncelli, “Set of secondary emission standards for calibration of the spectral responsivity in emission spectroscopy,” Appl. Spectrosc.52(9), 1179–1189 (1998).
[CrossRef]

1996 (1)

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

1995 (1)

H. Lumerman, P. Freedman, and S. Kerpel, “Oral epithelial dysplasia and the development of invasive squamous cell carcinoma,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod.79(3), 321–329 (1995).
[CrossRef] [PubMed]

1993 (1)

I. B. Gimenez-Conti and T. J. Slaga, “The hamster cheek pouch carcinogenesis model,” J. Cell. Biochem. Suppl.53(S17F), 83–90 (1993).
[CrossRef] [PubMed]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science248(4951), 73–76 (1990).
[CrossRef] [PubMed]

Amelink, A.

Bard, M. P.

Bell, B.

Ben-Yakar, A.

N. J. Durr, C. T. Weisspfennig, B. A. Holfeld, and A. Ben-Yakar, “Maximum imaging depth of two-photon autofluorescence microscopy in epithelial tissues,” J. Biomed. Opt.16(2), 026008 (2011).
[CrossRef] [PubMed]

Bigio, I. J.

L. B. Lovat, K. Johnson, G. D. Mackenzie, B. R. Clark, M. R. Novelli, S. Davies, M. O’Donovan, C. Selvasekar, S. M. Thorpe, D. Pickard, R. C. Fitzgerald, T. Fearn, I. J. Bigio, and S. G. Bown, “Elastic scattering spectroscopy accurately detects high grade dysplasia and cancer in Barrett’s oesophagus,” Gut55(8), 1078–1083 (2006).
[CrossRef] [PubMed]

Bi-Ying, Y.

Z. Zheng-Fei, L. Han-Ping, G. Zhou-Yi, Z. Shuang-Mu, Y. Bi-Ying, and D. Xiao-Yuan, “Second-harmonic generation as a DNA malignancy indicator of prostate glandular epithelial cells,” Chinese Phys. B19(4), 049501 (2010).
[CrossRef]

Boulesteix, T.

Bouma, B. E.

J. A. Evans, J. M. Poneros, B. E. Bouma, J. Bressner, E. F. Halpern, M. Shishkov, G. Y. Lauwers, M. Mino-Kenudson, N. S. Nishioka, and G. J. Tearney, “Optical coherence tomography to identify intramucosal carcinoma and high-grade dysplasia in Barrett’s esophagus,” Clin. Gastroenterol. Hepatol.4(1), 38–43 (2006).
[CrossRef] [PubMed]

Bouquot, J. E.

J. E. Bouquot, P. M. Speight, and P. M. Farthing, “Epithelial dysplasia of the oral mucosa-Diagnostic problems and prognostic features,” Curr. Diagn. Pathol.12(1), 11–21 (2006).
[CrossRef]

Bown, S. G.

L. B. Lovat, K. Johnson, G. D. Mackenzie, B. R. Clark, M. R. Novelli, S. Davies, M. O’Donovan, C. Selvasekar, S. M. Thorpe, D. Pickard, R. C. Fitzgerald, T. Fearn, I. J. Bigio, and S. G. Bown, “Elastic scattering spectroscopy accurately detects high grade dysplasia and cancer in Barrett’s oesophagus,” Gut55(8), 1078–1083 (2006).
[CrossRef] [PubMed]

Bressner, J.

J. A. Evans, J. M. Poneros, B. E. Bouma, J. Bressner, E. F. Halpern, M. Shishkov, G. Y. Lauwers, M. Mino-Kenudson, N. S. Nishioka, and G. J. Tearney, “Optical coherence tomography to identify intramucosal carcinoma and high-grade dysplasia in Barrett’s esophagus,” Clin. Gastroenterol. Hepatol.4(1), 38–43 (2006).
[CrossRef] [PubMed]

Brookner, C.

Burgers, S. A.

Cao, N.

S. Zhuo, J. Chen, X. Jiang, S. Xie, R. Chen, N. Cao, Q. Zou, and S. Xiong, “The layered-resolved microstructure and spectroscopy of mouse oral mucosa using multiphoton microscopy,” Phys. Med. Biol.52(16), 4967–4980 (2007).
[CrossRef] [PubMed]

Chen, C. T.

C. Y. Wang, H. K. Chiang, C. T. Chen, C. P. Chiang, Y. S. Kuo, and S. N. Chow, “Diagnosis of oral cancer by light-induced autofluorescence spectroscopy using double excitation wavelengths,” Oral Oncol.35(2), 144–150 (1999).
[CrossRef] [PubMed]

Chen, J.

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Holfeld, B. A.

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D. L. Heintzelman, U. Utzinger, H. Fuchs, A. Zuluaga, K. Gossage, A. M. Gillenwater, R. Jacob, B. Kemp, and R. R. Richards-Kortum, “Optimal excitation wavelengths for in vivo detection of oral neoplasia using fluorescence spectroscopy,” Photochem. Photobiol.72(1), 103–113 (2000).
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H. Lumerman, P. Freedman, and S. Kerpel, “Oral epithelial dysplasia and the development of invasive squamous cell carcinoma,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod.79(3), 321–329 (1995).
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G. Zuccaro, N. Gladkova, J. Vargo, F. Feldchtein, E. Zagaynova, D. Conwell, G. Falk, J. Goldblum, J. Dumot, J. Ponsky, G. Gelikonov, B. Davros, E. Donchenko, and J. Richter, “Optical coherence tomography of the esophagus and proximal stomach in health and disease,” Am. J. Gastroenterol.96(9), 2633–2639 (2001).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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N. J. Durr, C. T. Weisspfennig, B. A. Holfeld, and A. Ben-Yakar, “Maximum imaging depth of two-photon autofluorescence microscopy in epithelial tissues,” J. Biomed. Opt.16(2), 026008 (2011).
[CrossRef] [PubMed]

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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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Williams, M. D.

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D. C. G. De Veld, M. J. Witjes, H. J. Sterenborg, and J. L. Roodenburg, “The status of in vivo autofluorescence spectroscopy and imaging for oral oncology,” Oral Oncol.41(2), 117–131 (2005).
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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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S. Zhuo, J. Chen, X. Jiang, S. Xie, R. Chen, N. Cao, Q. Zou, and S. Xiong, “The layered-resolved microstructure and spectroscopy of mouse oral mucosa using multiphoton microscopy,” Phys. Med. Biol.52(16), 4967–4980 (2007).
[CrossRef] [PubMed]

J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit esophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys.9(7), 212 (2007).
[CrossRef]

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J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit esophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys.9(7), 212 (2007).
[CrossRef]

S. Zhuo, J. Chen, X. Jiang, S. Xie, R. Chen, N. Cao, Q. Zou, and S. Xiong, “The layered-resolved microstructure and spectroscopy of mouse oral mucosa using multiphoton microscopy,” Phys. Med. Biol.52(16), 4967–4980 (2007).
[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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Chinese Phys. B (1)

Z. Zheng-Fei, L. Han-Ping, G. Zhou-Yi, Z. Shuang-Mu, Y. Bi-Ying, and D. Xiao-Yuan, “Second-harmonic generation as a DNA malignancy indicator of prostate glandular epithelial cells,” Chinese Phys. B19(4), 049501 (2010).
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Clin. Cancer Res. (1)

I. Pavlova, M. Williams, A. El-Naggar, R. Richards-Kortum, and A. Gillenwater, “Understanding the biological basis of autofluorescence imaging for oral cancer detection: high-resolution fluorescence microscopy in viable tissue,” Clin. Cancer Res.14(8), 2396–2404 (2008).
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J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit esophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys.9(7), 212 (2007).
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D. C. G. De Veld, M. J. Witjes, H. J. Sterenborg, and J. L. Roodenburg, “The status of in vivo autofluorescence spectroscopy and imaging for oral oncology,” Oral Oncol.41(2), 117–131 (2005).
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S. Zhuo, J. Chen, X. Jiang, S. Xie, R. Chen, N. Cao, Q. Zou, and S. Xiong, “The layered-resolved microstructure and spectroscopy of mouse oral mucosa using multiphoton microscopy,” Phys. Med. Biol.52(16), 4967–4980 (2007).
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Proc. Natl. Acad. Sci. U.S.A. (2)

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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Figures (8)

Fig. 1
Fig. 1

Diagram depicting experimental setup for in vivo two photon autofluorescence spectroscopy and imaging. HWP: half wave plate; GT: Glans Thompson prism; BE: beam expander; DF: dichroic filter; TM: translational mirror.

Fig. 2
Fig. 2

Cross-sectional H&E sections of normal (a), moderate dysplasia (b) and severe dysplasia (c) for hamster oral mucosa. The region above the basal layer in figure (a) represents the epithelium with the stroma represented by the structure below this layer. The dysplastic specimens are characterized by significant changes including a thickening of the stratum corneum (hyperkeratosis) HK which is observed in figures (b) and (c).

Fig. 3
Fig. 3

2P micrographs of the stratum corneum of the oral mucosa for (a) normal, (b) moderate and (c) severe dysplasia (Scale bar in a-c is 50 µm). Representative spectra from each of these three groups is shown in (d) for 780 nm excitation. Plot (e) represents the emission peak position with respect to excitation wavelength for the three groups with standard error bars. For each grading classification, the total emission intensity at 780 nm to 890 nm excitation is shown in (f). The error bar in (e) represents the standard error. Level of significance is shown for moderate and severe relative to normal *(p < 0.05), ** (p < 0.001).

Fig. 4
Fig. 4

Images (a)–(c) are in vivo 2P micrographs of normal, moderate dysplasia and severe dysplasia respectively, of the superficial epithelium of the oral mucosa at 780 nm excitation. The results for the basal layer are represented in images (d)–(f). The dotted white circle in (a) represents a collection of prickle cells in which the dark elliptical centers correspond to the nuclei. The cytoplasm of these cells is bright relative to the nuclei. Scale bar in a–f is 50 µm.

Fig. 5
Fig. 5

Representative emission spectra plots for normal, moderate and severe oral mucosal tissue are shown in (a) and (b), at 780 nm excitation for the superficial and basal epithelium respectively. Plots (c) and (d) represent the emission peak position as a function of excitation wavelength for the different classifications. The total emission intensity of the three tissue grades are show for the superficial epithelium (e) and basal epithelium (f), at four excitation wavelengths. Level of significance is shown for moderate or severe relative to normal *(p < 0.05), ** (p < 0.001).

Fig. 6
Fig. 6

(a) Spectral plots for 780 nm and 890 nm excitation of the epithelia layer of normal oral mucosa (red and blue plots respectively) are displayed. The green plot represents the difference between the two plots after normalization at longer wavelengths and represents the contribution due to NAD(P)H) only. The bar graph shown in (b) represents the redox ratio for the superficial and basal epithelium of normal, moderate and severe dysplasia of the oral mucosa, **(p<0.001).

Fig. 7
Fig. 7

Images (a) to (c) are 2P images of the stroma for normal, moderate and severe oral mucosa tissue. The normalized spectroscopy results for 780 nm excitation are represented in (d). Plot (e) represents the emission peak position as a function of excitation wavelength. Bar plot (f) depicts the emission intensity results. Scale bar in a-c is 50 µm. Level of significance is shown for moderate or severe relative to normal *(p < 0.05), ** (p < 0.001).

Fig. 8
Fig. 8

Emission spectra for the stroma for normal, moderate and severe dysplasia oral mucosa at 890 nm excitation. A very strong SHG peak was observed in addition to a very weak Raman peak. A similar result was observed for 840 nm excitation of this layer.

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