Abstract

Timely detection of cutaneous squamous cell carcinoma with non-invasive modalities like nonlinear spectral imaging (NLSI) can ensure efficient preventive or therapeutic measures for patients. In this study, in vivo NLSI was used to study spectral characteristics in murine skin treated with 7, 12-dimethylbenz(a)anthracene. The results show that NLSI could detect emission spectral changes during the early preclinical stages of skin carcinogenesis. Analyzing these emission spectra using simulated band-pass filters at 450-460 nm and 525-535 nm, gave parameters that were expressed as a ratio. This ratio was increased and thus suggestive of elevated metabolic activity in early stages of skin carcinogenesis.

© 2014 Optical Society of America

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2014 (6)

M. B. Veierød, E. Couto, E. Lund, H.-O. Adami, and E. Weiderpass, “Host characteristics, sun exposure, indoor tanning and risk of squamous cell carcinoma of the skin,” Int. J. Cancer 135(2), 413–422 (2014).
[Crossref] [PubMed]

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

N. R. Liu, G. N. Chen, S. S. Wu, and R. Chen, “Distinguishing human normal or cancerous esophagus tissue ex vivo using multiphoton microscopy,” J. Opt. 16(2), 025301 (2014).
[Crossref]

A. Varone, J. Xylas, K. P. Quinn, D. Pouli, G. Sridharan, M. E. McLaughlin-Drubin, C. Alonzo, K. Lee, K. Münger, and I. Georgakoudi, “Endogenous Two-Photon Fluorescence Imaging Elucidates Metabolic Changes Related to Enhanced Glycolysis and Glutamine Consumption in Precancerous Epithelial Tissues,” Cancer Res. 74(11), 3067–3075 (2014).
[Crossref] [PubMed]

G. Thomas, O. Nadiarnykh, J. van Voskuilen, C. L. Hoy, H. C. Gerritsen, and H. J. C. M. Sterenborg, “Estimating the risk of squamous cell cancer induction in skin following nonlinear optical imaging,” J Biophotonics 7(7), 492–505 (2014).
[Crossref] [PubMed]

G. Thomas, J. van Voskuilen, H. C. Gerritsen, and H. J. C. M. Sterenborg, “Advances and challenges in label-free nonlinear optical imaging using two-photon excitation fluorescence and second harmonic generation for cancer research,” J. Photochem. Photobiol. B 141, 128–138 (2014).

2013 (6)

J. M. Watson, S. L. Marion, P. F. Rice, U. Utzinger, M. A. Brewer, P. B. Hoyer, and J. K. Barton, “Two-photon excited fluorescence imaging of endogenous contrast in a mouse model of ovarian cancer,” Lasers Surg. Med. 45(3), 155–166 (2013).
[Crossref] [PubMed]

J. T. Keyes, B. R. Simon, and J. P. Vande Geest, “Location-Dependent Coronary Artery Diffusive and Convective Mass Transport Properties of a Lipophilic Drug Surrogate Measured Using Nonlinear Microscopy,” Pharm. Res. 30(4), 1147–1160 (2013).
[Crossref] [PubMed]

R. Cicchi, A. Sturiale, G. Nesi, D. Kapsokalyvas, G. Alemanno, F. Tonelli, and F. S. Pavone, “Multiphoton morpho-functional imaging of healthy colon mucosa, adenomatous polyp and adenocarcinoma,” Biomed. Opt. Express 4(7), 1204–1213 (2013).
[Crossref] [PubMed]

G. Chen, L. Wang, J. Lu, W. Zhu, H. Zhang, J. Chen, S. Zhuo, and J. Yan, “Optical diagnosis for lung cancer using multiphoton imaging,” Scanning 35(6), 362–365 (2013).
[Crossref] [PubMed]

M. Manfredini, F. Arginelli, C. Dunsby, P. French, C. Talbot, K. König, G. Pellacani, G. Ponti, and S. Seidenari, “High-resolution imaging of basal cell carcinoma: a comparison between multiphoton microscopy with fluorescence lifetime imaging and reflectance confocal microscopy,” Skin Res. Technol. 19(1), e433–e443 (2013).
[Crossref] [PubMed]

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical Metabolic Imaging Identifies Glycolytic Levels, Subtypes, and Early-Treatment Response in Breast Cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

2012 (5)

N. Sachs, P. Secades, L. van Hulst, M. Kreft, J.-Y. Song, and A. Sonnenberg, “Loss of integrin α3 prevents skin tumor formation by promoting epidermal turnover and depletion of slow-cycling cells,” Proc. Natl. Acad. Sci. U.S.A. 109(52), 21468–21473 (2012).
[Crossref] [PubMed]

M. C. Fargnoli, D. Kostaki, A. Piccioni, T. Micantonio, and K. Peris, “Dermoscopy in the diagnosis and management of non-melanoma skin cancers,” Eur. J. Dermatol. 22(4), 456–463 (2012).
[PubMed]

S. W. Perry, R. M. Burke, and E. B. Brown, “Two-Photon and Second Harmonic Microscopy in Clinical and Translational Cancer Research,” Ann. Biomed. Eng. 40(2), 277–291 (2012).
[Crossref] [PubMed]

K. Edward, S. Qiu, V. Resto, S. McCammon, and G. Vargas, “In vivo layer-resolved characterization of oral dysplasia via nonlinear optical micro-spectroscopy,” Biomed. Opt. Express 3(7), 1579–1593 (2012).
[Crossref] [PubMed]

K. Koenig, “Hybrid multiphoton multimodal tomography of in vivo human skin,” Intravital 1(1), 11–26 (2012).
[Crossref]

2011 (6)

A. N. Bader, A.-M. Pena, C. Johan van Voskuilen, J. A. Palero, F. Leroy, A. Colonna, and H. C. Gerritsen, “Fast nonlinear spectral microscopy of in vivo human skin,” Biomed. Opt. Express 2(2), 365–373 (2011).
[Crossref] [PubMed]

S. Zhuo, J. Yan, G. Chen, J. Chen, Y. Liu, J. Lu, X. Zhu, X. Jiang, and S. Xie, “Label-free monitoring of colonic cancer progression using multiphoton microscopy,” Biomed. Opt. Express 2(3), 615–619 (2011).
[Crossref] [PubMed]

M. S. Roberts, Y. Dancik, T. W. Prow, C. A. Thorling, L. L. Lin, J. E. Grice, T. A. Robertson, K. König, and W. Becker, “Non-invasive imaging of skin physiology and percutaneous penetration using fluorescence spectral and lifetime imaging with multiphoton and confocal microscopy,” Eur. J. Pharm. Biopharm. 77(3), 469–488 (2011).
[Crossref] [PubMed]

R. Diaz-Ruiz, M. Rigoulet, and A. Devin, “The Warburg and Crabtree effects: On the origin of cancer cell energy metabolism and of yeast glucose repression,” Biochimica et Biophysica Acta (BBA) - Bioenergetics 1807(6), 568–576 (2011).
[Crossref]

S. Y. Xiong, J. G. Yang, and J. Zhuang, “Nonlinear spectral imaging of human normal skin, basal cell carcinoma and squamous cell carcinoma based on two-photon excited fluorescence and second-harmonic generation,” Laser Phys. 21(10), 1844–1849 (2011).
[Crossref]

D. Leupold, M. Scholz, G. Stankovic, J. Reda, S. Buder, R. Eichhorn, G. Wessler, M. Stücker, K. Hoffmann, J. Bauer, and C. Garbe, “The stepwise two-photon excited melanin fluorescence is a unique diagnostic tool for the detection of malignant transformation in melanocytes,” Pigment Cell Melanoma Res 24(3), 438–445 (2011).
[Crossref] [PubMed]

2010 (2)

2009 (3)

S. Zhuo, J. Chen, T. Luo, X. Jiang, S. Xie, and R. Chen, “Two-layered multiphoton microscopic imaging of cervical tissue,” Lasers Med. Sci. 24(3), 359–363 (2009).
[Crossref] [PubMed]

E. Dimitrow, M. Ziemer, M. J. Koehler, J. Norgauer, K. König, P. Elsner, and M. Kaatz, “Sensitivity and Specificity of Multiphoton Laser Tomography for In Vivo and Ex Vivo Diagnosis of Malignant Melanoma,” J. Invest. Dermatol. 129(7), 1752–1758 (2009).
[Crossref] [PubMed]

V. De Giorgi, D. Massi, S. Sestini, R. Cicchi, F. S. Pavone, and T. Lotti, “Combined non-linear laser imaging (two-photon excitation fluorescence microscopy, fluorescence lifetime imaging microscopy, multispectral multiphoton microscopy) in cutaneous tumours: first experiences,” J. Eur. Acad. Dermatol. Venereol. 23(3), 314–316 (2009).
[Crossref] [PubMed]

2008 (2)

C. Calabrese, A. Pisi, G. Di Febo, G. Liguori, G. Filippini, M. Cervellera, V. Righi, P. Lucchi, A. Mucci, L. Schenetti, V. Tonini, M. R. Tosi, and V. Tugnoli, “Biochemical Alterations from Normal Mucosa to Gastric Cancer by Ex vivo Magnetic Resonance Spectroscopy,” Cancer Epidemiol. Biomarkers Prev. 17(6), 1386–1395 (2008).
[Crossref] [PubMed]

K. König, “Clinical multiphoton tomography,” J Biophotonics 1(1), 13–23 (2008).
[Crossref] [PubMed]

2007 (8)

J. A. Palero, H. S. de Bruijn, A. van der Ploeg van den Heuvel, H. J. 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]

J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit oesophageal 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]

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. 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]

N. D. Kirkpatrick, M. A. Brewer, and U. Utzinger, “Endogenous Optical Biomarkers of Ovarian Cancer Evaluated with Multiphoton Microscopy,” Cancer Epidemiol. Biomarkers Prev. 16(10), 2048–2057 (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]

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

2006 (3)

J. Zhou, T. Schmid, S. Schnitzer, and B. Brüne, “Tumor hypoxia and cancer progression,” Cancer Lett. 237(1), 10–21 (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. Express 14(10), 4395–4402 (2006).
[Crossref] [PubMed]

Y. J. Chen, Y. D. Cheng, H. Y. Liu, P. Y. Lin, and C. S. Wang, “Observation of biochemical imaging changes in human pancreatic cancer tissue using Fourier-transform infrared microspectroscopy,” Chang Gung Med. J. 29(5), 518–527 (2006).
[PubMed]

2005 (1)

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

2003 (1)

K. Kolanjiappan, C. R. Ramachandran, and S. Manoharan, “Biochemical changes in tumor tissues of oral cancer patients,” Clin. Biochem. 36(1), 61–65 (2003).
[Crossref] [PubMed]

2002 (1)

M. Stücker, A. Struk, P. Altmeyer, M. Herde, H. Baumgärtl, and D. W. Lübbers, “The cutaneous uptake of atmospheric oxygen contributes significantly to the oxygen supply of human dermis and epidermis,” J. Physiol. 538(3), 985–994 (2002).
[Crossref] [PubMed]

2000 (2)

K. König, “Multiphoton microscopy in life sciences,” J. Microsc. 200(2), 83–104 (2000).
[Crossref] [PubMed]

R. Gillies, G. Zonios, R. R. Anderson, and N. Kollias, “Fluorescence Excitation Spectroscopy Provides Information About Human Skin In Vivo,” J. Invest. Dermatol. 115(4), 704–707 (2000).
[Crossref] [PubMed]

1998 (1)

A. Terman and U. T. Brunk, “Lipofuscin: mechanisms of formation and increase with age,” APMIS 106(2), 265–276 (1998).
[Crossref] [PubMed]

1996 (1)

C. J. Gulledge and M. W. Dewhirst, “Tumor oxygenation: a matter of supply and demand,” Anticancer Res. 16(2), 741–749 (1996).
[PubMed]

1995 (3)

K. Ozawa, M. Yamamoto, Y. Shimahara, A. Kishida, R. Tabata, M. Takahashi, Y. Terada, S. Iwata, and T. Kobayashi, “The redox theory in evolution,” J. Hep. Bil. Pancr. Surg. 2(3), 205–214 (1995).
[Crossref]

R. P. Gallagher, G. B. Hill, C. D. Bajdik, A. J. Coldman, S. Fincham, D. I. McLean, and W. J. Threlfall, “Sunlight exposure, pigmentation factors, and risk of nonmelanocytic skin cancer. II. Squamous cell carcinoma,” Arch. Dermatol. 131(2), 164–169 (1995).
[Crossref] [PubMed]

Y. Mochizuki, M. K. Park, T. Mori, and S. Kawashima, “The difference in autofluorescence features of lipofuscin between brain and adrenal,” Zoolog. Sci. 12(3), 283–288 (1995).
[Crossref] [PubMed]

1989 (1)

B. Chance, “Metabolic heterogeneities in rapidly metabolizing tissues,” J. Appl. Cardiol. 4, 207–221 (1989).

1988 (1)

G. Weagle, P. E. Paterson, J. Kennedy, and R. Pottier, “The nature of the chromophore responsible for naturally occurring fluorescence in mouse skin,” J. Photochem. Photobiol. B 2(3), 313–320 (1988).
[Crossref] [PubMed]

1979 (1)

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

1978 (1)

F. E. Mohs, “Chemosurgery: microscopically controlled surgery for skin cancer--past, present and future,” J. Dermatol. Surg. Oncol. 4(1), 41–54 (1978).
[Crossref] [PubMed]

1962 (3)

B. Chance and B. Schoener, “Correlation of oxidation-reduction changes of intracellular reduced pyridine nucleotide and changes in electroencephalogram of the rat in anoxia,” Nature 195(4845), 956–958 (1962).
[Crossref] [PubMed]

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

N. Bloembergen and P. S. Pershan, “Light Waves at the Boundary of Nonlinear Media,” Phys. Rev. 128(2), 606–622 (1962).
[Crossref]

1956 (1)

O. Warburg, “On the origin of cancer cells,” Science 123(3191), 309–314 (1956).
[Crossref] [PubMed]

1931 (1)

M. Göppert-Mayer, “Über Elementarakte mit zwei Quantensprüngen,” Annalen der Physik 401(3), 273–294 (1931).
[Crossref]

Adami, H.-O.

M. B. Veierød, E. Couto, E. Lund, H.-O. Adami, and E. Weiderpass, “Host characteristics, sun exposure, indoor tanning and risk of squamous cell carcinoma of the skin,” Int. J. Cancer 135(2), 413–422 (2014).
[Crossref] [PubMed]

Adur, J.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

Alemanno, G.

Alonzo, C.

A. Varone, J. Xylas, K. P. Quinn, D. Pouli, G. Sridharan, M. E. McLaughlin-Drubin, C. Alonzo, K. Lee, K. Münger, and I. Georgakoudi, “Endogenous Two-Photon Fluorescence Imaging Elucidates Metabolic Changes Related to Enhanced Glycolysis and Glutamine Consumption in Precancerous Epithelial Tissues,” Cancer Res. 74(11), 3067–3075 (2014).
[Crossref] [PubMed]

Altmeyer, P.

M. Stücker, A. Struk, P. Altmeyer, M. Herde, H. Baumgärtl, and D. W. Lübbers, “The cutaneous uptake of atmospheric oxygen contributes significantly to the oxygen supply of human dermis and epidermis,” J. Physiol. 538(3), 985–994 (2002).
[Crossref] [PubMed]

Anderson, R. R.

R. Gillies, G. Zonios, R. R. Anderson, and N. Kollias, “Fluorescence Excitation Spectroscopy Provides Information About Human Skin In Vivo,” J. Invest. Dermatol. 115(4), 704–707 (2000).
[Crossref] [PubMed]

Andrade, L. A. L. A.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

Arginelli, F.

M. Manfredini, F. Arginelli, C. Dunsby, P. French, C. Talbot, K. König, G. Pellacani, G. Ponti, and S. Seidenari, “High-resolution imaging of basal cell carcinoma: a comparison between multiphoton microscopy with fluorescence lifetime imaging and reflectance confocal microscopy,” Skin Res. Technol. 19(1), e433–e443 (2013).
[Crossref] [PubMed]

Arteaga, C. L.

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical Metabolic Imaging Identifies Glycolytic Levels, Subtypes, and Early-Treatment Response in Breast Cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Bader, A. N.

Bajdik, C. D.

R. P. Gallagher, G. B. Hill, C. D. Bajdik, A. J. Coldman, S. Fincham, D. I. McLean, and W. J. Threlfall, “Sunlight exposure, pigmentation factors, and risk of nonmelanocytic skin cancer. II. Squamous cell carcinoma,” Arch. Dermatol. 131(2), 164–169 (1995).
[Crossref] [PubMed]

Baratti, M. O.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

Barton, J. K.

J. M. Watson, S. L. Marion, P. F. Rice, U. Utzinger, M. A. Brewer, P. B. Hoyer, and J. K. Barton, “Two-photon excited fluorescence imaging of endogenous contrast in a mouse model of ovarian cancer,” Lasers Surg. Med. 45(3), 155–166 (2013).
[Crossref] [PubMed]

Bauer, J.

D. Leupold, M. Scholz, G. Stankovic, J. Reda, S. Buder, R. Eichhorn, G. Wessler, M. Stücker, K. Hoffmann, J. Bauer, and C. Garbe, “The stepwise two-photon excited melanin fluorescence is a unique diagnostic tool for the detection of malignant transformation in melanocytes,” Pigment Cell Melanoma Res 24(3), 438–445 (2011).
[Crossref] [PubMed]

Baumgärtl, H.

M. Stücker, A. Struk, P. Altmeyer, M. Herde, H. Baumgärtl, and D. W. Lübbers, “The cutaneous uptake of atmospheric oxygen contributes significantly to the oxygen supply of human dermis and epidermis,” J. Physiol. 538(3), 985–994 (2002).
[Crossref] [PubMed]

Becker, W.

M. S. Roberts, Y. Dancik, T. W. Prow, C. A. Thorling, L. L. Lin, J. E. Grice, T. A. Robertson, K. König, and W. Becker, “Non-invasive imaging of skin physiology and percutaneous penetration using fluorescence spectral and lifetime imaging with multiphoton and confocal microscopy,” Eur. J. Pharm. Biopharm. 77(3), 469–488 (2011).
[Crossref] [PubMed]

Bird, D. K.

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

Bloembergen, N.

N. Bloembergen and P. S. Pershan, “Light Waves at the Boundary of Nonlinear Media,” Phys. Rev. 128(2), 606–622 (1962).
[Crossref]

Bottcher-Luiz, F.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

Brewer, M. A.

J. M. Watson, S. L. Marion, P. F. Rice, U. Utzinger, M. A. Brewer, P. B. Hoyer, and J. K. Barton, “Two-photon excited fluorescence imaging of endogenous contrast in a mouse model of ovarian cancer,” Lasers Surg. Med. 45(3), 155–166 (2013).
[Crossref] [PubMed]

N. D. Kirkpatrick, M. A. Brewer, and U. Utzinger, “Endogenous Optical Biomarkers of Ovarian Cancer Evaluated with Multiphoton Microscopy,” Cancer Epidemiol. Biomarkers Prev. 16(10), 2048–2057 (2007).
[Crossref] [PubMed]

Brown, E. B.

S. W. Perry, R. M. Burke, and E. B. Brown, “Two-Photon and Second Harmonic Microscopy in Clinical and Translational Cancer Research,” Ann. Biomed. Eng. 40(2), 277–291 (2012).
[Crossref] [PubMed]

Brüne, B.

J. Zhou, T. Schmid, S. Schnitzer, and B. Brüne, “Tumor hypoxia and cancer progression,” Cancer Lett. 237(1), 10–21 (2006).
[Crossref] [PubMed]

Brunk, U. T.

A. Terman and U. T. Brunk, “Lipofuscin: mechanisms of formation and increase with age,” APMIS 106(2), 265–276 (1998).
[Crossref] [PubMed]

Buder, S.

D. Leupold, M. Scholz, G. Stankovic, J. Reda, S. Buder, R. Eichhorn, G. Wessler, M. Stücker, K. Hoffmann, J. Bauer, and C. Garbe, “The stepwise two-photon excited melanin fluorescence is a unique diagnostic tool for the detection of malignant transformation in melanocytes,” Pigment Cell Melanoma Res 24(3), 438–445 (2011).
[Crossref] [PubMed]

Burke, R. M.

S. W. Perry, R. M. Burke, and E. B. Brown, “Two-Photon and Second Harmonic Microscopy in Clinical and Translational Cancer Research,” Ann. Biomed. Eng. 40(2), 277–291 (2012).
[Crossref] [PubMed]

Calabrese, C.

C. Calabrese, A. Pisi, G. Di Febo, G. Liguori, G. Filippini, M. Cervellera, V. Righi, P. Lucchi, A. Mucci, L. Schenetti, V. Tonini, M. R. Tosi, and V. Tugnoli, “Biochemical Alterations from Normal Mucosa to Gastric Cancer by Ex vivo Magnetic Resonance Spectroscopy,” Cancer Epidemiol. Biomarkers Prev. 17(6), 1386–1395 (2008).
[Crossref] [PubMed]

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]

Carini, M.

Carvalho, H. F.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

Cervellera, M.

C. Calabrese, A. Pisi, G. Di Febo, G. Liguori, G. Filippini, M. Cervellera, V. Righi, P. Lucchi, A. Mucci, L. Schenetti, V. Tonini, M. R. Tosi, and V. Tugnoli, “Biochemical Alterations from Normal Mucosa to Gastric Cancer by Ex vivo Magnetic Resonance Spectroscopy,” Cancer Epidemiol. Biomarkers Prev. 17(6), 1386–1395 (2008).
[Crossref] [PubMed]

Cesar, C. L.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J Biophotonics 7(1-2), 37–48 (2014).
[Crossref] [PubMed]

Chance, B.

B. Chance, “Metabolic heterogeneities in rapidly metabolizing tissues,” J. Appl. Cardiol. 4, 207–221 (1989).

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

B. Chance and B. Schoener, “Correlation of oxidation-reduction changes of intracellular reduced pyridine nucleotide and changes in electroencephalogram of the rat in anoxia,” Nature 195(4845), 956–958 (1962).
[Crossref] [PubMed]

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

Chen, G.

G. Chen, L. Wang, J. Lu, W. Zhu, H. Zhang, J. Chen, S. Zhuo, and J. Yan, “Optical diagnosis for lung cancer using multiphoton imaging,” Scanning 35(6), 362–365 (2013).
[Crossref] [PubMed]

S. Zhuo, J. Yan, G. Chen, J. Chen, Y. Liu, J. Lu, X. Zhu, X. Jiang, and S. Xie, “Label-free monitoring of colonic cancer progression using multiphoton microscopy,” Biomed. Opt. Express 2(3), 615–619 (2011).
[Crossref] [PubMed]

Chen, G. N.

N. R. Liu, G. N. Chen, S. S. Wu, and R. Chen, “Distinguishing human normal or cancerous esophagus tissue ex vivo using multiphoton microscopy,” J. Opt. 16(2), 025301 (2014).
[Crossref]

Chen, J.

G. Chen, L. Wang, J. Lu, W. Zhu, H. Zhang, J. Chen, S. Zhuo, and J. Yan, “Optical diagnosis for lung cancer using multiphoton imaging,” Scanning 35(6), 362–365 (2013).
[Crossref] [PubMed]

S. Zhuo, J. Yan, G. Chen, J. Chen, Y. Liu, J. Lu, X. Zhu, X. Jiang, and S. Xie, “Label-free monitoring of colonic cancer progression using multiphoton microscopy,” Biomed. Opt. Express 2(3), 615–619 (2011).
[Crossref] [PubMed]

S. Zhuo, J. Chen, T. Luo, X. Jiang, S. Xie, and R. Chen, “Two-layered multiphoton microscopic imaging of cervical tissue,” Lasers Med. Sci. 24(3), 359–363 (2009).
[Crossref] [PubMed]

J. Chen, S. Zhuo, R. Chen, X. Jiang, S. Xie, and Q. Zou, “Depth-resolved spectral imaging of rabbit oesophageal 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]

Chen, R.

N. R. Liu, G. N. Chen, S. S. Wu, and R. Chen, “Distinguishing human normal or cancerous esophagus tissue ex vivo using multiphoton microscopy,” J. Opt. 16(2), 025301 (2014).
[Crossref]

S. Zhuo, J. Chen, T. Luo, X. Jiang, S. Xie, and R. Chen, “Two-layered multiphoton microscopic imaging of cervical tissue,” Lasers Med. Sci. 24(3), 359–363 (2009).
[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 oesophageal tissue based on two-photon excited fluorescence and second-harmonic generation,” New J. Phys. 9(7), 212 (2007).
[Crossref]

Chen, Y. J.

Y. J. Chen, Y. D. Cheng, H. Y. Liu, P. Y. Lin, and C. S. Wang, “Observation of biochemical imaging changes in human pancreatic cancer tissue using Fourier-transform infrared microspectroscopy,” Chang Gung Med. J. 29(5), 518–527 (2006).
[PubMed]

Cheng, Y. D.

Y. J. Chen, Y. D. Cheng, H. Y. Liu, P. Y. Lin, and C. S. Wang, “Observation of biochemical imaging changes in human pancreatic cancer tissue using Fourier-transform infrared microspectroscopy,” Chang Gung Med. J. 29(5), 518–527 (2006).
[PubMed]

Cicchi, R.

Cohen, P.

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

Coldman, A. J.

R. P. Gallagher, G. B. Hill, C. D. Bajdik, A. J. Coldman, S. Fincham, D. I. McLean, and W. J. Threlfall, “Sunlight exposure, pigmentation factors, and risk of nonmelanocytic skin cancer. II. Squamous cell carcinoma,” Arch. Dermatol. 131(2), 164–169 (1995).
[Crossref] [PubMed]

Colonna, A.

Cook, R. S.

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical Metabolic Imaging Identifies Glycolytic Levels, Subtypes, and Early-Treatment Response in Breast Cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Cosci, A.

Couto, E.

M. B. Veierød, E. Couto, E. Lund, H.-O. Adami, and E. Weiderpass, “Host characteristics, sun exposure, indoor tanning and risk of squamous cell carcinoma of the skin,” Int. J. Cancer 135(2), 413–422 (2014).
[Crossref] [PubMed]

Crisci, A.

Dancik, Y.

M. S. Roberts, Y. Dancik, T. W. Prow, C. A. Thorling, L. L. Lin, J. E. Grice, T. A. Robertson, K. König, and W. Becker, “Non-invasive imaging of skin physiology and percutaneous penetration using fluorescence spectral and lifetime imaging with multiphoton and confocal microscopy,” Eur. J. Pharm. Biopharm. 77(3), 469–488 (2011).
[Crossref] [PubMed]

de Bruijn, H. S.

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]

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]

J. A. Palero, H. S. de Bruijn, A. van der Ploeg van den Heuvel, H. J. 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]

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. Express 14(10), 4395–4402 (2006).
[Crossref] [PubMed]

De Giorgi, V.

V. De Giorgi, D. Massi, S. Sestini, R. Cicchi, F. S. Pavone, and T. Lotti, “Combined non-linear laser imaging (two-photon excitation fluorescence microscopy, fluorescence lifetime imaging microscopy, multispectral multiphoton microscopy) in cutaneous tumours: first experiences,” J. Eur. Acad. Dermatol. Venereol. 23(3), 314–316 (2009).
[Crossref] [PubMed]

de Thomaz, A. A.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, L. A. L. A. Andrade, H. F. Carvalho, F. Bottcher-Luiz, and C. L. Cesar, “Second harmonic generation microscopy as a powerful diagnostic imaging modality for human ovarian cancer,” J Biophotonics 7(1-2), 37–48 (2014).
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Figures (8)

Fig. 1
Fig. 1 Schematic diagram of the NLSI setup. (EMCCD – Electron Multiplying Charge Coupled Device)
Fig. 2
Fig. 2 Comparison between axial NLSI x-z scans and H&E stained sections for normal skin, skin with preclinical hyperplasia and clinically visible tumors (top to bottom). Axial x-z scans clearly displays stratum corneum (green layer), the deeper epidermis (blue layer) and the dermis (violet layer) (2a). The RGB colors in the images were obtained by multiplying the emission spectrum from skin with the spectra for the red, green and blue sensitivities of the human eye. The RGB colors in NLSI scans correspond to the wavelengths in tissue emission spectra shown. Epidermal proliferation can be clearly observed with in vivo NLSI in 2c and 2e. The corresponding H&E stained images show normal SKH1-hr mice skin (b), hyperplasia with no atypia (d) and severe hyperplasia with atypia (part of an acanthoma) (f). The corresponding axial H&E obtained from biopsy of the imaged spot may not represent the exact position of the imaged spot. (x-z scan scale – 100 μm × 60 μm, 224 pixels × 224 pixels).
Fig. 3
Fig. 3 Transverse x-y NLSI obtained at depths of 3 μm, 6 μm, 12 μm, 18 μm, 24 μm and 36 μm from surface for normal skin, skin with preclinical hyperplasia and clinically visible skin tumor. Epidermal autofluorescence was present down to 24 μm for preclinical hyperplasia and persisted even deeper for clinically visible skin tumors respectively, when compared to normal mice skin. The RGB colors in the images were obtained by multiplying the emission spectrum by the spectra for the red, green and blue sensitivities of the human eye. RGB colors in NLSI scans correspond to the wavelengths in tissue emission spectra shown. (x-y scan scale – 100 μm × 100 μm, 224 pixels × 224 pixels).
Fig. 4
Fig. 4 Higher magnification of transverse NLSI x-y scans showing the cytonuclear morphology in (a) normal skin, (b) skin with preclinical hyperplasia and (c) clinically visible skin tumor. Yellow continuous circle denotes epidermal cells with enlarged nuclei and white dotted circle indicates dividing (mitotic) epidermal cells in skin tumor.
Fig. 5
Fig. 5 (a) Reference emission spectra (normalized) from rat tail tendon collagen, free NADH, keratin and FAD, (b) Normalized emission spectra from axial x-z scans in normal mice skin (z = 17, s = 17, n = 12), mice skin with preclinical changes (z = 8, s = 8, n = 6) and clinically visible mice skin tumors (z = 7, s = 7, n = 6). The corresponding spectrum is an average of the emission spectra obtained from ‘z’ axial x-z NLSI scans (100 μm × 60 μm) in ‘s’ regions from ‘n’ mice for each clinco-pathologic grade.
Fig. 6
Fig. 6 Normalized emission spectra for normal mice skin (y = 17, s = 17, n = 12), skin with preclinical hyperplasia (y = 8, s = 8, n = 6) and clinically visible skin tumors (y = 7, s = 7, n = 6) at depths of (a) 3 μm, (b) 6 μm, (c) 12 μm, (d) 18 μm, (e) 24 μm and (f) 36 μm from skin surface. The depicted spectrum is an average of the emission spectra obtained at the corresponding depth from ‘y’ transverse x-y NLSI scans (100 μm × 100 μm) in ‘s’ regions from ‘n’ mice for each clinico-pathologic grade.
Fig. 7
Fig. 7 Comparison of mean total autofluorescence intensity (410 nm – 650 nm) and mean total SHG intensity (370 nm – 410 nm) for normal mice skin (z = 17, s = 17, n = 12), skin with preclinical hyperplasia (z = 8,s = 8, n = 6) and clinically visible skin tumors (z = 7,s = 7, n = 6). The intensities were calculated and averaged from ‘z’ axial x-z NLSI scans (100 μm × 60 μm) in ‘s’ regions from ‘n’ mice for each clinico-pathologic grade. Y-bars stand for standard error of the mean (* - p-value < 0.05 with respect to normal skin, § - p-value < 0.05 for skin with preclinical hyperplasia with respect to clinically visible skin tumors).
Fig. 8
Fig. 8 Comparison of mean ratio AUC450nm-460nm/AUC525nm-535nm (AUC- Area under curve) between normal mice skin (y = 49, s = 17, n = 12), skin with preclinical hyperplasia (y = 42, s = 8, n = 6) and clinically visible skin tumors (y = 63, s = 7, n = 6). The ratio was calculated and averaged from ‘y’ transverse x-y NLSI scans (100 μm × 100 μm) in ‘s’ regions from ‘n’ mice for each clinico-pathologic grade. Y-bars stand for standard error of the mean (* - p-value < 0.05 with respect to normal mice skin).

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