Abstract

Actinic cheilitis is a potentially malignant disorder of the lips. Its first cause is believed to be UV sun radiation. The lesion is highly heterogeneous, making the choice of area to be biopsied difficult. This study exploits the capabilities of time-resolved fluorescence spectroscopy for the identification of the most representative area to be biopsied. A preliminary study was performed on fourteen patients. A classification algorithm was used on data acquired on nine different biopsies. The algorithm discriminated between absent, mild, and moderate dysplasia with a sensitivity of 92.9%, 90.0%, and 80.0%, respectively. The false positive rate for healthy tissue (specificity) was 88.8%.

© 2016 Optical Society of America

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Corrections

Alessandro Cosci, Marcelo Saito Nogueira, Sebastião Prataviera, Ademar Takahama, Rebeca de Souza Azevedo, and Cristina Kurachi, "Time-resolved fluorescence spectroscopy for clinical diagnosis of actinic cheilitis: erratum," Biomed. Opt. Express 9, 648-648 (2018)
https://www.osapublishing.org/boe/abstract.cfm?uri=boe-9-2-648

28 September 2016: A correction was made to the author listing.


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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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2016 (1)

M. S. Nogueira and C. Kurachi, “Assessing the photoaging process at sun exposed and non-exposed skin using fluorescence lifetime spectroscopy,” Proc. SPIE 9703, 97031W (2016).
[Crossref]

2015 (2)

M. Brandao, R. Iwakura, F. Basilio, K. Haleplian, A. Ito, L. C. de Freitas, and L. Bachmann, “Fluorescence lifetime of normal, benign, and malignant thyroid tissues,” J. Biomed. Opt. 20(6), 067003 (2015).
[Crossref] [PubMed]

M. S. Nogueira, R. G. T. Rosa, S. Pratavieira, C. P. D’Almeida, and C. Kurachi, “Assembly and characterization of a fluorescence lifetime spectroscopy system for skin lesions diagnostic,” Proc. SPIE 9531, 95313D (2015).
[Crossref]

2014 (6)

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

J. Bec, D. M. Ma, D. R. Yankelevich, J. Liu, W. T. Ferrier, J. Southard, and L. Marcu, “Multispectral fluorescence lifetime imaging system for intravascular diagnostics with ultrasound guidance: in vivo validation in swine arteries,” J. Biophotonics 7(5), 281–285 (2014).
[Crossref] [PubMed]

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19(6), 066004 (2014).
[Crossref] [PubMed]

S. Coda, A. J. Thompson, G. T. Kennedy, K. L. Roche, L. Ayaru, D. S. Bansi, G. W. Stamp, A. V. Thillainayagam, P. M. W. French, and C. Dunsby, “Fluorescence lifetime spectroscopy of tissue autofluorescence in normal and diseased colon measured ex vivo using a fiber-optic probe,” Biomed. Opt. Express 5(2), 515–538 (2014).
[Crossref] [PubMed]

L. Pires, M. S. Nogueira, S. Pratavieira, L. T. Moriyama, and C. Kurachi, “Time-resolved fluorescence lifetime for cutaneous melanoma detection,” Biomed. Opt. Express 5(9), 3080–3089 (2014).
[Crossref] [PubMed]

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

2013 (1)

A. T. Junior, C. Kurachi, A Cosci, I. S. P Faustino, D. R Camisasca, K.B. C Fontes, F.R Pires, and R.S Azevedo, “Usefulness of tissue autofluorescence imaging in actinic cheilitis diagnosis,” J. Biomed. Opt. 18(7), 076023 (2013).
[Crossref]

2012 (2)

Y. T. Jadotte and R. A. Schwartz, “Solar cheilosis: an ominous precursor: part I. Diagnostic insights,” J. Am. Acad. Dermatol. 66(2), 173–186 (2012).
[Crossref] [PubMed]

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

2011 (1)

K. H. Awan, P. R. Morgan, and S. Warnakulasuriya, “Evaluation of an autofluorescence based imaging system (VELscope™) in the detection of oral potentially malignant disorders and benign keratoses,” Oral Oncol. 47(4), 274–277 (2011).
[Crossref] [PubMed]

2010 (2)

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (2010).
[Crossref] [PubMed]

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J. Biophotonics 3(1-2), 103–107 (2010).
[Crossref] [PubMed]

2009 (3)

I. Pavlova, C. R. Weber, R. A. Schwarz, M. D. Williams, A. M. Gillenwater, and R. Richards-Kortum, “Fluorescence spectroscopy of oral tissue: Monte Carlo modeling with site-specific tissue properties,” J. Biomed. Opt. 14(1), 014009 (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]

D. Roblyer, C. Kurachi, V. Stepanek, M. D. Williams, A. K. El-Naggar, J. J. Lee, A. M. Gillenwater, and R. Richards-Kortum, “Objective detection and delineation of oral neoplasia using autofluorescence imaging,” Cancer Prev. Res. (Phila.) 2(5), 423–431 (2009).
[Crossref] [PubMed]

2008 (2)

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]

A. S. R. Cavalcante, A. L. Anbinder, and Y. R. Carvalho, “Actinic Cheilitis: Clinical and Histological Features,” J. Oral Maxillofac. Surg. 66(3), 498–503 (2008).
[Crossref] [PubMed]

2007 (3)

M. Menta Simonsen Nico, E. A. Rivitti, and S. V. Lourenço, “Actinic cheilitis: histologic study of the entire vermilion and comparison with previous biopsy,” J. Cutan. Pathol. 34(4), 309–314 (2007).
[Crossref] [PubMed]

W. Becker, A. Bergmann, and C. Biskup, “Multispectral fluorescence lifetime imaging by TCSPC,” Microsc. Res. Tech. 70(5), 403–409 (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]

2006 (1)

2005 (2)

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

H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational Dependence of Intracellular NADH on Metabolic State Revealed by Associated Fluorescence Anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (2005).
[Crossref] [PubMed]

2004 (1)

A. Markopoulos, E. Albanidou-Farmaki, and I. Kayavis, “Actinic cheilitis: clinical and pathologic characteristics in 65 cases,” Oral Dis. 10(4), 212–216 (2004).
[Crossref] [PubMed]

2003 (1)

1999 (2)

C. S. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25(4), 323–334 (1999).
[Crossref] [PubMed]

G. E. Kaugars, T. Pillion, J. A. Svirsky, D. G. Page, J. C. Burns, and L. M. Abbey, “Actinic cheilitis: A review of 152 cases,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 88(2), 181–186 (1999).
[Crossref] [PubMed]

1998 (1)

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).
[Crossref] [PubMed]

1927 (1)

E. Gaviola, “Ein fluorometer. Apparat zur messung von fluoreszenzabklingungszeiten,” Zeitschrift fur Physik A Hadrons and Nuclei 42(11), 853–861 (1927).

Abbey, L. M.

G. E. Kaugars, T. Pillion, J. A. Svirsky, D. G. Page, J. C. Burns, and L. M. Abbey, “Actinic cheilitis: A review of 152 cases,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 88(2), 181–186 (1999).
[Crossref] [PubMed]

Albanidou-Farmaki, E.

A. Markopoulos, E. Albanidou-Farmaki, and I. Kayavis, “Actinic cheilitis: clinical and pathologic characteristics in 65 cases,” Oral Dis. 10(4), 212–216 (2004).
[Crossref] [PubMed]

Alvarez, F.

Anbinder, A. L.

A. S. R. Cavalcante, A. L. Anbinder, and Y. R. Carvalho, “Actinic Cheilitis: Clinical and Histological Features,” J. Oral Maxillofac. Surg. 66(3), 498–503 (2008).
[Crossref] [PubMed]

Andersson-Engels, S.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Awan, K. H.

K. H. Awan, P. R. Morgan, and S. Warnakulasuriya, “Evaluation of an autofluorescence based imaging system (VELscope™) in the detection of oral potentially malignant disorders and benign keratoses,” Oral Oncol. 47(4), 274–277 (2011).
[Crossref] [PubMed]

Ayaru, L.

Azevedo, R.S

A. T. Junior, C. Kurachi, A Cosci, I. S. P Faustino, D. R Camisasca, K.B. C Fontes, F.R Pires, and R.S Azevedo, “Usefulness of tissue autofluorescence imaging in actinic cheilitis diagnosis,” J. Biomed. Opt. 18(7), 076023 (2013).
[Crossref]

Bachmann, L.

M. Brandao, R. Iwakura, F. Basilio, K. Haleplian, A. Ito, L. C. de Freitas, and L. Bachmann, “Fluorescence lifetime of normal, benign, and malignant thyroid tissues,” J. Biomed. Opt. 20(6), 067003 (2015).
[Crossref] [PubMed]

Bain, A. J.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Bansi, D. S.

Basilio, F.

M. Brandao, R. Iwakura, F. Basilio, K. Haleplian, A. Ito, L. C. de Freitas, and L. Bachmann, “Fluorescence lifetime of normal, benign, and malignant thyroid tissues,” J. Biomed. Opt. 20(6), 067003 (2015).
[Crossref] [PubMed]

Baumgartner, R.

C. S. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25(4), 323–334 (1999).
[Crossref] [PubMed]

Bec, J.

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

J. Bec, D. M. Ma, D. R. Yankelevich, J. Liu, W. T. Ferrier, J. Southard, and L. Marcu, “Multispectral fluorescence lifetime imaging system for intravascular diagnostics with ultrasound guidance: in vivo validation in swine arteries,” J. Biophotonics 7(5), 281–285 (2014).
[Crossref] [PubMed]

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19(6), 066004 (2014).
[Crossref] [PubMed]

Becker, W.

W. Becker, A. Bergmann, and C. Biskup, “Multispectral fluorescence lifetime imaging by TCSPC,” Microsc. Res. Tech. 70(5), 403–409 (2007).
[Crossref] [PubMed]

Bendsøe, N.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Beres-Pawlik, E.

M. Popenda, Ł. Pajewski, Z. Grzebieniak, and E. Bereś-Pawlik, “Fluorescence lifetime measurements with all-fiber optical setup for non-invasive in-vivo diagnostics”, In 17th International Conference on Transparent Optical Networks (ICTON, 2015), pp. 1–4. IEEE.
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W. Becker, A. Bergmann, and C. Biskup, “Multispectral fluorescence lifetime imaging by TCSPC,” Microsc. Res. Tech. 70(5), 403–409 (2007).
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C. S. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25(4), 323–334 (1999).
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W. Becker, A. Bergmann, and C. Biskup, “Multispectral fluorescence lifetime imaging by TCSPC,” Microsc. Res. Tech. 70(5), 403–409 (2007).
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T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
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Brandao, M.

M. Brandao, R. Iwakura, F. Basilio, K. Haleplian, A. Ito, L. C. de Freitas, and L. Bachmann, “Fluorescence lifetime of normal, benign, and malignant thyroid tissues,” J. Biomed. Opt. 20(6), 067003 (2015).
[Crossref] [PubMed]

Bückle, R.

Burns, J. C.

G. E. Kaugars, T. Pillion, J. A. Svirsky, D. G. Page, J. C. Burns, and L. M. Abbey, “Actinic cheilitis: A review of 152 cases,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 88(2), 181–186 (1999).
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Camisasca, D. R

A. T. Junior, C. Kurachi, A Cosci, I. S. P Faustino, D. R Camisasca, K.B. C Fontes, F.R Pires, and R.S Azevedo, “Usefulness of tissue autofluorescence imaging in actinic cheilitis diagnosis,” J. Biomed. Opt. 18(7), 076023 (2013).
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A. S. R. Cavalcante, A. L. Anbinder, and Y. R. Carvalho, “Actinic Cheilitis: Clinical and Histological Features,” J. Oral Maxillofac. Surg. 66(3), 498–503 (2008).
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A. S. R. Cavalcante, A. L. Anbinder, and Y. R. Carvalho, “Actinic Cheilitis: Clinical and Histological Features,” J. Oral Maxillofac. Surg. 66(3), 498–503 (2008).
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Chuang, F. S.

Clayman, G.

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).
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Coda, S.

S. Coda, A. J. Thompson, G. T. Kennedy, K. L. Roche, L. Ayaru, D. S. Bansi, G. W. Stamp, A. V. Thillainayagam, P. M. W. French, and C. Dunsby, “Fluorescence lifetime spectroscopy of tissue autofluorescence in normal and diseased colon measured ex vivo using a fiber-optic probe,” Biomed. Opt. Express 5(2), 515–538 (2014).
[Crossref] [PubMed]

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Cosci, A

A. T. Junior, C. Kurachi, A Cosci, I. S. P Faustino, D. R Camisasca, K.B. C Fontes, F.R Pires, and R.S Azevedo, “Usefulness of tissue autofluorescence imaging in actinic cheilitis diagnosis,” J. Biomed. Opt. 18(7), 076023 (2013).
[Crossref]

D’Almeida, C. P.

M. S. Nogueira, R. G. T. Rosa, S. Pratavieira, C. P. D’Almeida, and C. Kurachi, “Assembly and characterization of a fluorescence lifetime spectroscopy system for skin lesions diagnostic,” Proc. SPIE 9531, 95313D (2015).
[Crossref]

De Beule, P. A. A.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

de Freitas, L. C.

M. Brandao, R. Iwakura, F. Basilio, K. Haleplian, A. Ito, L. C. de Freitas, and L. Bachmann, “Fluorescence lifetime of normal, benign, and malignant thyroid tissues,” J. Biomed. Opt. 20(6), 067003 (2015).
[Crossref] [PubMed]

Duchen, M. R.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Dunsby, C.

S. Coda, A. J. Thompson, G. T. Kennedy, K. L. Roche, L. Ayaru, D. S. Bansi, G. W. Stamp, A. V. Thillainayagam, P. M. W. French, and C. Dunsby, “Fluorescence lifetime spectroscopy of tissue autofluorescence in normal and diseased colon measured ex vivo using a fiber-optic probe,” Biomed. Opt. Express 5(2), 515–538 (2014).
[Crossref] [PubMed]

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J. Biophotonics 3(1-2), 103–107 (2010).
[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).
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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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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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El-Naggar, A. K.

D. Roblyer, C. Kurachi, V. Stepanek, M. D. Williams, A. K. El-Naggar, J. J. Lee, A. M. Gillenwater, and R. Richards-Kortum, “Objective detection and delineation of oral neoplasia using autofluorescence imaging,” Cancer Prev. Res. (Phila.) 2(5), 423–431 (2009).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Elsner, P.

Elson, D. S.

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
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G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J. Biophotonics 3(1-2), 103–107 (2010).
[Crossref] [PubMed]

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (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).
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J. Siegel, D. S. Elson, S. E. D. Webb, K. C. B. Lee, A. Vlandas, G. L. Gambaruto, S. Lévêque-Fort, M. J. Lever, P. J. Tadrous, G. W. Stamp, A. L. Wallace, A. Sandison, T. F. Watson, F. Alvarez, and P. M. French, “Studying biological tissue with fluorescence lifetime imaging: microscopy, endoscopy, and complex decay profiles,” Appl. Opt. 42(16), 2995–3004 (2003).
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Farwell, D. G.

Fatakdawala, H.

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19(6), 066004 (2014).
[Crossref] [PubMed]

Faustino, I. S. P

A. T. Junior, C. Kurachi, A Cosci, I. S. P Faustino, D. R Camisasca, K.B. C Fontes, F.R Pires, and R.S Azevedo, “Usefulness of tissue autofluorescence imaging in actinic cheilitis diagnosis,” J. Biomed. Opt. 18(7), 076023 (2013).
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Ferrier, W. T.

J. Bec, D. M. Ma, D. R. Yankelevich, J. Liu, W. T. Ferrier, J. Southard, and L. Marcu, “Multispectral fluorescence lifetime imaging system for intravascular diagnostics with ultrasound guidance: in vivo validation in swine arteries,” J. Biophotonics 7(5), 281–285 (2014).
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Fontes, K.B. C

A. T. Junior, C. Kurachi, A Cosci, I. S. P Faustino, D. R Camisasca, K.B. C Fontes, F.R Pires, and R.S Azevedo, “Usefulness of tissue autofluorescence imaging in actinic cheilitis diagnosis,” J. Biomed. Opt. 18(7), 076023 (2013).
[Crossref]

French, P. M.

French, P. M. W.

S. Coda, A. J. Thompson, G. T. Kennedy, K. L. Roche, L. Ayaru, D. S. Bansi, G. W. Stamp, A. V. Thillainayagam, P. M. W. French, and C. Dunsby, “Fluorescence lifetime spectroscopy of tissue autofluorescence in normal and diseased colon measured ex vivo using a fiber-optic probe,” Biomed. Opt. Express 5(2), 515–538 (2014).
[Crossref] [PubMed]

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J. Biophotonics 3(1-2), 103–107 (2010).
[Crossref] [PubMed]

Gale, J. E.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Gambaruto, G. L.

Ganeshappa, R.

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).
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E. Gaviola, “Ein fluorometer. Apparat zur messung von fluoreszenzabklingungszeiten,” Zeitschrift fur Physik A Hadrons and Nuclei 42(11), 853–861 (1927).

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.

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]

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).
[Crossref] [PubMed]

Gillenwater, A. M.

I. Pavlova, C. R. Weber, R. A. Schwarz, M. D. Williams, A. M. Gillenwater, and R. Richards-Kortum, “Fluorescence spectroscopy of oral tissue: Monte Carlo modeling with site-specific tissue properties,” J. Biomed. Opt. 14(1), 014009 (2009).
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D. Roblyer, C. Kurachi, V. Stepanek, M. D. Williams, A. K. El-Naggar, J. J. Lee, A. M. Gillenwater, and R. Richards-Kortum, “Objective detection and delineation of oral neoplasia using autofluorescence imaging,” Cancer Prev. Res. (Phila.) 2(5), 423–431 (2009).
[Crossref] [PubMed]

Gorin, F.

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (2010).
[Crossref] [PubMed]

Gorpas, D.

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19(6), 066004 (2014).
[Crossref] [PubMed]

Grevers, G.

C. S. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25(4), 323–334 (1999).
[Crossref] [PubMed]

Grzebieniak, Z.

M. Popenda, Ł. Pajewski, Z. Grzebieniak, and E. Bereś-Pawlik, “Fluorescence lifetime measurements with all-fiber optical setup for non-invasive in-vivo diagnostics”, In 17th International Conference on Transparent Optical Networks (ICTON, 2015), pp. 1–4. IEEE.
[Crossref]

Haleplian, K.

M. Brandao, R. Iwakura, F. Basilio, K. Haleplian, A. Ito, L. C. de Freitas, and L. Bachmann, “Fluorescence lifetime of normal, benign, and malignant thyroid tissues,” J. Biomed. Opt. 20(6), 067003 (2015).
[Crossref] [PubMed]

Hatami, N.

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (2010).
[Crossref] [PubMed]

Heikal, A. A.

H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational Dependence of Intracellular NADH on Metabolic State Revealed by Associated Fluorescence Anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (2005).
[Crossref] [PubMed]

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

Ito, A.

M. Brandao, R. Iwakura, F. Basilio, K. Haleplian, A. Ito, L. C. de Freitas, and L. Bachmann, “Fluorescence lifetime of normal, benign, and malignant thyroid tissues,” J. Biomed. Opt. 20(6), 067003 (2015).
[Crossref] [PubMed]

Iwakura, R.

M. Brandao, R. Iwakura, F. Basilio, K. Haleplian, A. Ito, L. C. de Freitas, and L. Bachmann, “Fluorescence lifetime of normal, benign, and malignant thyroid tissues,” J. Biomed. Opt. 20(6), 067003 (2015).
[Crossref] [PubMed]

Jacob, R.

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).
[Crossref] [PubMed]

Jadotte, Y. T.

Y. T. Jadotte and R. A. Schwartz, “Solar cheilosis: an ominous precursor: part I. Diagnostic insights,” J. Am. Acad. Dermatol. 66(2), 173–186 (2012).
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Junior, A. T.

A. T. Junior, C. Kurachi, A Cosci, I. S. P Faustino, D. R Camisasca, K.B. C Fontes, F.R Pires, and R.S Azevedo, “Usefulness of tissue autofluorescence imaging in actinic cheilitis diagnosis,” J. Biomed. Opt. 18(7), 076023 (2013).
[Crossref]

Kaatz, M.

Kasischke, K. A.

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

H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational Dependence of Intracellular NADH on Metabolic State Revealed by Associated Fluorescence Anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (2005).
[Crossref] [PubMed]

Kaugars, G. E.

G. E. Kaugars, T. Pillion, J. A. Svirsky, D. G. Page, J. C. Burns, and L. M. Abbey, “Actinic cheilitis: A review of 152 cases,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 88(2), 181–186 (1999).
[Crossref] [PubMed]

Kayavis, I.

A. Markopoulos, E. Albanidou-Farmaki, and I. Kayavis, “Actinic cheilitis: clinical and pathologic characteristics in 65 cases,” Oral Dis. 10(4), 212–216 (2004).
[Crossref] [PubMed]

Kemp, B.

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).
[Crossref] [PubMed]

Kennedy, G.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Kennedy, G. T.

S. Coda, A. J. Thompson, G. T. Kennedy, K. L. Roche, L. Ayaru, D. S. Bansi, G. W. Stamp, A. V. Thillainayagam, P. M. W. French, and C. Dunsby, “Fluorescence lifetime spectroscopy of tissue autofluorescence in normal and diseased colon measured ex vivo using a fiber-optic probe,” Biomed. Opt. Express 5(2), 515–538 (2014).
[Crossref] [PubMed]

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J. Biophotonics 3(1-2), 103–107 (2010).
[Crossref] [PubMed]

Koehler, M. J.

König, K.

Kurachi, C.

M. S. Nogueira and C. Kurachi, “Assessing the photoaging process at sun exposed and non-exposed skin using fluorescence lifetime spectroscopy,” Proc. SPIE 9703, 97031W (2016).
[Crossref]

M. S. Nogueira, R. G. T. Rosa, S. Pratavieira, C. P. D’Almeida, and C. Kurachi, “Assembly and characterization of a fluorescence lifetime spectroscopy system for skin lesions diagnostic,” Proc. SPIE 9531, 95313D (2015).
[Crossref]

L. Pires, M. S. Nogueira, S. Pratavieira, L. T. Moriyama, and C. Kurachi, “Time-resolved fluorescence lifetime for cutaneous melanoma detection,” Biomed. Opt. Express 5(9), 3080–3089 (2014).
[Crossref] [PubMed]

A. T. Junior, C. Kurachi, A Cosci, I. S. P Faustino, D. R Camisasca, K.B. C Fontes, F.R Pires, and R.S Azevedo, “Usefulness of tissue autofluorescence imaging in actinic cheilitis diagnosis,” J. Biomed. Opt. 18(7), 076023 (2013).
[Crossref]

D. Roblyer, C. Kurachi, V. Stepanek, M. D. Williams, A. K. El-Naggar, J. J. Lee, A. M. Gillenwater, and R. Richards-Kortum, “Objective detection and delineation of oral neoplasia using autofluorescence imaging,” Cancer Prev. Res. (Phila.) 2(5), 423–431 (2009).
[Crossref] [PubMed]

Lacombe, F.

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J. Biophotonics 3(1-2), 103–107 (2010).
[Crossref] [PubMed]

Lee, J. J.

D. Roblyer, C. Kurachi, V. Stepanek, M. D. Williams, A. K. El-Naggar, J. J. Lee, A. M. Gillenwater, and R. Richards-Kortum, “Objective detection and delineation of oral neoplasia using autofluorescence imaging,” Cancer Prev. Res. (Phila.) 2(5), 423–431 (2009).
[Crossref] [PubMed]

Lee, K. C. B.

Leunig, A.

C. S. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25(4), 323–334 (1999).
[Crossref] [PubMed]

Lévêque-Fort, S.

Lever, M. J.

Liu, J.

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

J. Bec, D. M. Ma, D. R. Yankelevich, J. Liu, W. T. Ferrier, J. Southard, and L. Marcu, “Multispectral fluorescence lifetime imaging system for intravascular diagnostics with ultrasound guidance: in vivo validation in swine arteries,” J. Biophotonics 7(5), 281–285 (2014).
[Crossref] [PubMed]

Lourenço, S. V.

M. Menta Simonsen Nico, E. A. Rivitti, and S. V. Lourenço, “Actinic cheilitis: histologic study of the entire vermilion and comparison with previous biopsy,” J. Cutan. Pathol. 34(4), 309–314 (2007).
[Crossref] [PubMed]

Ma, D.

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19(6), 066004 (2014).
[Crossref] [PubMed]

Ma, D. M.

J. Bec, D. M. Ma, D. R. Yankelevich, J. Liu, W. T. Ferrier, J. Southard, and L. Marcu, “Multispectral fluorescence lifetime imaging system for intravascular diagnostics with ultrasound guidance: in vivo validation in swine arteries,” J. Biophotonics 7(5), 281–285 (2014).
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J. B. MacQueen, “Some Methods for classification and Analysis of Multivariate Observations,” Proceedings of 5th Berkeley Symposium on Mathematical Statistics and Probability1(14) 281–297 (1967).

Mann, Z. F.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Manning, H. B.

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J. Biophotonics 3(1-2), 103–107 (2010).
[Crossref] [PubMed]

Marcu, L.

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19(6), 066004 (2014).
[Crossref] [PubMed]

J. Bec, D. M. Ma, D. R. Yankelevich, J. Liu, W. T. Ferrier, J. Southard, and L. Marcu, “Multispectral fluorescence lifetime imaging system for intravascular diagnostics with ultrasound guidance: in vivo validation in swine arteries,” J. Biophotonics 7(5), 281–285 (2014).
[Crossref] [PubMed]

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (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]

Markopoulos, A.

A. Markopoulos, E. Albanidou-Farmaki, and I. Kayavis, “Actinic cheilitis: clinical and pathologic characteristics in 65 cases,” Oral Dis. 10(4), 212–216 (2004).
[Crossref] [PubMed]

Mehlmann, M.

C. S. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25(4), 323–334 (1999).
[Crossref] [PubMed]

Meier, J.

Menta Simonsen Nico, M.

M. Menta Simonsen Nico, E. A. Rivitti, and S. V. Lourenço, “Actinic cheilitis: histologic study of the entire vermilion and comparison with previous biopsy,” J. Cutan. Pathol. 34(4), 309–314 (2007).
[Crossref] [PubMed]

Mitchell, M. F.

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).
[Crossref] [PubMed]

Morgan, P. R.

K. H. Awan, P. R. Morgan, and S. Warnakulasuriya, “Evaluation of an autofluorescence based imaging system (VELscope™) in the detection of oral potentially malignant disorders and benign keratoses,” Oral Oncol. 47(4), 274–277 (2011).
[Crossref] [PubMed]

Moriyama, L. T.

Neil, M. A. A.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J. Biophotonics 3(1-2), 103–107 (2010).
[Crossref] [PubMed]

Nogueira, M. S.

M. S. Nogueira and C. Kurachi, “Assessing the photoaging process at sun exposed and non-exposed skin using fluorescence lifetime spectroscopy,” Proc. SPIE 9703, 97031W (2016).
[Crossref]

M. S. Nogueira, R. G. T. Rosa, S. Pratavieira, C. P. D’Almeida, and C. Kurachi, “Assembly and characterization of a fluorescence lifetime spectroscopy system for skin lesions diagnostic,” Proc. SPIE 9531, 95313D (2015).
[Crossref]

L. Pires, M. S. Nogueira, S. Pratavieira, L. T. Moriyama, and C. Kurachi, “Time-resolved fluorescence lifetime for cutaneous melanoma detection,” Biomed. Opt. Express 5(9), 3080–3089 (2014).
[Crossref] [PubMed]

Page, D. G.

G. E. Kaugars, T. Pillion, J. A. Svirsky, D. G. Page, J. C. Burns, and L. M. Abbey, “Actinic cheilitis: A review of 152 cases,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 88(2), 181–186 (1999).
[Crossref] [PubMed]

Pajewski, L.

M. Popenda, Ł. Pajewski, Z. Grzebieniak, and E. Bereś-Pawlik, “Fluorescence lifetime measurements with all-fiber optical setup for non-invasive in-vivo diagnostics”, In 17th International Conference on Transparent Optical Networks (ICTON, 2015), pp. 1–4. IEEE.
[Crossref]

Palmer, J. L.

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).
[Crossref] [PubMed]

Patalay, R.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Pavlova, I.

I. Pavlova, C. R. Weber, R. A. Schwarz, M. D. Williams, A. M. Gillenwater, and R. Richards-Kortum, “Fluorescence spectroscopy of oral tissue: Monte Carlo modeling with site-specific tissue properties,” J. Biomed. Opt. 14(1), 014009 (2009).
[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]

Phipps, J.

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (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]

Pillion, T.

G. E. Kaugars, T. Pillion, J. A. Svirsky, D. G. Page, J. C. Burns, and L. M. Abbey, “Actinic cheilitis: A review of 152 cases,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 88(2), 181–186 (1999).
[Crossref] [PubMed]

Pires, F.R

A. T. Junior, C. Kurachi, A Cosci, I. S. P Faustino, D. R Camisasca, K.B. C Fontes, F.R Pires, and R.S Azevedo, “Usefulness of tissue autofluorescence imaging in actinic cheilitis diagnosis,” J. Biomed. Opt. 18(7), 076023 (2013).
[Crossref]

Pires, L.

Poirier, B.

Popenda, M.

M. Popenda, Ł. Pajewski, Z. Grzebieniak, and E. Bereś-Pawlik, “Fluorescence lifetime measurements with all-fiber optical setup for non-invasive in-vivo diagnostics”, In 17th International Conference on Transparent Optical Networks (ICTON, 2015), pp. 1–4. IEEE.
[Crossref]

Pratavieira, S.

M. S. Nogueira, R. G. T. Rosa, S. Pratavieira, C. P. D’Almeida, and C. Kurachi, “Assembly and characterization of a fluorescence lifetime spectroscopy system for skin lesions diagnostic,” Proc. SPIE 9531, 95313D (2015).
[Crossref]

L. Pires, M. S. Nogueira, S. Pratavieira, L. T. Moriyama, and C. Kurachi, “Time-resolved fluorescence lifetime for cutaneous melanoma detection,” Biomed. Opt. Express 5(9), 3080–3089 (2014).
[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]

Richards-Kortum, R.

I. Pavlova, C. R. Weber, R. A. Schwarz, M. D. Williams, A. M. Gillenwater, and R. Richards-Kortum, “Fluorescence spectroscopy of oral tissue: Monte Carlo modeling with site-specific tissue properties,” J. Biomed. Opt. 14(1), 014009 (2009).
[Crossref] [PubMed]

D. Roblyer, C. Kurachi, V. Stepanek, M. D. Williams, A. K. El-Naggar, J. J. Lee, A. M. Gillenwater, and R. Richards-Kortum, “Objective detection and delineation of oral neoplasia using autofluorescence imaging,” Cancer Prev. Res. (Phila.) 2(5), 423–431 (2009).
[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]

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).
[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]

Rick, K.

C. S. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25(4), 323–334 (1999).
[Crossref] [PubMed]

Rivitti, E. A.

M. Menta Simonsen Nico, E. A. Rivitti, and S. V. Lourenço, “Actinic cheilitis: histologic study of the entire vermilion and comparison with previous biopsy,” J. Cutan. Pathol. 34(4), 309–314 (2007).
[Crossref] [PubMed]

Roblyer, D.

D. Roblyer, C. Kurachi, V. Stepanek, M. D. Williams, A. K. El-Naggar, J. J. Lee, A. M. Gillenwater, and R. Richards-Kortum, “Objective detection and delineation of oral neoplasia using autofluorescence imaging,” Cancer Prev. Res. (Phila.) 2(5), 423–431 (2009).
[Crossref] [PubMed]

Roche, K. L.

Rosa, R. G. T.

M. S. Nogueira, R. G. T. Rosa, S. Pratavieira, C. P. D’Almeida, and C. Kurachi, “Assembly and characterization of a fluorescence lifetime spectroscopy system for skin lesions diagnostic,” Proc. SPIE 9531, 95313D (2015).
[Crossref]

Sandison, A.

Schrot, R. J.

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (2010).
[Crossref] [PubMed]

Schwartz, R. A.

Y. T. Jadotte and R. A. Schwartz, “Solar cheilosis: an ominous precursor: part I. Diagnostic insights,” J. Am. Acad. Dermatol. 66(2), 173–186 (2012).
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Schwarz, R. A.

I. Pavlova, C. R. Weber, R. A. Schwarz, M. D. Williams, A. M. Gillenwater, and R. Richards-Kortum, “Fluorescence spectroscopy of oral tissue: Monte Carlo modeling with site-specific tissue properties,” J. Biomed. Opt. 14(1), 014009 (2009).
[Crossref] [PubMed]

Siegel, J.

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]

Sørensen, M. B.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Southard, J.

J. Bec, D. M. Ma, D. R. Yankelevich, J. Liu, W. T. Ferrier, J. Southard, and L. Marcu, “Multispectral fluorescence lifetime imaging system for intravascular diagnostics with ultrasound guidance: in vivo validation in swine arteries,” J. Biophotonics 7(5), 281–285 (2014).
[Crossref] [PubMed]

Stamp, G. W.

Stepanek, V.

D. Roblyer, C. Kurachi, V. Stepanek, M. D. Williams, A. K. El-Naggar, J. J. Lee, A. M. Gillenwater, and R. Richards-Kortum, “Objective detection and delineation of oral neoplasia using autofluorescence imaging,” Cancer Prev. Res. (Phila.) 2(5), 423–431 (2009).
[Crossref] [PubMed]

Stepp, H.

C. S. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25(4), 323–334 (1999).
[Crossref] [PubMed]

Stoy, H.

Sun, Y.

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (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]

Svanberg, K.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Svirsky, J. A.

G. E. Kaugars, T. Pillion, J. A. Svirsky, D. G. Page, J. C. Burns, and L. M. Abbey, “Actinic cheilitis: A review of 152 cases,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 88(2), 181–186 (1999).
[Crossref] [PubMed]

Szabadkai, G.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Tadrous, P. J.

Thillainayagam, A. V.

Thompson, A. J.

S. Coda, A. J. Thompson, G. T. Kennedy, K. L. Roche, L. Ayaru, D. S. Bansi, G. W. Stamp, A. V. Thillainayagam, P. M. W. French, and C. Dunsby, “Fluorescence lifetime spectroscopy of tissue autofluorescence in normal and diseased colon measured ex vivo using a fiber-optic probe,” Biomed. Opt. Express 5(2), 515–538 (2014).
[Crossref] [PubMed]

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Tinling, S.

Viellerobe, B.

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J. Biophotonics 3(1-2), 103–107 (2010).
[Crossref] [PubMed]

Vishwasrao, H. D.

H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational Dependence of Intracellular NADH on Metabolic State Revealed by Associated Fluorescence Anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (2005).
[Crossref] [PubMed]

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

Vlandas, A.

Waitong-Brämming, U.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Wallace, A. L.

Warnakulasuriya, S.

K. H. Awan, P. R. Morgan, and S. Warnakulasuriya, “Evaluation of an autofluorescence based imaging system (VELscope™) in the detection of oral potentially malignant disorders and benign keratoses,” Oral Oncol. 47(4), 274–277 (2011).
[Crossref] [PubMed]

Watson, T. F.

Webb, S. E. D.

Webb, W. W.

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

H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational Dependence of Intracellular NADH on Metabolic State Revealed by Associated Fluorescence Anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (2005).
[Crossref] [PubMed]

Weber, C. R.

I. Pavlova, C. R. Weber, R. A. Schwarz, M. D. Williams, A. M. Gillenwater, and R. Richards-Kortum, “Fluorescence spectroscopy of oral tissue: Monte Carlo modeling with site-specific tissue properties,” J. Biomed. Opt. 14(1), 014009 (2009).
[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]

Williams, M.

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]

Williams, M. D.

I. Pavlova, C. R. Weber, R. A. Schwarz, M. D. Williams, A. M. Gillenwater, and R. Richards-Kortum, “Fluorescence spectroscopy of oral tissue: Monte Carlo modeling with site-specific tissue properties,” J. Biomed. Opt. 14(1), 014009 (2009).
[Crossref] [PubMed]

D. Roblyer, C. Kurachi, V. Stepanek, M. D. Williams, A. K. El-Naggar, J. J. Lee, A. M. Gillenwater, and R. Richards-Kortum, “Objective detection and delineation of oral neoplasia using autofluorescence imaging,” Cancer Prev. Res. (Phila.) 2(5), 423–431 (2009).
[Crossref] [PubMed]

Yankelevich, D. R.

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19(6), 066004 (2014).
[Crossref] [PubMed]

J. Bec, D. M. Ma, D. R. Yankelevich, J. Liu, W. T. Ferrier, J. Southard, and L. Marcu, “Multispectral fluorescence lifetime imaging system for intravascular diagnostics with ultrasound guidance: in vivo validation in swine arteries,” J. Biophotonics 7(5), 281–285 (2014).
[Crossref] [PubMed]

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

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Figures (2)

Fig. 1
Fig. 1 Illustration of lower lip with the 14 measurement sites. For each point the integration time was of 2 s. In red is shown a zoom of the biopsied area (for example on site number 6) and the five collection points for lifetime investigation (indicated by the letters “a,b,c,d,e”).
Fig. 2
Fig. 2 Boxplots for percentage weights and fluorescence lifetimes using 378 nm and 445 nm excitations. Black and red boxplots present the data distribution for 14 investigated areas from healthy volunteers and AC patients, respectively. Blue and purple boxplots present the same distribution for biopsied areas classified by histopathological assessment as mild and moderate dysplasia areas. Significant statistical different groups (Wilcoxon Rank Sum Test with Bonferroni correction, p < 0.01) are marked using the star symbol (*).

Tables (1)

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Table 1 Confusion matrix for classification using the TRFS algorithm versus histopathology assessment

Equations (1)

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F ( t ) = I R F * A * ( a 1   e t τ 1   +     a 2   e t τ 2     )

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