Abstract

In this paper, we demonstrate the ability of structured illumination microscopy to enhance the ability of fluorescence lifetime imaging to resolve fluorescence lifetimes in relatively thick samples that possess distinct but spectrally overlapping fluorescent layers. Structured illumination fluorescent lifetime imaging microscopy (SI-FLIM) is shown to be able to accurately reconstruct lifetime values in homogenous fluorophore samples (POPOP, NADH, and FAD) as well as accurately measure fluorescent lifetime in two layer models that are layered with NADH/FAD over POPOP, where NADH/FAD and POPOP have spectral overlap. Finally, the ability of SI-FLIM was demonstrated in a hamster cheek pouch ex vivo to show that more accurate lifetimes could be measured for each layer of interest in the oral mucosa (epithelium and submucosa).

© 2017 Optical Society of America

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References

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  1. J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
    [Crossref] [PubMed]
  2. E. B. van Munster and T. W. J. Gadella, “Fluorescence Lifetime Imaging Microscopy,” Microscopy Techniques 95, 143–175 (2005).
  3. S. Cheng, J. J. Rico-Jimenez, J. Jabbour, B. Malik, K. C. Maitland, J. Wright, Y. -S. Cheng, and J. A. Jo, “Flexible endoscope for continuous in vivo multispectral fluorescence lifetime imaging,” Opt. Lett. 38(9), 1515–1517 (2013).
    [Crossref] [PubMed]
  4. A. Squire and P. I. Bastiaens, “Three dimensional image restoration in fluorescence lifetime imaging microscopy,” J. Microsc. 193(1), 36–49 (1999).
    [Crossref] [PubMed]
  5. K. K. Sharman, A. Periasamy, H. Ashworth, and J. N. Demas, “Error Analysis of the Rapid Lifetime Determination Method for Double-Exponential Decays and New Windowing Schemes,” Anal. Chem. 71(5), 947–952 (1999).
    [Crossref] [PubMed]
  6. M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
    [Crossref] [PubMed]
  7. N. Bozinovic, C. Ventalon, T. Ford, and J. Mertz, “Fluorescence endomicroscopy with structured illumination,” Opt. Express 16(11), 8016–8025 (2008).
    [Crossref] [PubMed]
  8. C. Moore, S. P. Chan, J. N. Demas, and B. A. DeGraff, “Comparison of Methods for Rapid Evaluation of Lifetimes of Exponential Decays,” Appl. Spectrosc. 58(5), 603–607 (2004).
    [Crossref] [PubMed]
  9. N. Hagen, L. Gao, and T. S. Tkaczyk, “Quantitative sectioning and noise analysis for structured illumination microscopy,” Opt. Express 20(1), 403–413 (2012).
    [Crossref] [PubMed]
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    [PubMed]
  11. C. J. Gulledge and M. W. Dewhirst, “Tumor oxygenation: a matter of supply and demand,” Anticancer Res. 16(2), 741–749 (1996).
    [PubMed]
  12. P. Thomas, P. Pande, F. Clubb, J. Adame, and J. A. Jo, “Biochemical Imaging of Human Atherosclerotic Plaques with Fluorescence Lifetime Angioscopy,” Photochem. Photobiol. 86(3), 727–731 (2010).
    [Crossref] [PubMed]
  13. A. S. Kristoffersen, S. R. Erga, B. Hamre, and Ø. Frette, “Testing Fluorescence Lifetime Standards using Two-Photon Excitation and Time-Domain Instrumentation: Rhodamine B, Coumarin 6 and Lucifer Yellow,” J. Fluoresc. 24(4), 1015–1024 (2014).
    [Crossref] [PubMed]
  14. S. W. Smith, The Scientist and Engineer's Guide to Digital Signal Processing (California Technical Publishing, 1997), p. 625.
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    [Crossref] [PubMed]
  16. 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]
  17. W. Zheng, Y. Wu, D. Li, and J. Y. Qu, “Autofluorescence of epithelial tissue: single-photon versus two-photon excitation,” J. Biomed. Opt. 13, 054010 (2008).
  18. S. Cheng, R. M. Cuenca, B. Liu, B. H. Malik, J. M. Jabbour, K. C. Maitland, J. Wright, Y.-S. L. Cheng, and J. A. Jo, “Handheld multispectral fluorescence lifetime imaging system for in vivo applications,” Biomed. Opt. Express 5(3), 921–931 (2014).
    [Crossref] [PubMed]
  19. 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]
  20. Y. Wu and J. Y. Qu, “Combined depth- and time-resolved autofluorescence spectroscopy of epithelial tissue,” Opt. Lett. 31(12), 1833–1835 (2006).
    [Crossref] [PubMed]
  21. K. Maeda-Yorita and K. Aki, “Effect of Nicotinamide Adenine Dinucleotide on the Oxidation-Reduction Potentials of Lipoamide Dehydrogenase from Pig Heart,” J. Biochem. 96(3), 683–690 (1984).
    [PubMed]

2014 (3)

2013 (1)

2012 (1)

2010 (1)

P. Thomas, P. Pande, F. Clubb, J. Adame, and J. A. Jo, “Biochemical Imaging of Human Atherosclerotic Plaques with Fluorescence Lifetime Angioscopy,” Photochem. Photobiol. 86(3), 727–731 (2010).
[Crossref] [PubMed]

2008 (3)

W. Zheng, Y. Wu, D. Li, and J. Y. Qu, “Autofluorescence of epithelial tissue: single-photon versus two-photon excitation,” J. Biomed. Opt. 13, 054010 (2008).

N. Bozinovic, C. Ventalon, T. Ford, and J. Mertz, “Fluorescence endomicroscopy with structured illumination,” Opt. Express 16(11), 8016–8025 (2008).
[Crossref] [PubMed]

I. Pavlova, M. Williams, A. El-Naggar, R. Richards-Kortum, and A. Gillenwater, “Understanding the Biological Basis of Autofluorescence Imaging for Oral Cancer Detection: High-Resolution Fluorescence Microscopy in Viable Tissue,” Clin. Cancer Res. 14(8), 2396–2404 (2008).
[Crossref] [PubMed]

2007 (1)

2006 (1)

2005 (1)

E. B. van Munster and T. W. J. Gadella, “Fluorescence Lifetime Imaging Microscopy,” Microscopy Techniques 95, 143–175 (2005).

2004 (1)

2001 (1)

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

1999 (2)

A. Squire and P. I. Bastiaens, “Three dimensional image restoration in fluorescence lifetime imaging microscopy,” J. Microsc. 193(1), 36–49 (1999).
[Crossref] [PubMed]

K. K. Sharman, A. Periasamy, H. Ashworth, and J. N. Demas, “Error Analysis of the Rapid Lifetime Determination Method for Double-Exponential Decays and New Windowing Schemes,” Anal. Chem. 71(5), 947–952 (1999).
[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]

1992 (1)

J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
[Crossref] [PubMed]

1989 (1)

S. Banerjee and D. K. Bhatt, “Histochemical studies on the distribution of certain dehydrogenases in squamous cell carcinoma of cheek,” Indian J. Cancer 26(1), 21–30 (1989).
[PubMed]

1984 (1)

K. Maeda-Yorita and K. Aki, “Effect of Nicotinamide Adenine Dinucleotide on the Oxidation-Reduction Potentials of Lipoamide Dehydrogenase from Pig Heart,” J. Biochem. 96(3), 683–690 (1984).
[PubMed]

Adame, J.

P. Thomas, P. Pande, F. Clubb, J. Adame, and J. A. Jo, “Biochemical Imaging of Human Atherosclerotic Plaques with Fluorescence Lifetime Angioscopy,” Photochem. Photobiol. 86(3), 727–731 (2010).
[Crossref] [PubMed]

Aki, K.

K. Maeda-Yorita and K. Aki, “Effect of Nicotinamide Adenine Dinucleotide on the Oxidation-Reduction Potentials of Lipoamide Dehydrogenase from Pig Heart,” J. Biochem. 96(3), 683–690 (1984).
[PubMed]

Ashworth, H.

K. K. Sharman, A. Periasamy, H. Ashworth, and J. N. Demas, “Error Analysis of the Rapid Lifetime Determination Method for Double-Exponential Decays and New Windowing Schemes,” Anal. Chem. 71(5), 947–952 (1999).
[Crossref] [PubMed]

Ayaru, L.

Banerjee, S.

S. Banerjee and D. K. Bhatt, “Histochemical studies on the distribution of certain dehydrogenases in squamous cell carcinoma of cheek,” Indian J. Cancer 26(1), 21–30 (1989).
[PubMed]

Bansi, D. S.

Bastiaens, P. I.

A. Squire and P. I. Bastiaens, “Three dimensional image restoration in fluorescence lifetime imaging microscopy,” J. Microsc. 193(1), 36–49 (1999).
[Crossref] [PubMed]

Bhatt, D. K.

S. Banerjee and D. K. Bhatt, “Histochemical studies on the distribution of certain dehydrogenases in squamous cell carcinoma of cheek,” Indian J. Cancer 26(1), 21–30 (1989).
[PubMed]

Boccara, A. C.

Bozinovic, N.

Chan, S. P.

Chasles, F.

Cheng, S.

Cheng, Y. -S.

Cheng, Y.-S. L.

Clubb, F.

P. Thomas, P. Pande, F. Clubb, J. Adame, and J. A. Jo, “Biochemical Imaging of Human Atherosclerotic Plaques with Fluorescence Lifetime Angioscopy,” Photochem. Photobiol. 86(3), 727–731 (2010).
[Crossref] [PubMed]

Coda, S.

Cole, M. J.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Cuenca, R. M.

Dayel, M. J.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

DeGraff, B. A.

Demas, J. N.

C. Moore, S. P. Chan, J. N. Demas, and B. A. DeGraff, “Comparison of Methods for Rapid Evaluation of Lifetimes of Exponential Decays,” Appl. Spectrosc. 58(5), 603–607 (2004).
[Crossref] [PubMed]

K. K. Sharman, A. Periasamy, H. Ashworth, and J. N. Demas, “Error Analysis of the Rapid Lifetime Determination Method for Double-Exponential Decays and New Windowing Schemes,” Anal. Chem. 71(5), 947–952 (1999).
[Crossref] [PubMed]

Dewhirst, M. W.

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

Dowling, K.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Dubertret, B.

Dunsby, C.

El-Naggar, 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]

Erga, S. R.

A. S. Kristoffersen, S. R. Erga, B. Hamre, and Ø. Frette, “Testing Fluorescence Lifetime Standards using Two-Photon Excitation and Time-Domain Instrumentation: Rhodamine B, Coumarin 6 and Lucifer Yellow,” J. Fluoresc. 24(4), 1015–1024 (2014).
[Crossref] [PubMed]

Ford, T.

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]

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Frette, Ø.

A. S. Kristoffersen, S. R. Erga, B. Hamre, and Ø. Frette, “Testing Fluorescence Lifetime Standards using Two-Photon Excitation and Time-Domain Instrumentation: Rhodamine B, Coumarin 6 and Lucifer Yellow,” J. Fluoresc. 24(4), 1015–1024 (2014).
[Crossref] [PubMed]

Gadella, T. W. J.

E. B. van Munster and T. W. J. Gadella, “Fluorescence Lifetime Imaging Microscopy,” Microscopy Techniques 95, 143–175 (2005).

Gao, L.

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]

Gulledge, C. J.

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

Hagen, N.

Hamre, B.

A. S. Kristoffersen, S. R. Erga, B. Hamre, and Ø. Frette, “Testing Fluorescence Lifetime Standards using Two-Photon Excitation and Time-Domain Instrumentation: Rhodamine B, Coumarin 6 and Lucifer Yellow,” J. Fluoresc. 24(4), 1015–1024 (2014).
[Crossref] [PubMed]

Jabbour, J.

Jabbour, J. M.

Jo, J. A.

Johnson, M. L.

J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
[Crossref] [PubMed]

Jones, R.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Juskaitis, R.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Kennedy, G. T.

Kristoffersen, A. S.

A. S. Kristoffersen, S. R. Erga, B. Hamre, and Ø. Frette, “Testing Fluorescence Lifetime Standards using Two-Photon Excitation and Time-Domain Instrumentation: Rhodamine B, Coumarin 6 and Lucifer Yellow,” J. Fluoresc. 24(4), 1015–1024 (2014).
[Crossref] [PubMed]

Lakowicz, J. R.

J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
[Crossref] [PubMed]

Lever, M. J.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Li, D.

W. Zheng, Y. Wu, D. Li, and J. Y. Qu, “Autofluorescence of epithelial tissue: single-photon versus two-photon excitation,” J. Biomed. Opt. 13, 054010 (2008).

Liu, B.

Maeda-Yorita, K.

K. Maeda-Yorita and K. Aki, “Effect of Nicotinamide Adenine Dinucleotide on the Oxidation-Reduction Potentials of Lipoamide Dehydrogenase from Pig Heart,” J. Biochem. 96(3), 683–690 (1984).
[PubMed]

Maitland, K. C.

Malik, B.

Malik, B. H.

Mertz, J.

Moore, C.

Neil, M. A. A.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Nowaczyk, K.

J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
[Crossref] [PubMed]

Pande, P.

P. Thomas, P. Pande, F. Clubb, J. Adame, and J. A. Jo, “Biochemical Imaging of Human Atherosclerotic Plaques with Fluorescence Lifetime Angioscopy,” Photochem. Photobiol. 86(3), 727–731 (2010).
[Crossref] [PubMed]

Parsons Karavassilis, D.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Pavlova, I.

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]

Periasamy, A.

K. K. Sharman, A. Periasamy, H. Ashworth, and J. N. Demas, “Error Analysis of the Rapid Lifetime Determination Method for Double-Exponential Decays and New Windowing Schemes,” Anal. Chem. 71(5), 947–952 (1999).
[Crossref] [PubMed]

Qu, J. Y.

W. Zheng, Y. Wu, D. Li, and J. Y. Qu, “Autofluorescence of epithelial tissue: single-photon versus two-photon excitation,” J. Biomed. Opt. 13, 054010 (2008).

Y. Wu and J. Y. Qu, “Combined depth- and time-resolved autofluorescence spectroscopy of epithelial tissue,” Opt. Lett. 31(12), 1833–1835 (2006).
[Crossref] [PubMed]

Richards-Kortum, R.

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]

Rico-Jimenez, J. J.

Roche, K. L.

Sharman, K. K.

K. K. Sharman, A. Periasamy, H. Ashworth, and J. N. Demas, “Error Analysis of the Rapid Lifetime Determination Method for Double-Exponential Decays and New Windowing Schemes,” Anal. Chem. 71(5), 947–952 (1999).
[Crossref] [PubMed]

Siegel, J.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Squire, A.

A. Squire and P. I. Bastiaens, “Three dimensional image restoration in fluorescence lifetime imaging microscopy,” J. Microsc. 193(1), 36–49 (1999).
[Crossref] [PubMed]

Stamp, G. W.

Sucharov, L. O. D.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Szmacinski, H.

J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
[Crossref] [PubMed]

Thillainayagam, A. V.

Thomas, P.

P. Thomas, P. Pande, F. Clubb, J. Adame, and J. A. Jo, “Biochemical Imaging of Human Atherosclerotic Plaques with Fluorescence Lifetime Angioscopy,” Photochem. Photobiol. 86(3), 727–731 (2010).
[Crossref] [PubMed]

Thompson, A. J.

Tkaczyk, T. S.

van Munster, E. B.

E. B. van Munster and T. W. J. Gadella, “Fluorescence Lifetime Imaging Microscopy,” Microscopy Techniques 95, 143–175 (2005).

Ventalon, C.

Webb, S. E. D.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[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]

Wilson, T.

M. J. Cole, J. Siegel, S. E. D. Webb, R. Jones, K. Dowling, M. J. Dayel, D. Parsons Karavassilis, P. M. W. French, M. J. Lever, L. O. D. Sucharov, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Time-domain whole-field fluorescence lifetime imaging with optical sectioning,” J. Microsc. 203(3), 246–257 (2001).
[Crossref] [PubMed]

Wright, J.

Wu, Y.

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W. Zheng, Y. Wu, D. Li, and J. Y. Qu, “Autofluorescence of epithelial tissue: single-photon versus two-photon excitation,” J. Biomed. Opt. 13, 054010 (2008).

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Figures (6)

Fig. 1
Fig. 1 SI-FLIM system schematic. L1: fiber coupling lens; L2: collection/collimation lens; L3/L4: 1:1 spatial filter lens pair; L5: field lens; L6: tube lens; ICCD: intensified CCD camera; PD: photodiode. Black dashed lines represent the field; red dotted lines represent the image.
Fig. 2
Fig. 2 (A) Lateral resolution plot from “knife-edge” Ronchi ruling with Gaussian fit. (B) Axial response plot generated by translating a fluorescent planar sample through focus and plotting SIM image pixel intensity with Gaussian fit.
Fig. 3
Fig. 3 FLIM and SI-FLIM image comparison, color bar in nanoseconds. The capillary tubes in the SI-FLIM images appear to be smaller; however, this is a result of optical sectioning rejecting the out of focus blur that contributes to a larger perceived size in the wide-field FLIM images. Only the portion of the tube seen in the SI-FLIM images is actually in focus.
Fig. 4
Fig. 4 Schematic of the stacked capillary model. The top purple tube represents NADH/FAD and the bottom teal tube represents POPOP.
Fig. 5
Fig. 5 Top down view of optical phantoms with focus positioned at the middle of the top capillary tube. Top row: FAD overlaid on top of POPOP imaged with (A) wide-field FLIM and (B) SI-FLIM. POPOP is teal in A and B while FAD is orange-yellow. Bottom row: NADH overlaid on top of POPOP imaged with (C) wide-field FLIM and (D) SI-FLIM. POPOP is yellow for C and D while NADH is teal. The color bar for A and B is adjacent to B while the color bar for C and D is adjacent to D. Both color bars are in nanoseconds. Red circles indicate the region of capillary tube overlap that is measured while black circles represent the area of the capillary tubes without overlap that is measured.
Fig. 6
Fig. 6 Optical images of 450 nm spectral channel (targeting NADH) in preserved ex vivo hamster cheek pouch oral epithelium. (A) Sectioned image used as the first gate for the lifetime image in B. (B) SI-FLIM map of hamster cheek pouch. (C) Wide-field image used as the first gate for the lifetime image in D. (D) Wide-field FLIM map of hamster cheek pouch. As expected, the lifetime for the sectioned map is less than the wide-field map indicating removal of submucosa collagen fluorescence.

Tables (4)

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Table 1 Field of view, lateral resolution, and axial response (theoretical and measured)

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Table 2 Wide-field FLIM and SI-FLIM lifetimes in quartz capillary tubes (theoretical and measured means and standard error values for 5 samples)

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Table 3 Comparison of wide-field FLIM and SI-FLIM measurements from overlaid quartz capillary tubes containing NADH or FAD in the foreground and POPOP in the background

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Table 4 Percent Error between expected lifetime values with no overlapping fluorophore intensities and lifetime values with overlapping fluorophore intensities

Equations (5)

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

τ= Δt ln( G 2 G 1 )
S(x,y)= m 2 [1+sin(νx+ϕ)]
I mod = I B (x,y)+S(x,y)F(x,y)
I section = 2 2m ( I 1 I 2 ) 2 + ( I 2 I 3 ) 2 + ( I 1 I 3 ) 2
PercentError=100*abs((NooverlapROIOverlapROI)/(NooverlapROI))

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