Abstract

Multimodal imaging probes a variety of tissue properties in a single image acquisition by merging complimentary imaging technologies. Exploiting synergies amongst the data, algorithms can be developed that lead to better tissue characterization than could be accomplished by the constituent imaging modalities taken alone. The combination of optical coherence tomography (OCT) with fluorescence lifetime imaging microscopy (FLIM) provides access to detailed tissue morphology and local biochemistry. The optical system described here merges 1310 nm swept-source OCT with time-domain FLIM having excitation at 355 and 532 nm. The pulses from 355 and 532 nm lasers have been interleaved to enable simultaneous acquisition of endogenous and exogenous fluorescence signals, respectively. The multimodal imaging system was validated using tissue phantoms. Nonspecific tagging with Alexa Flour 532 in a Watanbe rabbit aorta and active tagging of the LOX-1 receptor in human coronary artery, demonstrate the capacity of the system for simultaneous acquisition of OCT, endogenous FLIM, and exogenous FLIM in tissues.

© 2016 Optical Society of America

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  1. Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (2005).
    [Crossref] [PubMed]
  2. J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
    [Crossref] [PubMed]
  3. Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
    [Crossref]
  4. P. C. Ashok, B. B. Praveen, N. Bellini, A. Riches, K. Dholakia, and C. S. Herrington, “Multi-modal approach using Raman spectroscopy and optical coherence tomography for the discrimination of colonic adenocarcinoma from normal colon,” Biomed. Opt. Express 4(10), 2179–2186 (2013).
    [Crossref] [PubMed]
  5. Z. Chen, S. Yang, and D. Xing, “Optically integrated trimodality imaging system: combined all-optical photoacoustic microscopy, optical coherence tomography, and fluorescence imaging,” Opt. Lett. 41(7), 1636–1639 (2016).
    [Crossref] [PubMed]
  6. C. A. Patil, H. Kirshnamoorthi, D. L. Ellis, T. G. van Leeuwen, and A. Mahadevan-Jansen, “A clinical instrument for combined raman spectroscopy-optical coherence tomography of skin cancers,” Lasers Surg. Med. 43(2), 143–151 (2011).
    [Crossref] [PubMed]
  7. B. W. Graf and S. A. Boppart, “Multimodal In Vivo Skin Imaging with Integrated Optical Coherence and Multiphoton Microscopy,” IEEE J. Sel. Top. Quantum Electron. 18(4), 1280–1286 (2012).
    [Crossref] [PubMed]
  8. S. Tang, Y. Zhou, and M. J. Ju, “Multimodal optical imaging with multiphoton microscopy and optical coherence tomography,” J. Biophotonics 5(5-6), 396–403 (2012).
    [Crossref] [PubMed]
  9. S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
    [Crossref] [PubMed]
  10. J. K. Barton, F. Guzman, and A. Tumlinson, “Dual modality instrument for simultaneous optical coherence tomography imaging and fluorescence spectroscopy,” J. Biomed. Opt. 9(3), 618–623 (2004).
    [Crossref] [PubMed]
  11. L. P. Hariri, A. R. Tumlinson, D. G. Besselsen, U. Utzinger, E. W. Gerner, and J. K. Barton, “Endoscopic optical coherence tomography and laser-induced fluorescence spectroscopy in a murine colon cancer model,” Lasers Surg. Med. 38(4), 305–313 (2006).
    [Crossref] [PubMed]
  12. J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
    [Crossref] [PubMed]
  13. J. Park, J. A. Jo, S. Shrestha, P. Pande, Q. Wan, and B. E. Applegate, “A dual-modality optical coherence tomography and fluorescence lifetime imaging microscopy system for simultaneous morphological and biochemical tissue characterization,” Biomed. Opt. Express 1(1), 186–200 (2010).
    [Crossref] [PubMed]
  14. M. Gora, K. Karnowski, M. Szkulmowski, B. J. Kaluzny, R. Huber, A. Kowalczyk, and M. Wojtkowski, “Ultra high-speed swept source OCT imaging of the anterior segment of human eye at 200 kHz with adjustable imaging range,” Opt. Express 17(17), 14880–14894 (2009).
    [Crossref] [PubMed]
  15. S. Shrestha, B. E. Applegate, J. Park, X. Xiao, P. Pande, and J. A. Jo, “High-Speed Multispectral Fluorescence Lifetime Imaging Implementation for in Vivo Applications,” Opt. Lett. 35(15), 2558–2560 (2010).
    [Crossref] [PubMed]
  16. H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U.S.A. 112(10), 3128–3133 (2015).
    [Crossref] [PubMed]
  17. A. Grinvald and I. Z. Steinberg, “On the analysis of fluorescence decay kinetics by the method of least-squares,” Anal. Biochem. 59(2), 583–598 (1974).
    [Crossref] [PubMed]
  18. M. Zuker, A. G. Szabo, L. Bramall, D. T. Krajcarski, and B. Selinger, “Delta-Function Convolution Method (Dfcm) for Fluorescence Decay Experiments,” Rev. Sci. Instrum. 56(1), 14–22 (1985).
    [Crossref]
  19. 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]
  20. D. Magde, G. E. Rojas, and P. G. Seybold, “Solvent dependence of the fluorescence lifetimes of xanthene dyes,” Photochem. Photobiol. 70(5), 737–744 (1999).
    [Crossref]
  21. M. Shiomi and T. Ito, “The Watanabe heritable hyperlipidemic (WHHL) rabbit, its characteristics and history of development: a tribute to the late Dr. Yoshio Watanabe,” Atherosclerosis 207(1), 1–7 (2009).
    [Crossref] [PubMed]
  22. J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
    [Crossref] [PubMed]
  23. D. J. Rader and A. Daugherty, “Translating molecular discoveries into new therapies for atherosclerosis,” Nature 451(7181), 904–913 (2008).
    [Crossref] [PubMed]
  24. H. Chen, S. S. Ahsan, M. B. Santiago-Berrios, H. D. Abruña, and W. W. Webb, “Mechanisms of quenching of Alexa fluorophores by natural amino acids,” J. Am. Chem. Soc. 132(21), 7244–7245 (2010).
    [Crossref] [PubMed]

2016 (1)

2015 (2)

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U.S.A. 112(10), 3128–3133 (2015).
[Crossref] [PubMed]

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

2013 (2)

P. C. Ashok, B. B. Praveen, N. Bellini, A. Riches, K. Dholakia, and C. S. Herrington, “Multi-modal approach using Raman spectroscopy and optical coherence tomography for the discrimination of colonic adenocarcinoma from normal colon,” Biomed. Opt. Express 4(10), 2179–2186 (2013).
[Crossref] [PubMed]

J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
[Crossref] [PubMed]

2012 (4)

B. W. Graf and S. A. Boppart, “Multimodal In Vivo Skin Imaging with Integrated Optical Coherence and Multiphoton Microscopy,” IEEE J. Sel. Top. Quantum Electron. 18(4), 1280–1286 (2012).
[Crossref] [PubMed]

S. Tang, Y. Zhou, and M. J. Ju, “Multimodal optical imaging with multiphoton microscopy and optical coherence tomography,” J. Biophotonics 5(5-6), 396–403 (2012).
[Crossref] [PubMed]

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
[Crossref] [PubMed]

2011 (1)

C. A. Patil, H. Kirshnamoorthi, D. L. Ellis, T. G. van Leeuwen, and A. Mahadevan-Jansen, “A clinical instrument for combined raman spectroscopy-optical coherence tomography of skin cancers,” Lasers Surg. Med. 43(2), 143–151 (2011).
[Crossref] [PubMed]

2010 (4)

J. Park, J. A. Jo, S. Shrestha, P. Pande, Q. Wan, and B. E. Applegate, “A dual-modality optical coherence tomography and fluorescence lifetime imaging microscopy system for simultaneous morphological and biochemical tissue characterization,” Biomed. Opt. Express 1(1), 186–200 (2010).
[Crossref] [PubMed]

S. Shrestha, B. E. Applegate, J. Park, X. Xiao, P. Pande, and J. A. Jo, “High-Speed Multispectral Fluorescence Lifetime Imaging Implementation for in Vivo Applications,” Opt. Lett. 35(15), 2558–2560 (2010).
[Crossref] [PubMed]

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

H. Chen, S. S. Ahsan, M. B. Santiago-Berrios, H. D. Abruña, and W. W. Webb, “Mechanisms of quenching of Alexa fluorophores by natural amino acids,” J. Am. Chem. Soc. 132(21), 7244–7245 (2010).
[Crossref] [PubMed]

2009 (2)

M. Shiomi and T. Ito, “The Watanabe heritable hyperlipidemic (WHHL) rabbit, its characteristics and history of development: a tribute to the late Dr. Yoshio Watanabe,” Atherosclerosis 207(1), 1–7 (2009).
[Crossref] [PubMed]

M. Gora, K. Karnowski, M. Szkulmowski, B. J. Kaluzny, R. Huber, A. Kowalczyk, and M. Wojtkowski, “Ultra high-speed swept source OCT imaging of the anterior segment of human eye at 200 kHz with adjustable imaging range,” Opt. Express 17(17), 14880–14894 (2009).
[Crossref] [PubMed]

2008 (1)

D. J. Rader and A. Daugherty, “Translating molecular discoveries into new therapies for atherosclerosis,” Nature 451(7181), 904–913 (2008).
[Crossref] [PubMed]

2006 (1)

L. P. Hariri, A. R. Tumlinson, D. G. Besselsen, U. Utzinger, E. W. Gerner, and J. K. Barton, “Endoscopic optical coherence tomography and laser-induced fluorescence spectroscopy in a murine colon cancer model,” Lasers Surg. Med. 38(4), 305–313 (2006).
[Crossref] [PubMed]

2005 (2)

Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (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)

J. K. Barton, F. Guzman, and A. Tumlinson, “Dual modality instrument for simultaneous optical coherence tomography imaging and fluorescence spectroscopy,” J. Biomed. Opt. 9(3), 618–623 (2004).
[Crossref] [PubMed]

1999 (1)

D. Magde, G. E. Rojas, and P. G. Seybold, “Solvent dependence of the fluorescence lifetimes of xanthene dyes,” Photochem. Photobiol. 70(5), 737–744 (1999).
[Crossref]

1985 (1)

M. Zuker, A. G. Szabo, L. Bramall, D. T. Krajcarski, and B. Selinger, “Delta-Function Convolution Method (Dfcm) for Fluorescence Decay Experiments,” Rev. Sci. Instrum. 56(1), 14–22 (1985).
[Crossref]

1974 (1)

A. Grinvald and I. Z. Steinberg, “On the analysis of fluorescence decay kinetics by the method of least-squares,” Anal. Biochem. 59(2), 583–598 (1974).
[Crossref] [PubMed]

Abruña, H. D.

H. Chen, S. S. Ahsan, M. B. Santiago-Berrios, H. D. Abruña, and W. W. Webb, “Mechanisms of quenching of Alexa fluorophores by natural amino acids,” J. Am. Chem. Soc. 132(21), 7244–7245 (2010).
[Crossref] [PubMed]

Adame, J.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

Ahsan, S. S.

H. Chen, S. S. Ahsan, M. B. Santiago-Berrios, H. D. Abruña, and W. W. Webb, “Mechanisms of quenching of Alexa fluorophores by natural amino acids,” J. Am. Chem. Soc. 132(21), 7244–7245 (2010).
[Crossref] [PubMed]

Applegate, B. E.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U.S.A. 112(10), 3128–3133 (2015).
[Crossref] [PubMed]

J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
[Crossref] [PubMed]

J. Park, J. A. Jo, S. Shrestha, P. Pande, Q. Wan, and B. E. Applegate, “A dual-modality optical coherence tomography and fluorescence lifetime imaging microscopy system for simultaneous morphological and biochemical tissue characterization,” Biomed. Opt. Express 1(1), 186–200 (2010).
[Crossref] [PubMed]

S. Shrestha, B. E. Applegate, J. Park, X. Xiao, P. Pande, and J. A. Jo, “High-Speed Multispectral Fluorescence Lifetime Imaging Implementation for in Vivo Applications,” Opt. Lett. 35(15), 2558–2560 (2010).
[Crossref] [PubMed]

Ashok, P. C.

Barton, J. K.

L. P. Hariri, A. R. Tumlinson, D. G. Besselsen, U. Utzinger, E. W. Gerner, and J. K. Barton, “Endoscopic optical coherence tomography and laser-induced fluorescence spectroscopy in a murine colon cancer model,” Lasers Surg. Med. 38(4), 305–313 (2006).
[Crossref] [PubMed]

J. K. Barton, F. Guzman, and A. Tumlinson, “Dual modality instrument for simultaneous optical coherence tomography imaging and fluorescence spectroscopy,” J. Biomed. Opt. 9(3), 618–623 (2004).
[Crossref] [PubMed]

Bellini, N.

Besselsen, D. G.

L. P. Hariri, A. R. Tumlinson, D. G. Besselsen, U. Utzinger, E. W. Gerner, and J. K. Barton, “Endoscopic optical coherence tomography and laser-induced fluorescence spectroscopy in a murine colon cancer model,” Lasers Surg. Med. 38(4), 305–313 (2006).
[Crossref] [PubMed]

Blackwell, T. R.

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

Boppart, S. A.

B. W. Graf and S. A. Boppart, “Multimodal In Vivo Skin Imaging with Integrated Optical Coherence and Multiphoton Microscopy,” IEEE J. Sel. Top. Quantum Electron. 18(4), 1280–1286 (2012).
[Crossref] [PubMed]

Bramall, L.

M. Zuker, A. G. Szabo, L. Bramall, D. T. Krajcarski, and B. Selinger, “Delta-Function Convolution Method (Dfcm) for Fluorescence Decay Experiments,” Rev. Sci. Instrum. 56(1), 14–22 (1985).
[Crossref]

Buja, L. M.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

Chen, H.

H. Chen, S. S. Ahsan, M. B. Santiago-Berrios, H. D. Abruña, and W. W. Webb, “Mechanisms of quenching of Alexa fluorophores by natural amino acids,” J. Am. Chem. Soc. 132(21), 7244–7245 (2010).
[Crossref] [PubMed]

Chen, Y.

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

Chen, Z.

Z. Chen, S. Yang, and D. Xing, “Optically integrated trimodality imaging system: combined all-optical photoacoustic microscopy, optical coherence tomography, and fluorescence imaging,” Opt. Lett. 41(7), 1636–1639 (2016).
[Crossref] [PubMed]

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

Cheng, S.

J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
[Crossref] [PubMed]

Cheng, Y. S.

J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
[Crossref] [PubMed]

Clubb, F.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
[Crossref] [PubMed]

Cuenca, R.

J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
[Crossref] [PubMed]

Daugherty, A.

D. J. Rader and A. Daugherty, “Translating molecular discoveries into new therapies for atherosclerosis,” Nature 451(7181), 904–913 (2008).
[Crossref] [PubMed]

Dholakia, K.

Durand, D. B.

Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (2005).
[Crossref] [PubMed]

Ellerbee, A. K.

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U.S.A. 112(10), 3128–3133 (2015).
[Crossref] [PubMed]

Ellis, D. L.

C. A. Patil, H. Kirshnamoorthi, D. L. Ellis, T. G. van Leeuwen, and A. Mahadevan-Jansen, “A clinical instrument for combined raman spectroscopy-optical coherence tomography of skin cancers,” Lasers Surg. Med. 43(2), 143–151 (2011).
[Crossref] [PubMed]

Feldman, M. D.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

Gerner, E. W.

L. P. Hariri, A. R. Tumlinson, D. G. Besselsen, U. Utzinger, E. W. Gerner, and J. K. Barton, “Endoscopic optical coherence tomography and laser-induced fluorescence spectroscopy in a murine colon cancer model,” Lasers Surg. Med. 38(4), 305–313 (2006).
[Crossref] [PubMed]

Glunde, K.

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

Gora, M.

Graf, B. W.

B. W. Graf and S. A. Boppart, “Multimodal In Vivo Skin Imaging with Integrated Optical Coherence and Multiphoton Microscopy,” IEEE J. Sel. Top. Quantum Electron. 18(4), 1280–1286 (2012).
[Crossref] [PubMed]

Grinvald, A.

A. Grinvald and I. Z. Steinberg, “On the analysis of fluorescence decay kinetics by the method of least-squares,” Anal. Biochem. 59(2), 583–598 (1974).
[Crossref] [PubMed]

Guzman, F.

J. K. Barton, F. Guzman, and A. Tumlinson, “Dual modality instrument for simultaneous optical coherence tomography imaging and fluorescence spectroscopy,” J. Biomed. Opt. 9(3), 618–623 (2004).
[Crossref] [PubMed]

Hariri, L. P.

L. P. Hariri, A. R. Tumlinson, D. G. Besselsen, U. Utzinger, E. W. Gerner, and J. K. Barton, “Endoscopic optical coherence tomography and laser-induced fluorescence spectroscopy in a murine colon cancer model,” Lasers Surg. Med. 38(4), 305–313 (2006).
[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]

Herrington, C. S.

Huber, R.

Ito, T.

M. Shiomi and T. Ito, “The Watanabe heritable hyperlipidemic (WHHL) rabbit, its characteristics and history of development: a tribute to the late Dr. Yoshio Watanabe,” Atherosclerosis 207(1), 1–7 (2009).
[Crossref] [PubMed]

Jabbour, J. M.

J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
[Crossref] [PubMed]

Jing, J.

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

Jo, J. A.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
[Crossref] [PubMed]

J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
[Crossref] [PubMed]

S. Shrestha, B. E. Applegate, J. Park, X. Xiao, P. Pande, and J. A. Jo, “High-Speed Multispectral Fluorescence Lifetime Imaging Implementation for in Vivo Applications,” Opt. Lett. 35(15), 2558–2560 (2010).
[Crossref] [PubMed]

J. Park, J. A. Jo, S. Shrestha, P. Pande, Q. Wan, and B. E. Applegate, “A dual-modality optical coherence tomography and fluorescence lifetime imaging microscopy system for simultaneous morphological and biochemical tissue characterization,” Biomed. Opt. Express 1(1), 186–200 (2010).
[Crossref] [PubMed]

Ju, M. J.

S. Tang, Y. Zhou, and M. J. Ju, “Multimodal optical imaging with multiphoton microscopy and optical coherence tomography,” J. Biophotonics 5(5-6), 396–403 (2012).
[Crossref] [PubMed]

Kaluzny, B. J.

Karnowski, K.

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]

Kirshnamoorthi, H.

C. A. Patil, H. Kirshnamoorthi, D. L. Ellis, T. G. van Leeuwen, and A. Mahadevan-Jansen, “A clinical instrument for combined raman spectroscopy-optical coherence tomography of skin cancers,” Lasers Surg. Med. 43(2), 143–151 (2011).
[Crossref] [PubMed]

Kowalczyk, A.

Krajcarski, D. T.

M. Zuker, A. G. Szabo, L. Bramall, D. T. Krajcarski, and B. Selinger, “Delta-Function Convolution Method (Dfcm) for Fluorescence Decay Experiments,” Rev. Sci. Instrum. 56(1), 14–22 (1985).
[Crossref]

Lee, H. Y.

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U.S.A. 112(10), 3128–3133 (2015).
[Crossref] [PubMed]

Li, J.

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

Li, Q. A.

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

Liang, S.

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

Liu, G.

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

Magde, D.

D. Magde, G. E. Rojas, and P. G. Seybold, “Solvent dependence of the fluorescence lifetimes of xanthene dyes,” Photochem. Photobiol. 70(5), 737–744 (1999).
[Crossref]

Mahadevan-Jansen, A.

C. A. Patil, H. Kirshnamoorthi, D. L. Ellis, T. G. van Leeuwen, and A. Mahadevan-Jansen, “A clinical instrument for combined raman spectroscopy-optical coherence tomography of skin cancers,” Lasers Surg. Med. 43(2), 143–151 (2011).
[Crossref] [PubMed]

Maitland, K. C.

J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
[Crossref] [PubMed]

Malik, B. H.

J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
[Crossref] [PubMed]

Naphas, R.

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

Narula, J.

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

Oghalai, J. S.

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U.S.A. 112(10), 3128–3133 (2015).
[Crossref] [PubMed]

Pan, Y. T.

Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (2005).
[Crossref] [PubMed]

Pande, P.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
[Crossref] [PubMed]

J. Park, J. A. Jo, S. Shrestha, P. Pande, Q. Wan, and B. E. Applegate, “A dual-modality optical coherence tomography and fluorescence lifetime imaging microscopy system for simultaneous morphological and biochemical tissue characterization,” Biomed. Opt. Express 1(1), 186–200 (2010).
[Crossref] [PubMed]

S. Shrestha, B. E. Applegate, J. Park, X. Xiao, P. Pande, and J. A. Jo, “High-Speed Multispectral Fluorescence Lifetime Imaging Implementation for in Vivo Applications,” Opt. Lett. 35(15), 2558–2560 (2010).
[Crossref] [PubMed]

Park, J.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U.S.A. 112(10), 3128–3133 (2015).
[Crossref] [PubMed]

J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
[Crossref] [PubMed]

J. Park, J. A. Jo, S. Shrestha, P. Pande, Q. Wan, and B. E. Applegate, “A dual-modality optical coherence tomography and fluorescence lifetime imaging microscopy system for simultaneous morphological and biochemical tissue characterization,” Biomed. Opt. Express 1(1), 186–200 (2010).
[Crossref] [PubMed]

S. Shrestha, B. E. Applegate, J. Park, X. Xiao, P. Pande, and J. A. Jo, “High-Speed Multispectral Fluorescence Lifetime Imaging Implementation for in Vivo Applications,” Opt. Lett. 35(15), 2558–2560 (2010).
[Crossref] [PubMed]

Patil, C. A.

C. A. Patil, H. Kirshnamoorthi, D. L. Ellis, T. G. van Leeuwen, and A. Mahadevan-Jansen, “A clinical instrument for combined raman spectroscopy-optical coherence tomography of skin cancers,” Lasers Surg. Med. 43(2), 143–151 (2011).
[Crossref] [PubMed]

Phipps, J. E.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

Praveen, B. B.

Rader, D. J.

D. J. Rader and A. Daugherty, “Translating molecular discoveries into new therapies for atherosclerosis,” Nature 451(7181), 904–913 (2008).
[Crossref] [PubMed]

Raman, V.

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

Raphael, P. D.

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U.S.A. 112(10), 3128–3133 (2015).
[Crossref] [PubMed]

Riches, A.

Rico Jimenez, J. J.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

Rojas, G. E.

D. Magde, G. E. Rojas, and P. G. Seybold, “Solvent dependence of the fluorescence lifetimes of xanthene dyes,” Photochem. Photobiol. 70(5), 737–744 (1999).
[Crossref]

Saidi, A.

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

Santiago-Berrios, M. B.

H. Chen, S. S. Ahsan, M. B. Santiago-Berrios, H. D. Abruña, and W. W. Webb, “Mechanisms of quenching of Alexa fluorophores by natural amino acids,” J. Am. Chem. Soc. 132(21), 7244–7245 (2010).
[Crossref] [PubMed]

Schoenberg, M.

Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (2005).
[Crossref] [PubMed]

Selinger, B.

M. Zuker, A. G. Szabo, L. Bramall, D. T. Krajcarski, and B. Selinger, “Delta-Function Convolution Method (Dfcm) for Fluorescence Decay Experiments,” Rev. Sci. Instrum. 56(1), 14–22 (1985).
[Crossref]

Serafino, M. J.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

Seybold, P. G.

D. Magde, G. E. Rojas, and P. G. Seybold, “Solvent dependence of the fluorescence lifetimes of xanthene dyes,” Photochem. Photobiol. 70(5), 737–744 (1999).
[Crossref]

Shiomi, M.

M. Shiomi and T. Ito, “The Watanabe heritable hyperlipidemic (WHHL) rabbit, its characteristics and history of development: a tribute to the late Dr. Yoshio Watanabe,” Atherosclerosis 207(1), 1–7 (2009).
[Crossref] [PubMed]

Shrestha, S.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
[Crossref] [PubMed]

S. Shrestha, B. E. Applegate, J. Park, X. Xiao, P. Pande, and J. A. Jo, “High-Speed Multispectral Fluorescence Lifetime Imaging Implementation for in Vivo Applications,” Opt. Lett. 35(15), 2558–2560 (2010).
[Crossref] [PubMed]

J. Park, J. A. Jo, S. Shrestha, P. Pande, Q. Wan, and B. E. Applegate, “A dual-modality optical coherence tomography and fluorescence lifetime imaging microscopy system for simultaneous morphological and biochemical tissue characterization,” Biomed. Opt. Express 1(1), 186–200 (2010).
[Crossref] [PubMed]

Steinberg, I. Z.

A. Grinvald and I. Z. Steinberg, “On the analysis of fluorescence decay kinetics by the method of least-squares,” Anal. Biochem. 59(2), 583–598 (1974).
[Crossref] [PubMed]

Sun, C.

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

Szabo, A. G.

M. Zuker, A. G. Szabo, L. Bramall, D. T. Krajcarski, and B. Selinger, “Delta-Function Convolution Method (Dfcm) for Fluorescence Decay Experiments,” Rev. Sci. Instrum. 56(1), 14–22 (1985).
[Crossref]

Szkulmowski, M.

Tang, S.

S. Tang, Y. Zhou, and M. J. Ju, “Multimodal optical imaging with multiphoton microscopy and optical coherence tomography,” J. Biophotonics 5(5-6), 396–403 (2012).
[Crossref] [PubMed]

Tumlinson, A.

J. K. Barton, F. Guzman, and A. Tumlinson, “Dual modality instrument for simultaneous optical coherence tomography imaging and fluorescence spectroscopy,” J. Biomed. Opt. 9(3), 618–623 (2004).
[Crossref] [PubMed]

Tumlinson, A. R.

L. P. Hariri, A. R. Tumlinson, D. G. Besselsen, U. Utzinger, E. W. Gerner, and J. K. Barton, “Endoscopic optical coherence tomography and laser-induced fluorescence spectroscopy in a murine colon cancer model,” Lasers Surg. Med. 38(4), 305–313 (2006).
[Crossref] [PubMed]

Utzinger, U.

L. P. Hariri, A. R. Tumlinson, D. G. Besselsen, U. Utzinger, E. W. Gerner, and J. K. Barton, “Endoscopic optical coherence tomography and laser-induced fluorescence spectroscopy in a murine colon cancer model,” Lasers Surg. Med. 38(4), 305–313 (2006).
[Crossref] [PubMed]

van Leeuwen, T. G.

C. A. Patil, H. Kirshnamoorthi, D. L. Ellis, T. G. van Leeuwen, and A. Mahadevan-Jansen, “A clinical instrument for combined raman spectroscopy-optical coherence tomography of skin cancers,” Lasers Surg. Med. 43(2), 143–151 (2011).
[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]

Walton, B.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

Wan, Q.

Wang, Z. G.

Z. G. Wang, D. B. Durand, M. Schoenberg, and Y. T. Pan, “Fluorescence guided optical coherence tomography for the diagnosis of early bladder cancer in a rat model,” J. Urol. 174(6), 2376–2381 (2005).
[Crossref] [PubMed]

Webb, W. W.

H. Chen, S. S. Ahsan, M. B. Santiago-Berrios, H. D. Abruña, and W. W. Webb, “Mechanisms of quenching of Alexa fluorophores by natural amino acids,” J. Am. Chem. Soc. 132(21), 7244–7245 (2010).
[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]

Wierwille, J.

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

Winnard, P. T.

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

Wojtkowski, M.

Wright, J.

J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
[Crossref] [PubMed]

Xiao, X.

Xing, D.

Yang, S.

Yuan, S. A.

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

Zhang, J.

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

Zhou, Y.

S. Tang, Y. Zhou, and M. J. Ju, “Multimodal optical imaging with multiphoton microscopy and optical coherence tomography,” J. Biophotonics 5(5-6), 396–403 (2012).
[Crossref] [PubMed]

Zuker, M.

M. Zuker, A. G. Szabo, L. Bramall, D. T. Krajcarski, and B. Selinger, “Delta-Function Convolution Method (Dfcm) for Fluorescence Decay Experiments,” Rev. Sci. Instrum. 56(1), 14–22 (1985).
[Crossref]

Anal. Biochem. (1)

A. Grinvald and I. Z. Steinberg, “On the analysis of fluorescence decay kinetics by the method of least-squares,” Anal. Biochem. 59(2), 583–598 (1974).
[Crossref] [PubMed]

Atherosclerosis (2)

M. Shiomi and T. Ito, “The Watanabe heritable hyperlipidemic (WHHL) rabbit, its characteristics and history of development: a tribute to the late Dr. Yoshio Watanabe,” Atherosclerosis 207(1), 1–7 (2009).
[Crossref] [PubMed]

J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
[Crossref] [PubMed]

Biomed. Opt. Express (2)

Eur. Heart J. Cardiovasc. Imaging (1)

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

IEEE J. Sel. Top. Quantum Electron. (2)

Y. Chen, S. A. Yuan, J. Wierwille, R. Naphas, Q. A. Li, T. R. Blackwell, P. T. Winnard, V. Raman, and K. Glunde, “Integrated Optical Coherence Tomography (OCT) and Fluorescence Laminar Optical Tomography (FLOT),” IEEE J. Sel. Top. Quantum Electron. 16(4), 755–766 (2010).
[Crossref]

B. W. Graf and S. A. Boppart, “Multimodal In Vivo Skin Imaging with Integrated Optical Coherence and Multiphoton Microscopy,” IEEE J. Sel. Top. Quantum Electron. 18(4), 1280–1286 (2012).
[Crossref] [PubMed]

J. Am. Chem. Soc. (1)

H. Chen, S. S. Ahsan, M. B. Santiago-Berrios, H. D. Abruña, and W. W. Webb, “Mechanisms of quenching of Alexa fluorophores by natural amino acids,” J. Am. Chem. Soc. 132(21), 7244–7245 (2010).
[Crossref] [PubMed]

J. Biol. Chem. (1)

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]

J. Biomed. Opt. (3)

J. M. Jabbour, S. Cheng, B. H. Malik, R. Cuenca, J. A. Jo, J. Wright, Y. S. Cheng, and K. C. Maitland, “Fluorescence lifetime imaging and reflectance confocal microscopy for multiscale imaging of oral precancer,” J. Biomed. Opt. 18(4), 046012 (2013).
[Crossref] [PubMed]

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17(7), 070511 (2012).
[Crossref] [PubMed]

J. K. Barton, F. Guzman, and A. Tumlinson, “Dual modality instrument for simultaneous optical coherence tomography imaging and fluorescence spectroscopy,” J. Biomed. Opt. 9(3), 618–623 (2004).
[Crossref] [PubMed]

J. Biophotonics (1)

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Figures (5)

Fig. 1
Fig. 1 Schematic of OCT_FLIM system. Green line represents the excitation beam for exogenous FLIM; Blue line is the excitation beam for endogenous FLIM; Olive line is the emission; Maroon line is the beam for OCT. Note that overlapping co-linear beams are shown as parallel lines for clarity. The thin grey line is the trigger path. DM1-DM7: Dichroic Mirrors, L1-L10: Lenses, M1-M2:Mirror, PC1-PC2:Polarization controller, F1-F2:Longpass and bandpass filters, MCP-PMT-Multi-channel plate photo multiplier tube, Pre-Amp-Pre-amplifier, MZI-Mach Zehender Interferometer, FPGA- Field Programmable Gate Array, DG-Delay Generator.
Fig. 2
Fig. 2 a) cartoon showing the fast and slow axes of a raster scan along with frame labels referenced in the trigger diagrams of b). The arrows represent the movement of the collinear OCT and FLIM beams steered by the galvo mirrors during imaging. b) Trigger diagrams for signals used to sample OCT and FLIM. The temporal sampling rates are fixed according to sweep rate of the OCT swept source (50 kHz) and the pulse repetition rate of the FLIM excitation lasers (10 kHz). For brevity only 10 OCT lines and 2 FLIM pixels are acquired per frame in this illustration. i) sweep trigger from swept source acts as the master clock. ii) internal trigger logic on FPGA/digitizer that omits the triggers during the galvo flyback. iii) 10 kHz digitial signal output by the analog output card and sent to a delay generator. iv) undelayed trigger signal from delay generator used to trigger 355 nm laser. v) 50 μs delayed trigger signal used to trigger 532 nm laser. vi) photodiode signal used to trigger FLIM digitizer.
Fig. 3
Fig. 3 (a) FLIM images of capillary tubes filled with POPOP, NADH and Rhodamine 6G, submerged in a scattering tissue phantom. As expected POPOP has maximum peak in channel 1, NADH in channel 2 and Rhodamine 6G in channel 3. Rhodamine 6G emitted when excited with both 355 nm or 532 nm. The average lifetimes derived from the time-resolved images where: POPOP (1.26 ± 0.04ns), NADH (0.42 ± 0.03 ns) and Rhodamine (3.51 ± 0.13 ns and 3.59 ± 0.06 ns when excited with 355 and 532nm respectively). (b) OCT volume (2.4 x 2.4 x 0.98 mm) image of the submersed capillary tubes overlaid with the combined lifetime data from channel 2 and channel 3.
Fig. 4
Fig. 4 Results Watanabe rabbit aorta samples. (a) FLIM maps of Watanabe rabbit aorta (Sample 1). Intensity and lifetime maps in channel 1 and 2 due to 355nm laser excitation are consistent with collagen fluorescence. In this unstained sample low/no signal in channel 3 indicates a lack of endogenous fluorescence upon 532 nm excitation. (b) Volumetric OCT image collected simultaneously showing a single bright homogenous layer characteristic of pathological intimal thickening (PIT). (c) FLIM images of Watanabe rabbit aorta tagged with Alexa Fluor 532 (Sample 2). Maps in channel 1 and 2 due to 355nm laser are consistent with collagen fluorescence. The lifetime measured in channel 3, 1.93ns, is consistent with the Alexa Fluor 532 fluorescent tag. (d) OCT volume overlaid with the intensity map of exogenous emission. A single bright homogenous layer in the OCT volume image is characteristic of PIT.
Fig. 5
Fig. 5 Results obtained by imaging human coronary artery before and after tagging with Alexa Fluor 532. (a) FLIM maps of the artery before tagging. (b) FLIM maps of the tissue after tagging. Intensity in channel 1 in both figures is higher than that in channel 2, suggesting a strong contribution of collagen fluorescence in the signal. Comparison of the absolute emission intensities in channel 3 of these figures indicate successful tagging of Alexa Fluor 532. Average lifetime of the tissue in channel 3 before tagging is 3.07 ± 0.26 ns. Channel 3 average lifetime after tagging (1.91 ± 0.03 ns) is similar to the lifetime of nonspecific tagged Alexa Fluor 532 in the Watanbe rabbit sample. (c) Representative cross-sectional image from the OCT volume overlaid with the exogenous emission map. The OCT image is consistent with pathological intimal thickening. The dark region (center-left) is a calcified area. The fluorescence intensity is consistent with a relatively uniform expression of LOX-1 except on the right corner of the tissue. (d) OCT volume image overlaid with the exogenous FLIM emission map. Red arrow indicates the approximate location of the cross-sectional image shown in (c).

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