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Multimodal characterization of compositional, structural and functional features of human atherosclerotic plaquesYang Sun, Abhijit J. Chaudhari, Matthew Lam, Hongtao Xie, Diego R. Yankelevich, Jennifer Phipps, Jing Liu, Michael C. Fishbein, Jonathan M. Cannata, K. Kirk Shung, and Laura Marcu »View Author Affiliations
Yang Sun,1
Abhijit J. Chaudhari,2
Matthew Lam,1
Hongtao Xie,1
Diego R. Yankelevich,3
Jennifer Phipps,1
Jing Liu,1
Michael C. Fishbein,4
Jonathan M. Cannata,5
K. Kirk Shung,5
and Laura Marcu1,*
1University of California, Davis, Department of Biomedical Engineering, 451 Health Sciences Drive, Davis, California 95616, USA 2University of California, Davis School of Medicine, Department of Radiology, 4860 Y Street, Sacramento, California 95817, USA 3University of California, Davis, Department of Electrical and Computer Engineering, One shields Avenue, Davis, California 95616, USA 4University of California, Los Angeles, Department of Pathology, 10833 Le Conte Ave, Los Angeles, California 90095, USA 5University of Southern California, Department of Biomedical Engineering, 1042 Downey way, DRB 140, Los Angeles, California 90089, USA *Corresponding author: lmarcu@ucdavis.edu |
Biomedical Optics Express, Vol. 2, Issue 8, pp. 2288-2298 (2011)
http://dx.doi.org/10.1364/BOE.2.002288
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Abstract
Detection of atherosclerotic plaque vulnerability has critical clinical implications for avoiding sudden death in patients with high risk of plaque rupture. We report on multimodality imaging of ex-vivo human carotid plaque samples using a system that integrates fluorescence lifetime imaging (FLIM), ultrasonic backscatter microscopy (UBM), and photoacoustic imaging (PAI). Biochemical composition is differentiated with a high temporal resolution and sensitivity at the surface of the plaque by the FLIM subsystem. 3D microanatomy of the whole plaque is reconstructed by the UBM. Functional imaging associated with optical absorption contrast is evaluated from the PAI component. Simultaneous recordings of the optical, ultrasonic, and photoacoustic data present a wealth of complementary information concerning the plaque composition, structure, and function that are related to plaque vulnerability. This approach is expected to improve our ability to study atherosclerotic plaques. The multimodal system presented here can be translated into a catheter based intraluminal system for future clinical studies.
© 2011 OSA
OCIS Codes
(110.7170) Imaging systems : Ultrasound
(170.5120) Medical optics and biotechnology : Photoacoustic imaging
(170.6510) Medical optics and biotechnology : Spectroscopy, tissue diagnostics
(300.6500) Spectroscopy : Spectroscopy, time-resolved
(170.6935) Medical optics and biotechnology : Tissue characterization
ToC Category:
Multimodal Imaging
History
Original Manuscript: May 2, 2011
Revised Manuscript: July 14, 2011
Manuscript Accepted: July 14, 2011
Published: July 19, 2011
Citation
Yang Sun, Abhijit J. Chaudhari, Matthew Lam, Hongtao Xie, Diego R. Yankelevich, Jennifer Phipps, Jing Liu, Michael C. Fishbein, Jonathan M. Cannata, K. Kirk Shung, and Laura Marcu, "Multimodal characterization of compositional, structural and functional features of human atherosclerotic plaques," Biomed. Opt. Express 2, 2288-2298 (2011)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-2-8-2288
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- Y. H. Sun, R. Liu, D. S. Elson, C. W. Hollars, J. A. Jo, J. Park, Y. Sun, and L. Marcu, “Simultaneous time- and wavelength-resolved fluorescence spectroscopy for near real-time tissue diagnosis,” Opt. Lett. 33(6), 630–632 (2008). [CrossRef] [PubMed]
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- A. B. Karpiouk, B. Wang, and S. Y. Emelianov, “Development of a catheter for combined intravascular ultrasound and photoacoustic imaging,” Rev. Sci. Instrum. 81(1), 014901 (2010). [CrossRef] [PubMed]
- S. Sethuraman, J. H. Amirian, S. H. Litovsky, R. W. Smalling, and S. Y. Emelianov, “Ex vivo characterization of atherosclerosis using intravascular photoacoustic imaging,” Opt. Express 15(25), 16657–16666 (2007). [CrossRef] [PubMed]
- L. Marcu, J. A. Jo, Q. Fang, T. Papaioannou, T. Reil, J. H. Qiao, J. D. Baker, J. A. Freischlag, and M. C. Fishbein, “Detection of rupture-prone atherosclerotic plaques by time-resolved laser-induced fluorescence spectroscopy,” Atherosclerosis 204(1), 156–164 (2009). [CrossRef] [PubMed]
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- L. Marcu, J. A. Jo, Q. Fang, T. Papaloannou, J. H. Qiao, M. C. Fishbein, J. D. Baker, and J. A. Freischlag, “Detection of high-risk atherosclerotic plaques by time-resolved laser induced fluorescence spectroscopy,” Circulation 112, U678 (2005).
- L. Marcu, Q. Fang, J. A. Jo, T. Papaioannou, A. Dorafshar, T. Reil, J. H. Qiao, J. D. Baker, J. A. Freischlag, and M. C. Fishbein, “In vivo detection of macrophages in a rabbit atherosclerotic model by time-resolved laser-induced fluorescence spectroscopy,” Atherosclerosis 181(2), 295–303 (2005). [CrossRef] [PubMed]
- R. Virmani, A. P. Burke, A. Farb, and F. D. Kolodgie, “Pathology of the vulnerable plaque,” J. Am. Coll. Cardiol. 47(8Suppl), C13–C18 (2006). [CrossRef] [PubMed]
- L. Marcu, J. A. Jo, Q. Fang, T. Papaioannou, T. Reil, J. H. Qiao, J. D. Baker, J. A. Freischlag, and M. C. Fishbein, “Detection of rupture-prone atherosclerotic plaques by time-resolved laser-induced fluorescence spectroscopy,” Atherosclerosis 204(1), 156–164 (2009). [CrossRef] [PubMed]
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- L. Marcu, J. A. Jo, Q. Fang, T. Papaloannou, J. H. Qiao, M. C. Fishbein, J. D. Baker, and J. A. Freischlag, “Detection of high-risk atherosclerotic plaques by time-resolved laser induced fluorescence spectroscopy,” Circulation 112, U678 (2005).
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- N. Komiyama, G. J. Berry, M. L. Kolz, A. Oshima, J. A. Metz, P. Preuss, A. F. Brisken, M. P. Moore, P. G. Yock, and P. J. Fitzgerald, “Tissue characterization of atherosclerotic plaques by intravascular ultrasound radiofrequency signal analysis: an in vitro study of human coronary arteries,” Am. Heart J. 140(4), 565–574 (2000). [CrossRef] [PubMed]
- L. Marcu, J. A. Jo, Q. Fang, T. Papaioannou, T. Reil, J. H. Qiao, J. D. Baker, J. A. Freischlag, and M. C. Fishbein, “Detection of rupture-prone atherosclerotic plaques by time-resolved laser-induced fluorescence spectroscopy,” Atherosclerosis 204(1), 156–164 (2009). [CrossRef] [PubMed]
- J. A. Jo, Q. Fang, T. Papaioannou, J. D. Baker, A. H. Dorafshar, T. Reil, J. H. Qiao, M. C. Fishbein, J. A. Freischlag, and L. Marcu, “Laguerre-based method for analysis of time-resolved fluorescence data: application to in-vivo characterization and diagnosis of atherosclerotic lesions,” J. Biomed. Opt. 11(2), 021004 (2006). [CrossRef] [PubMed]
- L. Marcu, J. A. Jo, Q. Fang, T. Papaloannou, J. H. Qiao, M. C. Fishbein, J. D. Baker, and J. A. Freischlag, “Detection of high-risk atherosclerotic plaques by time-resolved laser induced fluorescence spectroscopy,” Circulation 112, U678 (2005).
- L. Marcu, Q. Fang, J. A. Jo, T. Papaioannou, A. Dorafshar, T. Reil, J. H. Qiao, J. D. Baker, J. A. Freischlag, and M. C. Fishbein, “In vivo detection of macrophages in a rabbit atherosclerotic model by time-resolved laser-induced fluorescence spectroscopy,” Atherosclerosis 181(2), 295–303 (2005). [CrossRef] [PubMed]
- J. Phipps, Y. H. Sun, R. Saroufeem, N. Hatami, and L. Marcu, “Fluorescence lifetime imaging microscopy for the characterization of atherosclerotic plaques,” Proc. Soc. Photo Opt. Instrum. Eng. 7161, 71612G (2009). [PubMed]
- C. Studholme, D. L. G. Hill, and D. J. Hawkes, “An overlap invariant entropy measure of 3D medical image alignment,” Pattern Recognit. 32(1), 71–86 (1999). [CrossRef]
- C. Studholme, D. L. G. Hill, and D. J. Hawkes, “An overlap invariant entropy measure of 3D medical image alignment,” Pattern Recognit. 32(1), 71–86 (1999). [CrossRef]
- I. K. Jang, B. E. Bouma, D. H. Kang, S. J. Park, S. W. Park, K. B. Seung, K. B. Choi, M. Shishkov, K. Schlendorf, E. Pomerantsev, S. L. Houser, H. T. Aretz, and G. J. Tearney, “Visualization of coronary atherosclerotic plaques in patients using optical coherence tomography: comparison with intravascular ultrasound,” J. Am. Coll. Cardiol. 39(4), 604–609 (2002). [CrossRef] [PubMed]
- I. K. Jang, B. E. Bouma, D. H. Kang, S. J. Park, S. W. Park, K. B. Seung, K. B. Choi, M. Shishkov, K. Schlendorf, E. Pomerantsev, S. L. Houser, H. T. Aretz, and G. J. Tearney, “Visualization of coronary atherosclerotic plaques in patients using optical coherence tomography: comparison with intravascular ultrasound,” J. Am. Coll. Cardiol. 39(4), 604–609 (2002). [CrossRef] [PubMed]
- Y. Sun, J. Park, D. N. Stephens, J. A. Jo, L. Sun, J. M. Cannata, R. M. Saroufeem, K. K. Shung, and L. Marcu, “Development of a dual-modal tissue diagnostic system combining time-resolved fluorescence spectroscopy and ultrasonic backscatter microscopy,” Rev. Sci. Instrum. 80(6), 065104 (2009). [CrossRef] [PubMed]
- L. Marcu, J. A. Jo, Q. Fang, T. Papaioannou, T. Reil, J. H. Qiao, J. D. Baker, J. A. Freischlag, and M. C. Fishbein, “Detection of rupture-prone atherosclerotic plaques by time-resolved laser-induced fluorescence spectroscopy,” Atherosclerosis 204(1), 156–164 (2009). [CrossRef] [PubMed]
- Y. H. Sun, R. Liu, D. S. Elson, C. W. Hollars, J. A. Jo, J. Park, Y. Sun, and L. Marcu, “Simultaneous time- and wavelength-resolved fluorescence spectroscopy for near real-time tissue diagnosis,” Opt. Lett. 33(6), 630–632 (2008). [CrossRef] [PubMed]
- D. S. Elson, J. A. Jo, and L. Marcu, “Miniaturized side-viewing imaging probe for fluorescence lifetime imaging (FLIM): validation with fluorescence dyes, tissue structural proteins and tissue specimens,” N. J. Phys. 9(127), 1–13 (2007).
- J. A. Jo, Q. Fang, T. Papaioannou, J. D. Baker, A. H. Dorafshar, T. Reil, J. H. Qiao, M. C. Fishbein, J. A. Freischlag, and L. Marcu, “Laguerre-based method for analysis of time-resolved fluorescence data: application to in-vivo characterization and diagnosis of atherosclerotic lesions,” J. Biomed. Opt. 11(2), 021004 (2006). [CrossRef] [PubMed]
- L. Marcu, J. A. Jo, Q. Fang, T. Papaloannou, J. H. Qiao, M. C. Fishbein, J. D. Baker, and J. A. Freischlag, “Detection of high-risk atherosclerotic plaques by time-resolved laser induced fluorescence spectroscopy,” Circulation 112, U678 (2005).
- L. Marcu, Q. Fang, J. A. Jo, T. Papaioannou, A. Dorafshar, T. Reil, J. H. Qiao, J. D. Baker, J. A. Freischlag, and M. C. Fishbein, “In vivo detection of macrophages in a rabbit atherosclerotic model by time-resolved laser-induced fluorescence spectroscopy,” Atherosclerosis 181(2), 295–303 (2005). [CrossRef] [PubMed]
- I. K. Jang, B. E. Bouma, D. H. Kang, S. J. Park, S. W. Park, K. B. Seung, K. B. Choi, M. Shishkov, K. Schlendorf, E. Pomerantsev, S. L. Houser, H. T. Aretz, and G. J. Tearney, “Visualization of coronary atherosclerotic plaques in patients using optical coherence tomography: comparison with intravascular ultrasound,” J. Am. Coll. Cardiol. 39(4), 604–609 (2002). [CrossRef] [PubMed]
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Am. Heart J.
- N. Komiyama, G. J. Berry, M. L. Kolz, A. Oshima, J. A. Metz, P. Preuss, A. F. Brisken, M. P. Moore, P. G. Yock, and P. J. Fitzgerald, “Tissue characterization of atherosclerotic plaques by intravascular ultrasound radiofrequency signal analysis: an in vitro study of human coronary arteries,” Am. Heart J. 140(4), 565–574 (2000). [CrossRef] [PubMed]
Annu. Rev. Phys. Chem.
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Atherosclerosis
- L. Marcu, Q. Fang, J. A. Jo, T. Papaioannou, A. Dorafshar, T. Reil, J. H. Qiao, J. D. Baker, J. A. Freischlag, and M. C. Fishbein, “In vivo detection of macrophages in a rabbit atherosclerotic model by time-resolved laser-induced fluorescence spectroscopy,” Atherosclerosis 181(2), 295–303 (2005). [CrossRef] [PubMed]
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Circulation
- L. Marcu, J. A. Jo, Q. Fang, T. Papaloannou, J. H. Qiao, M. C. Fishbein, J. D. Baker, and J. A. Freischlag, “Detection of high-risk atherosclerotic plaques by time-resolved laser induced fluorescence spectroscopy,” Circulation 112, U678 (2005).
EuroIntervention
- S. Sathyanarayana, S. Carlier, W. Li, and L. Thomas, “Characterisation of atherosclerotic plaque by spectral similarity of radiofrequency intravascular ultrasound signals,” EuroIntervention 5(1), 133–139 (2009). [CrossRef] [PubMed]
IEEE J. Sel. Top. Quantum Electron.
- L. V. Wang, “Tutorial on photoacoustic microscopy and computed tomography,” IEEE J. Sel. Top. Quantum Electron. 14(1), 171–179 (2008). [CrossRef]
IEEE Trans. Ultrason. Ferroelectr. Freq. Control
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