Abstract

A femtosecond CARS-based nonlinear optical microscope was used to simultaneously image extracellular structural proteins and lipid-rich structures within intact aortic tissue obtained from myocardial infarction-prone Watanabe heritable hyperlipidemic rabbits (WHHLMI). Clear differences in the NLO microscopic images were observed between healthy arterial tissue and regions dominated by atherosclerotic lesions. In the current ex-vivo study, we present a single parameter based on intensity changes derived from multi-channel NLO image to classify plaque burden within the vessel. Using this parameter we were able to differentiate between healthy regions of the vessel and regions with plaque, as well as distinguish plaques relative to the age of the WHHLMI rabbit.

© 2010 OSA

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  23. R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
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  24. A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
    [CrossRef] [PubMed]
  25. J.-X. Cheng and X. S. Xie, “Coherent Anti-Stokes Raman Scattering Microscopy: Instrumentation, Theory, and Applications,” J. Phys. Chem. B 108(3), 827–840 (2004).
    [CrossRef]
  26. C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, C. P. Lin, and X. S. Xie, “Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(46), 16807–16812 (2005).
    [CrossRef] [PubMed]
  27. X. Nan, J.-X. Cheng, and X. S. Xie, “Vibrational imaging of lipid droplets in live fibroblast cells with coherent anti-Stokes Raman scattering microscopy,” J. Lipid Res. 44(11), 2202–2208 (2003).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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  39. M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Development of an animal model for spontaneous myocardial infarction (WHHLMI rabbit),” Arterioscler. Thromb. Vasc. Biol. 23(7), 1239–1244 (2003).
    [CrossRef] [PubMed]
  40. M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Correlation of vulnerable coronary plaques to sudden cardiac events. Lessons from a myocardial infarction-prone animal model (the WHHLMI rabbit),” J. Atheroscler. Thromb. 11(4), 184–189 (2004).
    [PubMed]
  41. P. Whittaker, R. A. Kloner, D. R. Boughner, and J. G. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
    [CrossRef] [PubMed]
  42. T. A. Pologruto, B. L. Sabatini, and K. Svoboda, “ScanImage: flexible software for operating laser scanning microscopes,” Biomed. Eng. Online 2(1), 13 (2003).
    [CrossRef] [PubMed]
  43. M. Strupler, A. M. Pena, M. Hernest, P. L. Tharaux, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express 15(7), 4054–4065 (2007).
    [CrossRef] [PubMed]
  44. H. C. Stary, A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull, M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, and R. W. Wissler, “A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association,” Circulation 92(5), 1355–1374 (1995).
    [PubMed]
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    [PubMed]
  46. A. M. Seddon, N. Woolf, A. La Ville, R. M. Pittilo, P. M. Rowles, P. R. Turner, and B. Lewis, “Hereditary hyperlipidemia and atherosclerosis in the rabbit due to overproduction of lipoproteins. II. Preliminary report of arterial pathology,” Arteriosclerosis 7(2), 113–124 (1987).
    [PubMed]

2010

A. C.-T. Ko, A. Ridsdale, M. S. D. Smith, L. B. Mostaço-Guidolin, M. D. Hewko, A. F. Pegoraro, E. K. Kohlenberg, B. Schattka, M. Shiomi, A. Stolow, and M. G. Sowa, “Multimodal nonlinear optical imaging of atherosclerotic plaque development in myocardial infarction-prone rabbits,” J. Biomed. Opt. 15(2), 020501 (2010).
[CrossRef] [PubMed]

M. Balu, G. Liu, Z. Chen, B. J. Tromberg, and E. O. Potma, “Fiber delivered probe for efficient CARS imaging of tissues,” Opt. Express 18(3), 2380–2388 (2010).
[CrossRef] [PubMed]

2009

A. F. Pegoraro, A. Ridsdale, D. J. Moffatt, Y. Jia, J. P. Pezacki, and A. Stolow, “Optimally chirped multimodal CARS microscopy based on a single Ti:sapphire oscillator,” Opt. Express 17(4), 2984–2996 (2009).
[CrossRef] [PubMed]

G. Liu, T. Xie, I. V. Tomov, J. Su, L. Yu, J. Zhang, B. J. Tromberg, and Z. Chen, “Rotational multiphoton endoscopy with a 1 microm fiber laser system,” Opt. Lett. 34(15), 2249–2251 (2009).
[CrossRef] [PubMed]

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[CrossRef] [PubMed]

P. Barlis and J. M. Schmitt, “Current and future developments in intracoronary optical coherence tomography imaging,” EuroIntervention 4(4), 529–533 (2009).
[PubMed]

Y.-M. Wu, H.-C. Chen, W.-T. Chang, J.-W. Jhan, H.-L. Lin, and I. Liau, “Quantitative assessment of hepatic fat of intact liver tissues with coherent anti-stokes Raman scattering microscopy,” Anal. Chem. 81(4), 1496–1504 (2009).
[CrossRef] [PubMed]

H.-W. Wang, I. M. Langohr, M. Sturek, and J.-X. Cheng, “Imaging and quantitative analysis of atherosclerotic lesions by CARS-based multimodal nonlinear optical microscopy,” Arterioscler. Thromb. Vasc. Biol. 29(9), 1342–1348 (2009).
[CrossRef] [PubMed]

2008

P. Barlis, P. W. Serruys, A. Devries, and E. Regar, “Optical coherence tomography assessment of vulnerable plaque rupture: predilection for the plaque ‘shoulder’,” Eur. Heart J. 29(16), 2023 (2008).
[CrossRef] [PubMed]

P. Barlis, G. Ferrante, F. Del Furia, and C. Di Mario, “In-vivo characterisation of coronary atherosclerosis with optical coherence tomography,” Med. J. Aust. 188(12), 728 (2008).
[PubMed]

B. K. Courtney, N. R. Munce, K. J. Anderson, A. S. Thind, G. Leung, P. E. Radau, F. S. Foster, I. A. Vitkin, R. S. Schwartz, A. J. Dick, G. A. Wright, and B. H. Strauss, “Innovations in imaging for chronic total occlusions: a glimpse into the future of angiography’s blind-spot,” Eur. Heart J. 29(5), 583–593 (2008).
[CrossRef] [PubMed]

D. A. Bluemke, S. Achenbach, M. Budoff, T. C. Gerber, B. Gersh, L. D. Hillis, W. G. Hundley, W. J. Manning, B. F. Printz, M. Stuber, and P. K. Woodard, “Noninvasive coronary artery imaging: magnetic resonance angiography and multidetector computed tomography angiography: a scientific statement from the american heart association committee on cardiovascular imaging and intervention of the council on cardiovascular radiology and intervention, and the councils on clinical cardiology and cardiovascular disease in the young,” Circulation 118(5), 586–606 (2008).
[CrossRef] [PubMed]

Y. Honda and P. J. Fitzgerald, “Frontiers in intravascular imaging technologies,” Circulation 117(15), 2024–2037 (2008).
[CrossRef] [PubMed]

H.-W. Wang, T. T. Le, and J.-X. Cheng, “Label-free imaging of arterial cells and extracellular matrix using a multimodal CARS microscope,” Opt. Commun. 281(7), 1813–1822 (2008).
[CrossRef] [PubMed]

J. Sun, Z. Zhang, B. Lu, W. Yu, Y. Yang, Y. Zhou, Y. Wang, and Z. Fan, “Identification and quantification of coronary atherosclerotic plaques: a comparison of 64-MDCT and intravascular ultrasound,” AJR Am. J. Roentgenol. 190(3), 748–754 (2008).
[CrossRef] [PubMed]

2007

M. B. Lilledahl, O. A. Haugen, C. de Lange Davies, and L. O. Svaasand, “Characterization of vulnerable plaques by multiphoton microscopy,” J. Biomed. Opt. 12(4), 044005 (2007).
[CrossRef] [PubMed]

T. T. Le, I. M. Langohr, M. J. Locker, M. Sturek, and J.-X. Cheng, “Label-free molecular imaging of atherosclerotic lesions using multimodal nonlinear optical microscopy,” J. Biomed. Opt. 12(5), 054007 (2007).
[CrossRef] [PubMed]

M. Strupler, A. M. Pena, M. Hernest, P. L. Tharaux, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express 15(7), 4054–4065 (2007).
[CrossRef] [PubMed]

R. Rocha, L. Silveira, A. B. Villaverde, C. A. Pasqualucci, M. S. Costa, A. Brugnera, and M. T. T. Pacheco, “Use of near-infrared Raman spectroscopy for identification of atherosclerotic plaques in the carotid artery,” Photomed. Laser Surg. 25(6), 482–486 (2007).
[CrossRef] [PubMed]

2006

Y. Komachi, H. Sato, and H. Tashiro, “Intravascular Raman spectroscopic catheter for molecular diagnosis of atherosclerotic coronary disease,” Appl. Opt. 45(30), 7938–7943 (2006).
[CrossRef] [PubMed]

P. Libby, “Atherosclerosis: disease biology affecting the coronary vasculature,” Am. J. Cardiol. 98(12), S3–S9 (2006).
[CrossRef] [PubMed]

J. T. Motz, M. Fitzmaurice, A. Miller, S. J. Gandhi, A. S. Haka, L. H. Galindo, R. R. Dasari, J. R. Kramer, and M. S. Feld, “In vivo Raman spectral pathology of human atherosclerosis and vulnerable plaque,” J. Biomed. Opt. 11(2), 021003 (2006).
[CrossRef] [PubMed]

2005

G. V. Nogueira, L. Silveira, A. A. Martin, R. A. Zângaro, M. T. Pacheco, M. C. Chavantes, and C. A. Pasqualucci, “Raman spectroscopy study of atherosclerosis in human carotid artery,” J. Biomed. Opt. 10(3), 031117 (2005).
[CrossRef] [PubMed]

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[CrossRef] [PubMed]

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

G. K. Hansson, “Inflammation, atherosclerosis, and coronary artery disease,” N. Engl. J. Med. 352(16), 1685–1695 (2005).
[CrossRef] [PubMed]

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, C. P. Lin, and X. S. Xie, “Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(46), 16807–16812 (2005).
[CrossRef] [PubMed]

I. K. Jang, G. J. Tearney, B. MacNeill, M. Takano, F. Moselewski, N. Iftima, M. Shishkov, S. Houser, H. T. Aretz, E. F. Halpern, and B. E. Bouma, “In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography,” Circulation 111(12), 1551–1555 (2005).
[CrossRef] [PubMed]

2004

M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Correlation of vulnerable coronary plaques to sudden cardiac events. Lessons from a myocardial infarction-prone animal model (the WHHLMI rabbit),” J. Atheroscler. Thromb. 11(4), 184–189 (2004).
[PubMed]

A. Zoumi, X. Lu, G. S. Kassab, and B. J. Tromberg, “Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy,” Biophys. J. 87(4), 2778–2786 (2004).
[CrossRef] [PubMed]

J.-X. Cheng and X. S. Xie, “Coherent Anti-Stokes Raman Scattering Microscopy: Instrumentation, Theory, and Applications,” J. Phys. Chem. B 108(3), 827–840 (2004).
[CrossRef]

2003

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21(11), 1356–1360 (2003).
[CrossRef] [PubMed]

X. Nan, J.-X. Cheng, and X. S. Xie, “Vibrational imaging of lipid droplets in live fibroblast cells with coherent anti-Stokes Raman scattering microscopy,” J. Lipid Res. 44(11), 2202–2208 (2003).
[CrossRef] [PubMed]

M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Development of an animal model for spontaneous myocardial infarction (WHHLMI rabbit),” Arterioscler. Thromb. Vasc. Biol. 23(7), 1239–1244 (2003).
[CrossRef] [PubMed]

T. A. Pologruto, B. L. Sabatini, and K. Svoboda, “ScanImage: flexible software for operating laser scanning microscopes,” Biomed. Eng. Online 2(1), 13 (2003).
[CrossRef] [PubMed]

2002

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

2000

T. J. Römer, J. F. Brennan, G. J. Puppels, A. H. Zwinderman, S. G. van Duinen, A. van der Laarse, A. F. van der Steen, N. A. Bom, and A. V. Bruschke, “Intravascular ultrasound combined with Raman spectroscopy to localize and quantify cholesterol and calcium salts in atherosclerotic coronary arteries,” Arterioscler. Thromb. Vasc. Biol. 20(2), 478–483 (2000).
[PubMed]

A. J. Lusis, “Atherosclerosis,” Nature 407(6801), 233–241 (2000).
[CrossRef] [PubMed]

1998

P. G. Yock and P. J. Fitzgerald, “Optimal Directional Coronary Atherectomy Final Results of the Optimal Atherectomy Restenosis Study (OARS),” Am. J. Cardiol. 81, 27E–32E (1998).
[PubMed]

1995

H. C. Stary, A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull, M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, and R. W. Wissler, “A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association,” Circulation 92(5), 1355–1374 (1995).
[PubMed]

1994

P. Whittaker, R. A. Kloner, D. R. Boughner, and J. G. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
[CrossRef] [PubMed]

1993

J. M. Hodgson, K. G. Reddy, R. Suneja, R. N. Nair, E. J. Lesnefsky, and H. M. Sheehan, “Intracoronary ultrasound imaging: correlation of plaque morphology with angiography, clinical syndrome and procedural results in patients undergoing coronary angioplasty,” J. Am. Coll. Cardiol. 21(1), 35–44 (1993).
[CrossRef] [PubMed]

1987

A. M. Seddon, N. Woolf, A. La Ville, R. M. Pittilo, P. M. Rowles, P. R. Turner, and B. Lewis, “Hereditary hyperlipidemia and atherosclerosis in the rabbit due to overproduction of lipoproteins. II. Preliminary report of arterial pathology,” Arteriosclerosis 7(2), 113–124 (1987).
[PubMed]

1983

L. M. Buja, T. Kita, J. L. Goldstein, Y. Watanabe, and M. S. Brown, “Cellular pathology of progressive atherosclerosis in the WHHL rabbit. An animal model of familial hypercholesterolemia,” Arteriosclerosis 3(1), 87–101 (1983).
[PubMed]

Achenbach, S.

D. A. Bluemke, S. Achenbach, M. Budoff, T. C. Gerber, B. Gersh, L. D. Hillis, W. G. Hundley, W. J. Manning, B. F. Printz, M. Stuber, and P. K. Woodard, “Noninvasive coronary artery imaging: magnetic resonance angiography and multidetector computed tomography angiography: a scientific statement from the american heart association committee on cardiovascular imaging and intervention of the council on cardiovascular radiology and intervention, and the councils on clinical cardiology and cardiovascular disease in the young,” Circulation 118(5), 586–606 (2008).
[CrossRef] [PubMed]

Ahn, Y. C.

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R. Rocha, L. Silveira, A. B. Villaverde, C. A. Pasqualucci, M. S. Costa, A. Brugnera, and M. T. T. Pacheco, “Use of near-infrared Raman spectroscopy for identification of atherosclerotic plaques in the carotid artery,” Photomed. Laser Surg. 25(6), 482–486 (2007).
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P. Barlis, G. Ferrante, F. Del Furia, and C. Di Mario, “In-vivo characterisation of coronary atherosclerosis with optical coherence tomography,” Med. J. Aust. 188(12), 728 (2008).
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P. Barlis, G. Ferrante, F. Del Furia, and C. Di Mario, “In-vivo characterisation of coronary atherosclerosis with optical coherence tomography,” Med. J. Aust. 188(12), 728 (2008).
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M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Development of an animal model for spontaneous myocardial infarction (WHHLMI rabbit),” Arterioscler. Thromb. Vasc. Biol. 23(7), 1239–1244 (2003).
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B. K. Courtney, N. R. Munce, K. J. Anderson, A. S. Thind, G. Leung, P. E. Radau, F. S. Foster, I. A. Vitkin, R. S. Schwartz, A. J. Dick, G. A. Wright, and B. H. Strauss, “Innovations in imaging for chronic total occlusions: a glimpse into the future of angiography’s blind-spot,” Eur. Heart J. 29(5), 583–593 (2008).
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H. C. Stary, A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull, M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, and R. W. Wissler, “A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association,” Circulation 92(5), 1355–1374 (1995).
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J. T. Motz, M. Fitzmaurice, A. Miller, S. J. Gandhi, A. S. Haka, L. H. Galindo, R. R. Dasari, J. R. Kramer, and M. S. Feld, “In vivo Raman spectral pathology of human atherosclerosis and vulnerable plaque,” J. Biomed. Opt. 11(2), 021003 (2006).
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J. T. Motz, M. Fitzmaurice, A. Miller, S. J. Gandhi, A. S. Haka, L. H. Galindo, R. R. Dasari, J. R. Kramer, and M. S. Feld, “In vivo Raman spectral pathology of human atherosclerosis and vulnerable plaque,” J. Biomed. Opt. 11(2), 021003 (2006).
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D. A. Bluemke, S. Achenbach, M. Budoff, T. C. Gerber, B. Gersh, L. D. Hillis, W. G. Hundley, W. J. Manning, B. F. Printz, M. Stuber, and P. K. Woodard, “Noninvasive coronary artery imaging: magnetic resonance angiography and multidetector computed tomography angiography: a scientific statement from the american heart association committee on cardiovascular imaging and intervention of the council on cardiovascular radiology and intervention, and the councils on clinical cardiology and cardiovascular disease in the young,” Circulation 118(5), 586–606 (2008).
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D. A. Bluemke, S. Achenbach, M. Budoff, T. C. Gerber, B. Gersh, L. D. Hillis, W. G. Hundley, W. J. Manning, B. F. Printz, M. Stuber, and P. K. Woodard, “Noninvasive coronary artery imaging: magnetic resonance angiography and multidetector computed tomography angiography: a scientific statement from the american heart association committee on cardiovascular imaging and intervention of the council on cardiovascular radiology and intervention, and the councils on clinical cardiology and cardiovascular disease in the young,” Circulation 118(5), 586–606 (2008).
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H. C. Stary, A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull, M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, and R. W. Wissler, “A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association,” Circulation 92(5), 1355–1374 (1995).
[PubMed]

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L. M. Buja, T. Kita, J. L. Goldstein, Y. Watanabe, and M. S. Brown, “Cellular pathology of progressive atherosclerosis in the WHHL rabbit. An animal model of familial hypercholesterolemia,” Arteriosclerosis 3(1), 87–101 (1983).
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J. T. Motz, M. Fitzmaurice, A. Miller, S. J. Gandhi, A. S. Haka, L. H. Galindo, R. R. Dasari, J. R. Kramer, and M. S. Feld, “In vivo Raman spectral pathology of human atherosclerosis and vulnerable plaque,” J. Biomed. Opt. 11(2), 021003 (2006).
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I. K. Jang, G. J. Tearney, B. MacNeill, M. Takano, F. Moselewski, N. Iftima, M. Shishkov, S. Houser, H. T. Aretz, E. F. Halpern, and B. E. Bouma, “In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography,” Circulation 111(12), 1551–1555 (2005).
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M. B. Lilledahl, O. A. Haugen, C. de Lange Davies, and L. O. Svaasand, “Characterization of vulnerable plaques by multiphoton microscopy,” J. Biomed. Opt. 12(4), 044005 (2007).
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F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
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D. A. Bluemke, S. Achenbach, M. Budoff, T. C. Gerber, B. Gersh, L. D. Hillis, W. G. Hundley, W. J. Manning, B. F. Printz, M. Stuber, and P. K. Woodard, “Noninvasive coronary artery imaging: magnetic resonance angiography and multidetector computed tomography angiography: a scientific statement from the american heart association committee on cardiovascular imaging and intervention of the council on cardiovascular radiology and intervention, and the councils on clinical cardiology and cardiovascular disease in the young,” Circulation 118(5), 586–606 (2008).
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Y. Honda and P. J. Fitzgerald, “Frontiers in intravascular imaging technologies,” Circulation 117(15), 2024–2037 (2008).
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I. K. Jang, G. J. Tearney, B. MacNeill, M. Takano, F. Moselewski, N. Iftima, M. Shishkov, S. Houser, H. T. Aretz, E. F. Halpern, and B. E. Bouma, “In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography,” Circulation 111(12), 1551–1555 (2005).
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D. A. Bluemke, S. Achenbach, M. Budoff, T. C. Gerber, B. Gersh, L. D. Hillis, W. G. Hundley, W. J. Manning, B. F. Printz, M. Stuber, and P. K. Woodard, “Noninvasive coronary artery imaging: magnetic resonance angiography and multidetector computed tomography angiography: a scientific statement from the american heart association committee on cardiovascular imaging and intervention of the council on cardiovascular radiology and intervention, and the councils on clinical cardiology and cardiovascular disease in the young,” Circulation 118(5), 586–606 (2008).
[CrossRef] [PubMed]

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W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

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I. K. Jang, G. J. Tearney, B. MacNeill, M. Takano, F. Moselewski, N. Iftima, M. Shishkov, S. Houser, H. T. Aretz, E. F. Halpern, and B. E. Bouma, “In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography,” Circulation 111(12), 1551–1555 (2005).
[CrossRef] [PubMed]

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H. C. Stary, A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull, M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, and R. W. Wissler, “A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association,” Circulation 92(5), 1355–1374 (1995).
[PubMed]

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M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Correlation of vulnerable coronary plaques to sudden cardiac events. Lessons from a myocardial infarction-prone animal model (the WHHLMI rabbit),” J. Atheroscler. Thromb. 11(4), 184–189 (2004).
[PubMed]

M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Development of an animal model for spontaneous myocardial infarction (WHHLMI rabbit),” Arterioscler. Thromb. Vasc. Biol. 23(7), 1239–1244 (2003).
[CrossRef] [PubMed]

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I. K. Jang, G. J. Tearney, B. MacNeill, M. Takano, F. Moselewski, N. Iftima, M. Shishkov, S. Houser, H. T. Aretz, E. F. Halpern, and B. E. Bouma, “In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography,” Circulation 111(12), 1551–1555 (2005).
[CrossRef] [PubMed]

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Y.-M. Wu, H.-C. Chen, W.-T. Chang, J.-W. Jhan, H.-L. Lin, and I. Liau, “Quantitative assessment of hepatic fat of intact liver tissues with coherent anti-stokes Raman scattering microscopy,” Anal. Chem. 81(4), 1496–1504 (2009).
[CrossRef] [PubMed]

Jia, Y.

Jung, W.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
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M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Development of an animal model for spontaneous myocardial infarction (WHHLMI rabbit),” Arterioscler. Thromb. Vasc. Biol. 23(7), 1239–1244 (2003).
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L. M. Buja, T. Kita, J. L. Goldstein, Y. Watanabe, and M. S. Brown, “Cellular pathology of progressive atherosclerosis in the WHHL rabbit. An animal model of familial hypercholesterolemia,” Arteriosclerosis 3(1), 87–101 (1983).
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P. Whittaker, R. A. Kloner, D. R. Boughner, and J. G. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
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P. Barlis, P. W. Serruys, A. Devries, and E. Regar, “Optical coherence tomography assessment of vulnerable plaque rupture: predilection for the plaque ‘shoulder’,” Eur. Heart J. 29(16), 2023 (2008).
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[CrossRef] [PubMed]

A. F. Pegoraro, A. Ridsdale, D. J. Moffatt, Y. Jia, J. P. Pezacki, and A. Stolow, “Optimally chirped multimodal CARS microscopy based on a single Ti:sapphire oscillator,” Opt. Express 17(4), 2984–2996 (2009).
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[PubMed]

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P. Barlis, P. W. Serruys, A. Devries, and E. Regar, “Optical coherence tomography assessment of vulnerable plaque rupture: predilection for the plaque ‘shoulder’,” Eur. Heart J. 29(16), 2023 (2008).
[CrossRef] [PubMed]

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J. M. Hodgson, K. G. Reddy, R. Suneja, R. N. Nair, E. J. Lesnefsky, and H. M. Sheehan, “Intracoronary ultrasound imaging: correlation of plaque morphology with angiography, clinical syndrome and procedural results in patients undergoing coronary angioplasty,” J. Am. Coll. Cardiol. 21(1), 35–44 (1993).
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A. C.-T. Ko, A. Ridsdale, M. S. D. Smith, L. B. Mostaço-Guidolin, M. D. Hewko, A. F. Pegoraro, E. K. Kohlenberg, B. Schattka, M. Shiomi, A. Stolow, and M. G. Sowa, “Multimodal nonlinear optical imaging of atherosclerotic plaque development in myocardial infarction-prone rabbits,” J. Biomed. Opt. 15(2), 020501 (2010).
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R. Rocha, L. Silveira, A. B. Villaverde, C. A. Pasqualucci, M. S. Costa, A. Brugnera, and M. T. T. Pacheco, “Use of near-infrared Raman spectroscopy for identification of atherosclerotic plaques in the carotid artery,” Photomed. Laser Surg. 25(6), 482–486 (2007).
[CrossRef] [PubMed]

G. V. Nogueira, L. Silveira, A. A. Martin, R. A. Zângaro, M. T. Pacheco, M. C. Chavantes, and C. A. Pasqualucci, “Raman spectroscopy study of atherosclerosis in human carotid artery,” J. Biomed. Opt. 10(3), 031117 (2005).
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A. C.-T. Ko, A. Ridsdale, M. S. D. Smith, L. B. Mostaço-Guidolin, M. D. Hewko, A. F. Pegoraro, E. K. Kohlenberg, B. Schattka, M. Shiomi, A. Stolow, and M. G. Sowa, “Multimodal nonlinear optical imaging of atherosclerotic plaque development in myocardial infarction-prone rabbits,” J. Biomed. Opt. 15(2), 020501 (2010).
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A. C.-T. Ko, A. Ridsdale, M. S. D. Smith, L. B. Mostaço-Guidolin, M. D. Hewko, A. F. Pegoraro, E. K. Kohlenberg, B. Schattka, M. Shiomi, A. Stolow, and M. G. Sowa, “Multimodal nonlinear optical imaging of atherosclerotic plaque development in myocardial infarction-prone rabbits,” J. Biomed. Opt. 15(2), 020501 (2010).
[CrossRef] [PubMed]

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[PubMed]

Stolow, A.

A. C.-T. Ko, A. Ridsdale, M. S. D. Smith, L. B. Mostaço-Guidolin, M. D. Hewko, A. F. Pegoraro, E. K. Kohlenberg, B. Schattka, M. Shiomi, A. Stolow, and M. G. Sowa, “Multimodal nonlinear optical imaging of atherosclerotic plaque development in myocardial infarction-prone rabbits,” J. Biomed. Opt. 15(2), 020501 (2010).
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A. F. Pegoraro, A. Ridsdale, D. J. Moffatt, Y. Jia, J. P. Pezacki, and A. Stolow, “Optimally chirped multimodal CARS microscopy based on a single Ti:sapphire oscillator,” Opt. Express 17(4), 2984–2996 (2009).
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Strauss, B. H.

B. K. Courtney, N. R. Munce, K. J. Anderson, A. S. Thind, G. Leung, P. E. Radau, F. S. Foster, I. A. Vitkin, R. S. Schwartz, A. J. Dick, G. A. Wright, and B. H. Strauss, “Innovations in imaging for chronic total occlusions: a glimpse into the future of angiography’s blind-spot,” Eur. Heart J. 29(5), 583–593 (2008).
[CrossRef] [PubMed]

Strupler, M.

Stuber, M.

D. A. Bluemke, S. Achenbach, M. Budoff, T. C. Gerber, B. Gersh, L. D. Hillis, W. G. Hundley, W. J. Manning, B. F. Printz, M. Stuber, and P. K. Woodard, “Noninvasive coronary artery imaging: magnetic resonance angiography and multidetector computed tomography angiography: a scientific statement from the american heart association committee on cardiovascular imaging and intervention of the council on cardiovascular radiology and intervention, and the councils on clinical cardiology and cardiovascular disease in the young,” Circulation 118(5), 586–606 (2008).
[CrossRef] [PubMed]

Sturek, M.

H.-W. Wang, I. M. Langohr, M. Sturek, and J.-X. Cheng, “Imaging and quantitative analysis of atherosclerotic lesions by CARS-based multimodal nonlinear optical microscopy,” Arterioscler. Thromb. Vasc. Biol. 29(9), 1342–1348 (2009).
[CrossRef] [PubMed]

T. T. Le, I. M. Langohr, M. J. Locker, M. Sturek, and J.-X. Cheng, “Label-free molecular imaging of atherosclerotic lesions using multimodal nonlinear optical microscopy,” J. Biomed. Opt. 12(5), 054007 (2007).
[CrossRef] [PubMed]

Su, J.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[CrossRef] [PubMed]

G. Liu, T. Xie, I. V. Tomov, J. Su, L. Yu, J. Zhang, B. J. Tromberg, and Z. Chen, “Rotational multiphoton endoscopy with a 1 microm fiber laser system,” Opt. Lett. 34(15), 2249–2251 (2009).
[CrossRef] [PubMed]

Sun, J.

J. Sun, Z. Zhang, B. Lu, W. Yu, Y. Yang, Y. Zhou, Y. Wang, and Z. Fan, “Identification and quantification of coronary atherosclerotic plaques: a comparison of 64-MDCT and intravascular ultrasound,” AJR Am. J. Roentgenol. 190(3), 748–754 (2008).
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J. M. Hodgson, K. G. Reddy, R. Suneja, R. N. Nair, E. J. Lesnefsky, and H. M. Sheehan, “Intracoronary ultrasound imaging: correlation of plaque morphology with angiography, clinical syndrome and procedural results in patients undergoing coronary angioplasty,” J. Am. Coll. Cardiol. 21(1), 35–44 (1993).
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M. B. Lilledahl, O. A. Haugen, C. de Lange Davies, and L. O. Svaasand, “Characterization of vulnerable plaques by multiphoton microscopy,” J. Biomed. Opt. 12(4), 044005 (2007).
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Svoboda, K.

T. A. Pologruto, B. L. Sabatini, and K. Svoboda, “ScanImage: flexible software for operating laser scanning microscopes,” Biomed. Eng. Online 2(1), 13 (2003).
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Takano, M.

I. K. Jang, G. J. Tearney, B. MacNeill, M. Takano, F. Moselewski, N. Iftima, M. Shishkov, S. Houser, H. T. Aretz, E. F. Halpern, and B. E. Bouma, “In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography,” Circulation 111(12), 1551–1555 (2005).
[CrossRef] [PubMed]

Tang, S.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[CrossRef] [PubMed]

Tashiro, H.

Tearney, G. J.

I. K. Jang, G. J. Tearney, B. MacNeill, M. Takano, F. Moselewski, N. Iftima, M. Shishkov, S. Houser, H. T. Aretz, E. F. Halpern, and B. E. Bouma, “In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography,” Circulation 111(12), 1551–1555 (2005).
[CrossRef] [PubMed]

Tharaux, P. L.

Thind, A. S.

B. K. Courtney, N. R. Munce, K. J. Anderson, A. S. Thind, G. Leung, P. E. Radau, F. S. Foster, I. A. Vitkin, R. S. Schwartz, A. J. Dick, G. A. Wright, and B. H. Strauss, “Innovations in imaging for chronic total occlusions: a glimpse into the future of angiography’s blind-spot,” Eur. Heart J. 29(5), 583–593 (2008).
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Tomov, I. V.

Tromberg, B. J.

M. Balu, G. Liu, Z. Chen, B. J. Tromberg, and E. O. Potma, “Fiber delivered probe for efficient CARS imaging of tissues,” Opt. Express 18(3), 2380–2388 (2010).
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S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[CrossRef] [PubMed]

G. Liu, T. Xie, I. V. Tomov, J. Su, L. Yu, J. Zhang, B. J. Tromberg, and Z. Chen, “Rotational multiphoton endoscopy with a 1 microm fiber laser system,” Opt. Lett. 34(15), 2249–2251 (2009).
[CrossRef] [PubMed]

A. Zoumi, X. Lu, G. S. Kassab, and B. J. Tromberg, “Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy,” Biophys. J. 87(4), 2778–2786 (2004).
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A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
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A. M. Seddon, N. Woolf, A. La Ville, R. M. Pittilo, P. M. Rowles, P. R. Turner, and B. Lewis, “Hereditary hyperlipidemia and atherosclerosis in the rabbit due to overproduction of lipoproteins. II. Preliminary report of arterial pathology,” Arteriosclerosis 7(2), 113–124 (1987).
[PubMed]

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T. J. Römer, J. F. Brennan, G. J. Puppels, A. H. Zwinderman, S. G. van Duinen, A. van der Laarse, A. F. van der Steen, N. A. Bom, and A. V. Bruschke, “Intravascular ultrasound combined with Raman spectroscopy to localize and quantify cholesterol and calcium salts in atherosclerotic coronary arteries,” Arterioscler. Thromb. Vasc. Biol. 20(2), 478–483 (2000).
[PubMed]

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T. J. Römer, J. F. Brennan, G. J. Puppels, A. H. Zwinderman, S. G. van Duinen, A. van der Laarse, A. F. van der Steen, N. A. Bom, and A. V. Bruschke, “Intravascular ultrasound combined with Raman spectroscopy to localize and quantify cholesterol and calcium salts in atherosclerotic coronary arteries,” Arterioscler. Thromb. Vasc. Biol. 20(2), 478–483 (2000).
[PubMed]

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T. J. Römer, J. F. Brennan, G. J. Puppels, A. H. Zwinderman, S. G. van Duinen, A. van der Laarse, A. F. van der Steen, N. A. Bom, and A. V. Bruschke, “Intravascular ultrasound combined with Raman spectroscopy to localize and quantify cholesterol and calcium salts in atherosclerotic coronary arteries,” Arterioscler. Thromb. Vasc. Biol. 20(2), 478–483 (2000).
[PubMed]

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[CrossRef] [PubMed]

Wagner, W. D.

H. C. Stary, A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull, M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, and R. W. Wissler, “A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association,” Circulation 92(5), 1355–1374 (1995).
[PubMed]

Wang, H.-W.

H.-W. Wang, I. M. Langohr, M. Sturek, and J.-X. Cheng, “Imaging and quantitative analysis of atherosclerotic lesions by CARS-based multimodal nonlinear optical microscopy,” Arterioscler. Thromb. Vasc. Biol. 29(9), 1342–1348 (2009).
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H.-W. Wang, T. T. Le, and J.-X. Cheng, “Label-free imaging of arterial cells and extracellular matrix using a multimodal CARS microscope,” Opt. Commun. 281(7), 1813–1822 (2008).
[CrossRef] [PubMed]

Wang, Y.

J. Sun, Z. Zhang, B. Lu, W. Yu, Y. Yang, Y. Zhou, Y. Wang, and Z. Fan, “Identification and quantification of coronary atherosclerotic plaques: a comparison of 64-MDCT and intravascular ultrasound,” AJR Am. J. Roentgenol. 190(3), 748–754 (2008).
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Watanabe, Y.

L. M. Buja, T. Kita, J. L. Goldstein, Y. Watanabe, and M. S. Brown, “Cellular pathology of progressive atherosclerosis in the WHHL rabbit. An animal model of familial hypercholesterolemia,” Arteriosclerosis 3(1), 87–101 (1983).
[PubMed]

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R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
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W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
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Whittaker, P.

P. Whittaker, R. A. Kloner, D. R. Boughner, and J. G. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
[CrossRef] [PubMed]

Williams, R. M.

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

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H. C. Stary, A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull, M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, and R. W. Wissler, “A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association,” Circulation 92(5), 1355–1374 (1995).
[PubMed]

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D. A. Bluemke, S. Achenbach, M. Budoff, T. C. Gerber, B. Gersh, L. D. Hillis, W. G. Hundley, W. J. Manning, B. F. Printz, M. Stuber, and P. K. Woodard, “Noninvasive coronary artery imaging: magnetic resonance angiography and multidetector computed tomography angiography: a scientific statement from the american heart association committee on cardiovascular imaging and intervention of the council on cardiovascular radiology and intervention, and the councils on clinical cardiology and cardiovascular disease in the young,” Circulation 118(5), 586–606 (2008).
[CrossRef] [PubMed]

Woolf, N.

A. M. Seddon, N. Woolf, A. La Ville, R. M. Pittilo, P. M. Rowles, P. R. Turner, and B. Lewis, “Hereditary hyperlipidemia and atherosclerosis in the rabbit due to overproduction of lipoproteins. II. Preliminary report of arterial pathology,” Arteriosclerosis 7(2), 113–124 (1987).
[PubMed]

Wright, G. A.

B. K. Courtney, N. R. Munce, K. J. Anderson, A. S. Thind, G. Leung, P. E. Radau, F. S. Foster, I. A. Vitkin, R. S. Schwartz, A. J. Dick, G. A. Wright, and B. H. Strauss, “Innovations in imaging for chronic total occlusions: a glimpse into the future of angiography’s blind-spot,” Eur. Heart J. 29(5), 583–593 (2008).
[CrossRef] [PubMed]

Wu, Y.-M.

Y.-M. Wu, H.-C. Chen, W.-T. Chang, J.-W. Jhan, H.-L. Lin, and I. Liau, “Quantitative assessment of hepatic fat of intact liver tissues with coherent anti-stokes Raman scattering microscopy,” Anal. Chem. 81(4), 1496–1504 (2009).
[CrossRef] [PubMed]

Xie, T.

S. Tang, W. Jung, D. McCormick, T. Xie, J. Su, Y. C. Ahn, B. J. Tromberg, and Z. Chen, “Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning,” J. Biomed. Opt. 14(3), 034005 (2009).
[CrossRef] [PubMed]

G. Liu, T. Xie, I. V. Tomov, J. Su, L. Yu, J. Zhang, B. J. Tromberg, and Z. Chen, “Rotational multiphoton endoscopy with a 1 microm fiber laser system,” Opt. Lett. 34(15), 2249–2251 (2009).
[CrossRef] [PubMed]

Xie, X. S.

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, C. P. Lin, and X. S. Xie, “Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(46), 16807–16812 (2005).
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J.-X. Cheng and X. S. Xie, “Coherent Anti-Stokes Raman Scattering Microscopy: Instrumentation, Theory, and Applications,” J. Phys. Chem. B 108(3), 827–840 (2004).
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X. Nan, J.-X. Cheng, and X. S. Xie, “Vibrational imaging of lipid droplets in live fibroblast cells with coherent anti-Stokes Raman scattering microscopy,” J. Lipid Res. 44(11), 2202–2208 (2003).
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M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Correlation of vulnerable coronary plaques to sudden cardiac events. Lessons from a myocardial infarction-prone animal model (the WHHLMI rabbit),” J. Atheroscler. Thromb. 11(4), 184–189 (2004).
[PubMed]

M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Development of an animal model for spontaneous myocardial infarction (WHHLMI rabbit),” Arterioscler. Thromb. Vasc. Biol. 23(7), 1239–1244 (2003).
[CrossRef] [PubMed]

Yang, Y.

J. Sun, Z. Zhang, B. Lu, W. Yu, Y. Yang, Y. Zhou, Y. Wang, and Z. Fan, “Identification and quantification of coronary atherosclerotic plaques: a comparison of 64-MDCT and intravascular ultrasound,” AJR Am. J. Roentgenol. 190(3), 748–754 (2008).
[CrossRef] [PubMed]

Yeh, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

Yock, P. G.

P. G. Yock and P. J. Fitzgerald, “Optimal Directional Coronary Atherectomy Final Results of the Optimal Atherectomy Restenosis Study (OARS),” Am. J. Cardiol. 81, 27E–32E (1998).
[PubMed]

Yu, L.

Yu, W.

J. Sun, Z. Zhang, B. Lu, W. Yu, Y. Yang, Y. Zhou, Y. Wang, and Z. Fan, “Identification and quantification of coronary atherosclerotic plaques: a comparison of 64-MDCT and intravascular ultrasound,” AJR Am. J. Roentgenol. 190(3), 748–754 (2008).
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Zângaro, R. A.

G. V. Nogueira, L. Silveira, A. A. Martin, R. A. Zângaro, M. T. Pacheco, M. C. Chavantes, and C. A. Pasqualucci, “Raman spectroscopy study of atherosclerosis in human carotid artery,” J. Biomed. Opt. 10(3), 031117 (2005).
[CrossRef] [PubMed]

Zhang, J.

Zhang, Z.

J. Sun, Z. Zhang, B. Lu, W. Yu, Y. Yang, Y. Zhou, Y. Wang, and Z. Fan, “Identification and quantification of coronary atherosclerotic plaques: a comparison of 64-MDCT and intravascular ultrasound,” AJR Am. J. Roentgenol. 190(3), 748–754 (2008).
[CrossRef] [PubMed]

Zhou, Y.

J. Sun, Z. Zhang, B. Lu, W. Yu, Y. Yang, Y. Zhou, Y. Wang, and Z. Fan, “Identification and quantification of coronary atherosclerotic plaques: a comparison of 64-MDCT and intravascular ultrasound,” AJR Am. J. Roentgenol. 190(3), 748–754 (2008).
[CrossRef] [PubMed]

Zipfel, W. R.

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Zoumi, A.

A. Zoumi, X. Lu, G. S. Kassab, and B. J. Tromberg, “Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy,” Biophys. J. 87(4), 2778–2786 (2004).
[CrossRef] [PubMed]

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

Zwinderman, A. H.

T. J. Römer, J. F. Brennan, G. J. Puppels, A. H. Zwinderman, S. G. van Duinen, A. van der Laarse, A. F. van der Steen, N. A. Bom, and A. V. Bruschke, “Intravascular ultrasound combined with Raman spectroscopy to localize and quantify cholesterol and calcium salts in atherosclerotic coronary arteries,” Arterioscler. Thromb. Vasc. Biol. 20(2), 478–483 (2000).
[PubMed]

AJR Am. J. Roentgenol.

J. Sun, Z. Zhang, B. Lu, W. Yu, Y. Yang, Y. Zhou, Y. Wang, and Z. Fan, “Identification and quantification of coronary atherosclerotic plaques: a comparison of 64-MDCT and intravascular ultrasound,” AJR Am. J. Roentgenol. 190(3), 748–754 (2008).
[CrossRef] [PubMed]

Am. J. Cardiol.

P. Libby, “Atherosclerosis: disease biology affecting the coronary vasculature,” Am. J. Cardiol. 98(12), S3–S9 (2006).
[CrossRef] [PubMed]

P. G. Yock and P. J. Fitzgerald, “Optimal Directional Coronary Atherectomy Final Results of the Optimal Atherectomy Restenosis Study (OARS),” Am. J. Cardiol. 81, 27E–32E (1998).
[PubMed]

Anal. Chem.

Y.-M. Wu, H.-C. Chen, W.-T. Chang, J.-W. Jhan, H.-L. Lin, and I. Liau, “Quantitative assessment of hepatic fat of intact liver tissues with coherent anti-stokes Raman scattering microscopy,” Anal. Chem. 81(4), 1496–1504 (2009).
[CrossRef] [PubMed]

Appl. Opt.

Arterioscler. Thromb. Vasc. Biol.

M. Shiomi, T. Ito, S. Yamada, S. Kawashima, and J. Fan, “Development of an animal model for spontaneous myocardial infarction (WHHLMI rabbit),” Arterioscler. Thromb. Vasc. Biol. 23(7), 1239–1244 (2003).
[CrossRef] [PubMed]

T. J. Römer, J. F. Brennan, G. J. Puppels, A. H. Zwinderman, S. G. van Duinen, A. van der Laarse, A. F. van der Steen, N. A. Bom, and A. V. Bruschke, “Intravascular ultrasound combined with Raman spectroscopy to localize and quantify cholesterol and calcium salts in atherosclerotic coronary arteries,” Arterioscler. Thromb. Vasc. Biol. 20(2), 478–483 (2000).
[PubMed]

H.-W. Wang, I. M. Langohr, M. Sturek, and J.-X. Cheng, “Imaging and quantitative analysis of atherosclerotic lesions by CARS-based multimodal nonlinear optical microscopy,” Arterioscler. Thromb. Vasc. Biol. 29(9), 1342–1348 (2009).
[CrossRef] [PubMed]

Arteriosclerosis

L. M. Buja, T. Kita, J. L. Goldstein, Y. Watanabe, and M. S. Brown, “Cellular pathology of progressive atherosclerosis in the WHHL rabbit. An animal model of familial hypercholesterolemia,” Arteriosclerosis 3(1), 87–101 (1983).
[PubMed]

A. M. Seddon, N. Woolf, A. La Ville, R. M. Pittilo, P. M. Rowles, P. R. Turner, and B. Lewis, “Hereditary hyperlipidemia and atherosclerosis in the rabbit due to overproduction of lipoproteins. II. Preliminary report of arterial pathology,” Arteriosclerosis 7(2), 113–124 (1987).
[PubMed]

Basic Res. Cardiol.

P. Whittaker, R. A. Kloner, D. R. Boughner, and J. G. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
[CrossRef] [PubMed]

Biomed. Eng. Online

T. A. Pologruto, B. L. Sabatini, and K. Svoboda, “ScanImage: flexible software for operating laser scanning microscopes,” Biomed. Eng. Online 2(1), 13 (2003).
[CrossRef] [PubMed]

Biophys. J.

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

A. Zoumi, X. Lu, G. S. Kassab, and B. J. Tromberg, “Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy,” Biophys. J. 87(4), 2778–2786 (2004).
[CrossRef] [PubMed]

Circulation

D. A. Bluemke, S. Achenbach, M. Budoff, T. C. Gerber, B. Gersh, L. D. Hillis, W. G. Hundley, W. J. Manning, B. F. Printz, M. Stuber, and P. K. Woodard, “Noninvasive coronary artery imaging: magnetic resonance angiography and multidetector computed tomography angiography: a scientific statement from the american heart association committee on cardiovascular imaging and intervention of the council on cardiovascular radiology and intervention, and the councils on clinical cardiology and cardiovascular disease in the young,” Circulation 118(5), 586–606 (2008).
[CrossRef] [PubMed]

Y. Honda and P. J. Fitzgerald, “Frontiers in intravascular imaging technologies,” Circulation 117(15), 2024–2037 (2008).
[CrossRef] [PubMed]

I. K. Jang, G. J. Tearney, B. MacNeill, M. Takano, F. Moselewski, N. Iftima, M. Shishkov, S. Houser, H. T. Aretz, E. F. Halpern, and B. E. Bouma, “In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography,” Circulation 111(12), 1551–1555 (2005).
[CrossRef] [PubMed]

H. C. Stary, A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull, M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, and R. W. Wissler, “A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association,” Circulation 92(5), 1355–1374 (1995).
[PubMed]

Eur. Heart J.

B. K. Courtney, N. R. Munce, K. J. Anderson, A. S. Thind, G. Leung, P. E. Radau, F. S. Foster, I. A. Vitkin, R. S. Schwartz, A. J. Dick, G. A. Wright, and B. H. Strauss, “Innovations in imaging for chronic total occlusions: a glimpse into the future of angiography’s blind-spot,” Eur. Heart J. 29(5), 583–593 (2008).
[CrossRef] [PubMed]

P. Barlis, P. W. Serruys, A. Devries, and E. Regar, “Optical coherence tomography assessment of vulnerable plaque rupture: predilection for the plaque ‘shoulder’,” Eur. Heart J. 29(16), 2023 (2008).
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EuroIntervention

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J. M. Hodgson, K. G. Reddy, R. Suneja, R. N. Nair, E. J. Lesnefsky, and H. M. Sheehan, “Intracoronary ultrasound imaging: correlation of plaque morphology with angiography, clinical syndrome and procedural results in patients undergoing coronary angioplasty,” J. Am. Coll. Cardiol. 21(1), 35–44 (1993).
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Figures (10)

Fig. 1
Fig. 1

Schematic of the home-built multimodal nonlinear optical laser scanning microscope. Light source for TPEF and SHG imaging is a Ti:Sapphire femto-second oscillator (Tsunami,Spectra-Physics). For CARS imaging, Stokes pulses are generated in PCF which is pumped by the same Ti:sapphire laser. Inset shows a typical video image of a tissue sample with lumen surface facing up. F-ISO: Faraday isolator; CM: chirp laser mirrors; BS: beam splitter; NIR-F: near-IR filter;; GS: galvo scanner; DM: dichroic mirror; OBJ: objective lens; BF: bandpass filter; NDF: neutral density filter; λ/2: half waveplate.

Fig. 2
Fig. 2

Comparison of (A) H&E (B) picro-sirius red (C) oil red O histological stain with (D) label-free multimodal CARS image of adjacent artery cross-sections. Color-codes shown in (D): green is TPEF representing mainly elastin, blue is SHG representing mainly collagen fibrils and red is CARS representing mainly lipids content. Both SHG and CARS signals are collected in the forward-direction while TPEF is collected in the backscattered (epi-) direction.

Fig. 3
Fig. 3

Representative multimodal epi-NLO image acquired from smooth/healthy luminal surface of the WHHLMI rabbit artery, that is (A) 4 months-old, (C) 16 months-old, (E) 18 months-old, (G) 24 months-old, and atherosclerotic plaques found on the WHHLMI rabbit arteries at (B) 4 months-old, (D) 16 months-old, (F) 18 months-old, and (H) 24 months-old. (20x air objective lens, 0.75 NA).

Fig. 4
Fig. 4

Comparison of the SS scores extracted from SHG, CARS and TPEF images acquired from the arterial lumen of four WHHLMI rabbits: 4 months-old, 16 months-old, 18 months-old and 24 months-old.

Fig. 5
Fig. 5

Representative multimodal epi-NLO image acquired from the luminal surface of WHHLMI rabbit arteries, with (A) -(C) healthy lumen; (D) early atherosclerotic plaque found in young rabbit; (E) atherosclerotic plaque (with dense collagen fibers shown blue); (F) atherosclerotic plaque with higher lipid content shown red; (G) atherosclerotic plaque containing collagen fibers and lipids, and (H) very advanced plaque (20x air objective lens, 0.75 NA).

Fig. 6
Fig. 6

Average SS scores extracted from SHG (blue squares), CARS (red circles) and TPEF (green triangles) images acquired from the arterial lumen of WHHLMI rabbits. Images A-H correspond to those shown in Fig. 5

Fig. 7
Fig. 7

Mean OIPB indexes of healthy and atherosclerotic lumen surfaces as a function of rabbits’ age.

Fig. 8
Fig. 8

Mean OIPB indexes of all regions of arterial lumen as a function of rabbits’ age.

Fig. 9
Fig. 9

OIPB indices of all images shown in Fig. 5. OIPB index is a better discriminatory parameter in differentiating plaque burden.

Fig. 10
Fig. 10

Representative epi-NLO images obtained from the luminal surface of thoracic aorta of rabbits sacrificed at (A), (B) and (C) 4 months (D) 16 months (E) 17 months and (F) 24 months of age. Images were collected using 20x air objective lens. These are the sum images of 5 consecutive image planes taken at 2 µm steps from 20µm to 30µm beneath the luminal surface. Green is TPEF signal representing elastin fiber and other endogenous fluorescent molecules; Blue is SHG signal representing fibrillar collagen; Red is CARS signal representing lipids-rich structures in plaque.

Equations (1)

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O I P B = S S S H G + S S C A R S + d ( S S S H G , S S T P E F ) + d ( S S C A R S , S S T P E F ) + d ( S S C A R S , S S S H G )

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