Abstract

Multiphoton microscopy using laser sources in the mid-infrared range (MIR, 1,300 nm and 1,700 nm) was used to image atherosclerotic plaques from murine and human samples. Third harmonic generation (THG) from atherosclerotic plaques revealed morphological details of cellular and extracellular lipid deposits. Simultaneous nonlinear optical signals from the same laser source, including second harmonic generation and endogenous fluorescence, resulted in label-free images of various layers within the diseased vessel wall. The THG signal adds an endogenous contrast mechanism with a practical degree of specificity for atherosclerotic plaques that complements current nonlinear optical methods for the investigation of cardiovascular disease. Our use of whole-mount tissue and backward scattered epi-detection suggests THG could potentially be used in the future as a clinical tool.

© 2017 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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  77. D. Sinefeld, H. P. Paudel, D. G. Ouzounov, T. G. Bifano, and C. Xu, “Adaptive optics in multiphoton microscopy: comparison of two, three and four photon fluorescence,” Opt. Express 23(24), 31472–31483 (2015).
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  78. N. Ji, “Adaptive optical fluorescence microscopy,” Nat. Methods 14(4), 374–380 (2017).
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  79. S. H. Chia, C. H. Yu, C. H. Lin, N. C. Cheng, T. M. Liu, M. C. Chan, I. H. Chen, and C. K. Sun, “Miniaturized video-rate epi-third-harmonic-generation fiber-microscope,” Opt. Express 18(16), 17382–17391 (2010).
    [Crossref] [PubMed]
  80. C. L. Hoy, O. Ferhanoğlu, M. Yildirim, W. Piyawattanametha, H. Ra, O. Solgaard, and A. Ben-Yakar, “Optical design and imaging performance testing of a 9.6-mm diameter femtosecond laser microsurgery probe,” Opt. Express 19(11), 10536–10552 (2011).
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  81. D. M. Huland, K. Charan, D. G. Ouzounov, J. S. Jones, N. Nishimura, and C. Xu, “Three-photon excited fluorescence imaging of unstained tissue using a GRIN lens endoscope,” Biomed. Opt. Express 4(5), 652–658 (2013).
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  82. C. M. Brown, D. R. Rivera, I. Pavlova, D. G. Ouzounov, W. O. Williams, S. Mohanan, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using a compact and flexible multiphoton microendoscope,” J. Biomed. Opt. 17(4), 040505 (2012).
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2017 (3)

R. F. Barth, D. A. Kellough, P. Allenby, L. E. Blower, S. H. Hammond, G. M. Allenby, and L. M. Buja, “Assessment of atherosclerotic luminal narrowing of coronary arteries based on morphometrically generated visual guides,” Cardiovasc. Pathol. 29, 53–60 (2017).
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D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y. T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
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N. Ji, “Adaptive optical fluorescence microscopy,” Nat. Methods 14(4), 374–380 (2017).
[Crossref] [PubMed]

2016 (7)

E. V. Gubarkova, V. V. Dudenkova, F. I. Feldchtein, L. B. Timofeeva, E. B. Kiseleva, S. S. Kuznetsov, B. E. Shakhov, A. A. Moiseev, V. M. Gelikonov, G. V. Gelikonov, A. Vitkin, and N. D. Gladkova, “Multi-modal optical imaging characterization of atherosclerotic plaques,” J. Biophotonics 9(10), 1009–1020 (2016).
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M. Seeger, A. Karlas, D. Soliman, J. Pelisek, and V. Ntziachristos, “Multimodal optoacoustic and multiphoton microscopy of human carotid atheroma,” Photoacoustics 4(3), 102–111 (2016).
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Š. Lhoták, G. Gyulay, J. C. Cutz, A. Al-Hashimi, B. L. Trigatti, C. D. Richards, S. A. Igdoura, G. R. Steinberg, J. Bramson, K. Ask, and R. C. Austin, “Characterization of proliferating lesion-resident cells during all stages of atherosclerotic growth,” J. Am. Heart Assoc. 5(8), e003945 (2016).
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H. N. Hutson, T. Marohl, M. Anderson, K. Eliceiri, P. Campagnola, and K. S. Masters, “Calcific aortic valve disease is associated with layer-specific alterations in collagen architecture,” PLoS One 11(9), e0163858 (2016).
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G. J. Ughi, H. Wang, E. Gerbaud, J. A. Gardecki, A. M. Fard, E. Hamidi, P. Vacas-Jacques, M. Rosenberg, F. A. Jaffer, and G. J. Tearney, “Clinical characterization of coronary atherosclerosis with dual-modality OCT and near-infrared autofluorescence imaging,” JACC Cardiovasc. Imaging 9(11), 1304–1314 (2016).
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R. Turcotte, D. J. Rutledge, E. Bélanger, D. Dill, W. B. Macklin, and D. C. Côté, “Intravital assessment of myelin molecular order with polarimetric multiphoton microscopy,” Sci. Rep. 6(1), 31685 (2016).
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S. Dochow, H. Fatakdawala, J. E. Phipps, D. Ma, T. Bocklitz, M. Schmitt, J. W. Bishop, K. B. Margulies, L. Marcu, and J. Popp, “Comparing Raman and fluorescence lifetime spectroscopy from human atherosclerotic lesions using a bimodal probe,” J. Biophotonics 9(9), 958–966 (2016).
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2015 (10)

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).
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H. Fatakdawala, D. Gorpas, J. W. Bishop, J. Bec, D. Ma, J. A. Southard, K. B. Margulies, and L. Marcu, “Fluorescence lifetime imaging combined with conventional intravascular ultrasound for enhanced assessment of atherosclerotic plaques: an ex vivo study in human coronary arteries,” J. Cardiovasc. Transl. Res. 8(4), 253–263 (2015).
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T. Wang, A. McElroy, D. Halaney, D. Vela, E. Fung, S. Hossain, J. Phipps, B. Wang, B. Yin, M. D. Feldman, and T. E. Milner, “Detection of plaque structure and composition using OCT combined with two-photon luminescence (TPL) imaging,” Lasers Surg. Med. 47(6), 485–494 (2015).
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T. Wang, A. McElroy, D. Halaney, D. Vela, E. Fung, S. Hossain, J. Phipps, B. Wang, B. Yin, M. D. Feldman, and T. E. Milner, “Dual-modality fiber-based OCT-TPL imaging system for simultaneous microstructural and molecular analysis of atherosclerotic plaques,” Biomed. Opt. Express 6(5), 1665–1678 (2015).
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L. M. Zadrozny, E. B. Neufeld, B. M. Lucotte, P. S. Connelly, Z. X. Yu, L. Dao, L. Y. Hsu, and R. S. Balaban, “Study of the development of the mouse thoracic aorta three-dimensional macromolecular structure using two-photon microscopy,” J. Histochem. Cytochem. 63(1), 8–21 (2015).
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N. G. Horton and C. Xu, “Dispersion compensation in three-photon fluorescence microscopy at 1,700 nm,” Biomed. Opt. Express 6(4), 1392–1397 (2015).
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J. Wang, C. Sun, N. Gerdes, C. Liu, M. Liao, J. Liu, M. A. Shi, A. He, Y. Zhou, G. K. Sukhova, H. Chen, X. W. Cheng, M. Kuzuya, T. Murohara, J. Zhang, X. Cheng, M. Jiang, G. E. Shull, S. Rogers, C. L. Yang, Q. Ke, S. Jelen, R. Bindels, D. H. Ellison, P. Jarolim, P. Libby, and G. P. Shi, “Interleukin 18 function in atherosclerosis is mediated by the interleukin 18 receptor and the Na-Cl co-transporter,” Nat. Med. 21(7), 820–826 (2015).
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Y. C. Chen, H. C. Hsu, C. M. Lee, and C. K. Sun, “Third-harmonic generation susceptibility spectroscopy in free fatty acids,” J. Biomed. Opt. 20(9), 095013 (2015).
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D. Mozaffarian, E. J. Benjamin, A. S. Go, D. K. Arnett, M. J. Blaha, M. Cushman, S. de Ferranti, J. P. Després, H. J. Fullerton, V. J. Howard, M. D. Huffman, S. E. Judd, B. M. Kissela, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, S. Liu, R. H. Mackey, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, P. Muntner, M. E. Mussolino, K. Nasir, R. W. Neumar, G. Nichol, L. Palaniappan, D. K. Pandey, M. J. Reeves, C. J. Rodriguez, P. D. Sorlie, J. Stein, A. Towfighi, T. N. Turan, S. S. Virani, J. Z. Willey, D. Woo, R. W. Yeh, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2015 update: a report from the American Heart Association,” Circulation 131(4), e29–e322 (2015).
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D. Sinefeld, H. P. Paudel, D. G. Ouzounov, T. G. Bifano, and C. Xu, “Adaptive optics in multiphoton microscopy: comparison of two, three and four photon fluorescence,” Opt. Express 23(24), 31472–31483 (2015).
[Crossref] [PubMed]

2014 (6)

D. D. Adraktas, E. Tong, A. D. Furtado, S. C. Cheng, and M. Wintermark, “Evolution of CT imaging features of carotid atherosclerotic plaques in a 1-year prospective cohort study,” J. Neuroimaging 24(1), 1–6 (2014).
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M. A. Latif and M. J. Budoff, “Role of CT angiography for detection of coronary atherosclerosis,” Expert Rev. Cardiovasc. Ther. 12(3), 373–382 (2014).
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G. Bautista, S. G. Pfisterer, M. J. Huttunen, S. Ranjan, K. Kanerva, E. Ikonen, and M. Kauranen, “Polarized THG microscopy identifies compositionally different lipid droplets in mammalian cells,” Biophys. J. 107(10), 2230–2236 (2014).
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D. M. Small, W. Y. Sanchez, S. Roy, M. J. Hickey, and G. C. Gobe, “Multiphoton fluorescence microscopy of the live kidney in health and disease,” J. Biomed. Opt. 19(2), 020901 (2014).
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A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
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R. Chèvre, J. M. González-Granado, R. T. Megens, V. Sreeramkumar, C. Silvestre-Roig, P. Molina-Sánchez, C. Weber, O. Soehnlein, A. Hidalgo, and V. Andrés, “High-resolution imaging of intravascular atherogenic inflammation in live mice,” Circ. Res. 114(5), 770–779 (2014).
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2013 (10)

Z. Wu, A. Curaj, S. Fokong, E. A. Liehn, C. Weber, T. Lammers, F. Kiessling, and M. Zandvoort van, “Rhodamine-loaded intercellular adhesion molecule-1-targeted microbubbles for dual-modality imaging under controlled shear stresses,” Circ Cardiovasc Imaging 6(6), 974–981 (2013).
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T. Wang, D. Halaney, D. Ho, M. D. Feldman, and T. E. Milner, “Two-photon luminescence properties of gold nanorods,” Biomed. Opt. Express 4(4), 584–595 (2013).
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I. Perrotta, “Ultrastructural features of human atherosclerosis,” Ultrastruct. Pathol. 37(1), 43–51 (2013).
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I. A. Sobenin, M. A. Sazonova, A. Y. Postnov, Y. V. Bobryshev, and A. N. Orekhov, “Changes of mitochondria in atherosclerosis: possible determinant in the pathogenesis of the disease,” Atherosclerosis 227(2), 283–288 (2013).
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A. Thomassen, H. Petersen, A. C. Diederichsen, H. Mickley, L. O. Jensen, A. Johansen, O. Gerke, P. E. Braad, P. Thayssen, M. M. Høilund-Carlsen, W. Vach, J. Knuuti, and P. F. Høilund-Carlsen, “Hybrid CT angiography and quantitative 15O-water PET for assessment of coronary artery disease: comparison with quantitative coronary angiography,” Eur. J. Nucl. Med. Mol. Imaging 40(12), 1894–1904 (2013).
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K. W. Moon, J. H. Kim, K. D. Yoo, S. S. Oh, D. B. Kim, and C. M. Kim, “Evaluation of radial artery atherosclerosis by intravascular ultrasound,” Angiology 64(1), 73–79 (2013).
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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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T. Meyer, M. Chemnitz, M. Baumgartl, T. Gottschall, T. Pascher, C. Matthäus, B. F. Romeike, B. R. Brehm, J. Limpert, A. Tünnermann, M. Schmitt, B. Dietzek, and J. Popp, “Expanding multimodal microscopy by high spectral resolution coherent anti-Stokes Raman scattering imaging for clinical disease diagnostics,” Anal. Chem. 85(14), 6703–6715 (2013).
[Crossref] [PubMed]

C. Xu and F. W. Wise, “Recent Advances in Fiber Lasers for Nonlinear Microscopy,” Nat. Photonics 7(12), 1006 (2013).
[Crossref] [PubMed]

D. M. Huland, K. Charan, D. G. Ouzounov, J. S. Jones, N. Nishimura, and C. Xu, “Three-photon excited fluorescence imaging of unstained tissue using a GRIN lens endoscope,” Biomed. Opt. Express 4(5), 652–658 (2013).
[Crossref] [PubMed]

2012 (3)

C. M. Brown, D. R. Rivera, I. Pavlova, D. G. Ouzounov, W. O. Williams, S. Mohanan, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using a compact and flexible multiphoton microendoscope,” J. Biomed. Opt. 17(4), 040505 (2012).
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T. Wang, J. J. Mancuso, S. M. Kazmi, J. Dwelle, V. Sapozhnikova, B. Willsey, L. L. Ma, J. Qiu, X. Li, A. K. Dunn, K. P. Johnston, M. D. Feldman, and T. E. Milner, “Combined two-photon luminescence microscopy and OCT for macrophage detection in the hypercholesterolemic rabbit aorta using plasmonic gold nanorose,” Lasers Surg. Med. 44(1), 49–59 (2012).
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J. L. Suhalim, C. Y. Chung, M. B. Lilledahl, R. S. Lim, M. Levi, B. J. Tromberg, and E. O. Potma, “Characterization of cholesterol crystals in atherosclerotic plaques using stimulated Raman scattering and second-harmonic generation microscopy,” Biophys. J. 102(8), 1988–1995 (2012).
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2011 (5)

G. van Soest, E. Regar, T. P. Goderie, N. Gonzalo, S. Koljenović, G. J. van Leenders, P. W. Serruys, and A. F. van der Steen, “Pitfalls in plaque characterization by OCT: image artifacts in native coronary arteries,” JACC Cardiovasc. Imaging 4(7), 810–813 (2011).
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R. Corti and V. Fuster, “Imaging of atherosclerosis: magnetic resonance imaging,” Eur. Heart J. 32(14), 1709–1719 (2011).
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M. J. Farrar, F. W. Wise, J. R. Fetcho, and C. B. Schaffer, “In vivo imaging of myelin in the vertebrate central nervous system using third harmonic generation microscopy,” Biophys. J. 100(5), 1362–1371 (2011).
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D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
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C. L. Hoy, O. Ferhanoğlu, M. Yildirim, W. Piyawattanametha, H. Ra, O. Solgaard, and A. Ben-Yakar, “Optical design and imaging performance testing of a 9.6-mm diameter femtosecond laser microsurgery probe,” Opt. Express 19(11), 10536–10552 (2011).
[Crossref] [PubMed]

2010 (2)

S. H. Chia, C. H. Yu, C. H. Lin, N. C. Cheng, T. M. Liu, M. C. Chan, I. H. Chen, and C. K. Sun, “Miniaturized video-rate epi-third-harmonic-generation fiber-microscope,” Opt. Express 18(16), 17382–17391 (2010).
[Crossref] [PubMed]

R. S. Lim, A. Kratzer, N. P. Barry, S. Miyazaki-Anzai, M. Miyazaki, W. W. Mantulin, M. Levi, E. O. Potma, and B. J. Tromberg, “Multimodal CARS microscopy determination of the impact of diet on macrophage infiltration and lipid accumulation on plaque formation in ApoE-deficient mice,” J. Lipid Res. 51(7), 1729–1737 (2010).
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2009 (4)

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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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).
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R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, and J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
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H. G. Bezerra, M. A. Costa, G. Guagliumi, A. M. Rollins, and D. I. Simon, “Intracoronary optical coherence tomography: a comprehensive review clinical and research applications,” JACC Cardiovasc. Interv. 2(11), 1035–1046 (2009).
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2008 (1)

A. Tanaka, T. Imanishi, H. Kitabata, T. Kubo, S. Takarada, H. Kataiwa, A. Kuroi, H. Tsujioka, T. Tanimoto, N. Nakamura, M. Mizukoshi, K. Hirata, and T. Akasaka, “Distribution and frequency of thin-capped fibroatheromas and ruptured plaques in the entire culprit coronary artery in patients with acute coronary syndrome as determined by optical coherence tomography,” Am. J. Cardiol. 102(8), 975–979 (2008).
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2007 (7)

D. Böse, C. von Birgelen, and R. Erbel, “Intravascular ultrasound for the evaluation of therapies targeting coronary atherosclerosis,” J. Am. Coll. Cardiol. 49(9), 925–932 (2007).
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N. Nishimura, C. B. Schaffer, B. Friedman, P. D. Lyden, and D. Kleinfeld, “Penetrating arterioles are a bottleneck in the perfusion of neocortex,” Proc. Natl. Acad. Sci. U.S.A. 104(1), 365–370 (2007).
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C. Auffray, D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. Cumano, G. Lauvau, and F. Geissmann, “Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior,” Science 317(5838), 666–670 (2007).
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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).
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Y. Nakashima, H. Fujii, S. Sumiyoshi, T. N. Wight, and K. Sueishi, “Early human atherosclerosis: accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration,” Arterioscler. Thromb. Vasc. Biol. 27(5), 1159–1165 (2007).
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W. Yu, J. C. Braz, A. M. Dutton, P. Prusakov, and M. Rekhter, “In vivo imaging of atherosclerotic plaques in apolipoprotein E deficient mice using nonlinear microscopy,” J. Biomed. Opt. 12(5), 054008 (2007).
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D. A. Tulis, “Histological and morphometric analyses for rat carotid balloon injury model,” Methods Mol. Med. 139, 31–66 (2007).
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2006 (3)

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).
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D. Débarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, “Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy,” Nat. Methods 3(1), 47–53 (2006).
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N. Nishimura, C. B. Schaffer, B. Friedman, P. S. Tsai, P. D. Lyden, and D. Kleinfeld, “Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke,” Nat. Methods 3(2), 99–108 (2006).
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2005 (2)

D. Débarre, W. Supatto, and E. Beaurepaire, “Structure sensitivity in third-harmonic generation microscopy,” Opt. Lett. 30(16), 2134–2136 (2005).
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G. K. Hansson, “Inflammation, atherosclerosis, and coronary artery disease,” N. Engl. J. Med. 352(16), 1685–1695 (2005).
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2004 (3)

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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K. S. Meir and E. Leitersdorf, “Atherosclerosis in the apolipoprotein-E-deficient mouse: a decade of progress,” Arterioscler. Thromb. Vasc. Biol. 24(6), 1006–1014 (2004).
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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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2003 (2)

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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2002 (3)

R. B. Singh, S. A. Mengi, Y. J. Xu, A. S. Arneja, and N. S. Dhalla, “Pathogenesis of atherosclerosis: A multifactorial process,” Exp. Clin. Cardiol. 7(1), 40–53 (2002).
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H. Yabushita, B. E. Bouma, S. L. Houser, H. T. Aretz, I. K. Jang, K. H. Schlendorf, C. R. Kauffman, M. Shishkov, D. H. Kang, E. F. Halpern, and G. J. Tearney, “Characterization of human atherosclerosis by optical coherence tomography,” Circulation 106(13), 1640–1645 (2002).
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K. Arakawa, K. Isoda, T. Ito, K. Nakajima, T. Shibuya, and F. Ohsuzu, “Fluorescence analysis of biochemical constituents identifies atherosclerotic plaque with a thin fibrous cap,” Arterioscler. Thromb. Vasc. Biol. 22(6), 1002–1007 (2002).
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2001 (1)

C. Yuan, L. M. Mitsumori, M. S. Ferguson, N. L. Polissar, D. Echelard, G. Ortiz, R. Small, J. W. Davies, W. S. Kerwin, and T. S. Hatsukami, “In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques,” Circulation 104(17), 2051–2056 (2001).
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2000 (3)

Z. A. Fayad, T. Nahar, J. T. Fallon, M. Goldman, J. G. Aguinaldo, J. J. Badimon, M. Shinnar, J. H. Chesebro, and V. Fuster, “In vivo magnetic resonance evaluation of atherosclerotic plaques in the human thoracic aorta: a comparison with transesophageal echocardiography,” Circulation 101(21), 2503–2509 (2000).
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A. J. Lusis, “Atherosclerosis,” Nature 407(6801), 233–241 (2000).
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R. Virmani, F. D. Kolodgie, A. P. Burke, A. Farb, and S. M. Schwartz, “Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions,” Arterioscler. Thromb. Vasc. Biol. 20(5), 1262–1275 (2000).
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1999 (2)

A. Zumbusch, G. R. Holtom, and X. S. Xie, “Three-dimensional vibrational imaging by coherent anti-Stokes Raman scattering,” Phys. Rev. Lett. 82(20), 4142–4145 (1999).
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J. Ge, F. Chirillo, J. Schwedtmann, G. Görge, M. Haude, D. Baumgart, V. Shah, C. von Birgelen, S. Sack, H. Boudoulas, and R. Erbel, “Screening of ruptured plaques in patients with coronary artery disease by intravascular ultrasound,” Heart 81(6), 621–627 (1999).
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1995 (2)

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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Figures (6)

Fig. 1
Fig. 1 Multiphoton microscopy shows vessel wall structures consistent with atherosclerotic lesions in whole-mounted aortas extracted from a murine model of atherosclerosis. (a) Aorta from an apolipoprotein E knockout mouse fed a high fat diet (ApoE−/−-HFD) shown with cross-sectional and enface views (i and ii) through a region with strong emission at the third harmonic generation (THG) wavelengths. Laser excitation was at 1,700 nm, incident on the lumen. (b) Histology with Masson’s trichrome and H&E staining of aorta from an ApoE−/−-HFD mouse. (c) Aorta from a wild type mice fed a normal chow diet (WT-Normal) and cross-sectional and enface views (iii and iv). (d) Histology of aorta from a WT-Normal mouse. Cross-sectional views in a and c are maximum intensity projections through the y-axis. Second harmonic generation (SHG); autofluorescence (AutoF). Scale bars are 50 µm.
Fig. 2
Fig. 2 Correlation between third harmonic generation (THG) and lipid stain. (a) Frozen section (20-µm thickness) of aorta from ApoE−/−-HFD stained for lipids using Nile-Red and imaged using two-photon excited fluorescence (2PEF) at 810 nm excitation. Displayed image shows fluorescence channel for Nile-Red (612–677 nm). (b) Same section imaged with 1,700 nm excitation showing the THG channel detected with 548–573 nm band pass filter. Scale bars are 50 µm.
Fig. 3
Fig. 3 Optical properties of atherosclerotic lesions in mouse aorta. (a and b) 1,300 nm excitation produces signals at third harmonic generation (THG) and second harmonic generation (SHG) wavelengths as well as autofluorescence (AutoF) at an atherosclerotic lesion. Cross-sectional, maximum projected (a) and enface (b) views of ApoE−/−-HFD aorta. Line in a shows location of b. (c) 1,300 nm excitation of a region within ApoE−/−-HFD aorta that has atherosclerotic features, produces a strong signal in the THG emission range (421–445 nm). (d) 1,700 nm excitation of the same region shows the same features in the THG emission range (548–573 nm). Scale bars are 50 µm.
Fig. 4
Fig. 4 Third harmonic generation (THG) microscopy using 1,700 nm excitation reveals varying features of atherosclerotic lesions. (a) WT-Normal and (b) ApoE−/−-HFD mouse aortas shown in cross-sectional projections and enface views, show second harmonic generation (SHG) of the tunica adventitia (a-iii and b-iii), autofluorescence (AutoF) in the media (a-ii and b-ii) and a strong THG signal within the thickened intimal layer of ApoE−/−-HFD (b-i) that is not present in WT-Normal (a-i). Single z-slices through different lesions (c-f) show variability in structures producing THG signal and the association between SHG, THG and AutoF. (c) Large deposit of THG signal 38 µm below lumen. (d) Small punctate regions of THG signal 48 µm below lumen, with SHG positioned in close association with THG (arrows). (e) Image from near the abluminal edge of aorta showing THG and SHG deposits. (f) Plaque near a vessel bifurcation off of the aortic arch. Scale bars are 50 µm.
Fig. 5
Fig. 5 Third harmonic generation (THG) microscopy of human coronary artery. (a) In a healthy coronary artery imaged from the luminal side with 1,300 nm excitation, a cross-sectional projection and enface planes (i and ii) show second harmonic generation (SHG) and broad autofluorescence (AutoF) throughout the intimal layer. (b) An artery sample with coronary artery disease imaged from the luminal side with 1,300 nm. i and ii show images from levels indicated in cross-sectional view. Yellow box shows location of magnified view. (c) Photograph and epi-fluorescence image of sample imaged in (b). Magenta box shows the locations of magnified regions. A small laser burn (red box) was induced during THG microscopy at a measured displacement to the imaged region in (b) indicated with an orange circle to aid in image registration. A 23-gauge needle was used to make a fiduciary mark (arrows). (d) Bright-field image of region imaged with multiphoton microscopy from a section of the tissue with fiduciary mark (black arrow). (e) Higher magnification images from the region imaged with multiphoton microscopy stained with H&E and (f) Masson’s Trichrome. Open, nucleated spaces (arrows) are consistent with lipid deposits. Sections from a sample with no atherosclerosis (healthy) are shown below. (g) Confocal microscopy of immunostaining for CD68 in a section from the same region. Unless otherwise noted, scale bars are 50 µm.
Fig. 6
Fig. 6 Summary of morphological features revealed by third harmonic generation (THG) microscopy. Small lipid deposits accumulate in monocytes of the intima during the initial stages of atherosclerosis and can be detected with THG as punctate regions within the intima. Continual uptake of atherogenic lipids increases the size of cellular lipid deposits leading to the formation of foam cells, that are characterized by a cytoplasm filled with lipids. Extracellular lipid pools develop following the breakdown of cellular components and appear with THG imaging as larger regions. Second harmonic generation (SHG) within extracellular lipid pools are most likely cholesterol crystals. Additional nonlinear optical processes simultaneously provide contrast of components of the medial layer (elastin and smooth muscle) and collagens within the adventitia. Red is THG, green is SHG, and blue is autofluorescence. Scale bars are 50 µm.

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