Abstract

New optical imaging techniques that provide contrast to study both the anatomy and composition of atherosclerotic plaques can be utilized to better understand the formation, progression and clinical complications of human coronary artery disease. We present a dual-modality fiber-based optical imaging system for simultaneous microstructural and molecular analysis of atherosclerotic plaques that combines optical coherence tomography (OCT) and two-photon luminescence (TPL) imaging. Experimental results from ex vivo human coronary arteries show that OCT and TPL optical contrast in recorded OCT-TPL images is complimentary and in agreement with histological analysis. Molecular composition (e.g., lipid and oxidized-LDL) detected by TPL imaging can be overlaid onto plaque microstructure depicted by OCT, providing new opportunities for atherosclerotic plaque identification and characterization.

© 2015 Optical Society of America

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J. E. Phipps, D. Vela, T. Hoyt, D. Halaney, J. J. Mancuso, L. M. Buja, R. Asmis, T. E. Milner, and M. D. Feldman, “Macrophages and intravascular optical coherence tomography bright spots: a quantitative study,” JACC Cardiovasc. Imaging 8(1), 63–72 (2015).
[Crossref] [PubMed]

2014 (4)

A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, M. J. Blaha, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, S. E. Judd, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, R. H. Mackey, D. J. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, R. W. Neumar, G. Nichol, D. K. Pandey, N. P. Paynter, M. J. Reeves, P. D. Sorlie, J. Stein, A. Towfighi, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2014 update: a report from the American Heart Association,” Circulation 129(3), e28–e292 (2014).
[Crossref] [PubMed]

J. Bec, D. M. Ma, D. R. Yankelevich, J. Liu, W. T. Ferrier, J. Southard, and L. Marcu, “Multispectral fluorescence lifetime imaging system for intravascular diagnostics with ultrasound guidance: in vivo validation in swine arteries,” J. Biophotonics 7(5), 281–285 (2014).
[Crossref] [PubMed]

X. Li, J. Li, J. Jing, T. Ma, S. Liang, J. Zhang, D. Mohar, A. Raney, S. Mahon, M. Brenner, P. Patel, K. K. Shung, Q. Zhou, and Z. Chen, “Integrated IVUS-OCT Imaging for Atherosclerotic Plaque Characterization,” IEEE J. Sel. Top. Quantum Electron. 20(2), 7100108 (2014).
[PubMed]

T. Wang, Q. Li, P. Xiao, J. Ahn, Y. E. Kim, Y. Park, M. Kim, M. Song, E. Chung, W. K. Chung, G. O. Ahn, S. Kim, P. Kim, S. J. Myung, and K. H. Kim, “Gradient index lens based combined two-photon microscopy and optical coherence tomography,” Opt. Express 22(11), 12962–12970 (2014).
[Crossref] [PubMed]

2013 (2)

2012 (3)

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).
[Crossref] [PubMed]

T. Wang, J. J. Mancuso, V. Sapozhnikova, J. Dwelle, L. L. Ma, B. Willsey, S. M. Kazmi, J. Qiu, X. Li, R. Asmis, K. P. Johnston, M. D. Feldman, and T. E. Milner, “Dual-wavelength multifrequency photothermal wave imaging combined with optical coherence tomography for macrophage and lipid detection in atherosclerotic plaques using gold nanoparticles,” J. Biomed. Opt. 17(3), 036009 (2012).
[Crossref] [PubMed]

J. Xi, Y. Chen, Y. Zhang, K. Murari, M. J. Li, and X. Li, “Integrated multimodal endomicroscopy platform for simultaneous en face optical coherence and two-photon fluorescence imaging,” Opt. Lett. 37(3), 362–364 (2012).
[Crossref] [PubMed]

2011 (3)

H. Yoo, J. W. Kim, M. Shishkov, E. Namati, T. Morse, R. Shubochkin, J. R. McCarthy, V. Ntziachristos, B. E. Bouma, F. A. Jaffer, and G. J. Tearney, “Intra-arterial catheter for simultaneous microstructural and molecular imaging in vivo,” Nat. Med. 17(12), 1680–1684 (2011).
[Crossref] [PubMed]

M. M. Arnida, M. M. Janát-Amsbury, A. Ray, C. M. Peterson, and H. Ghandehari, “Geometry and surface characteristics of gold nanoparticles influence their biodistribution and uptake by macrophages,” Eur. J. Pharm. Biopharm. 77(3), 417–423 (2011).
[Crossref] [PubMed]

B. Jeong, B. Lee, M. S. Jang, H. Nam, S. J. Yoon, T. Wang, J. Doh, B. G. Yang, M. H. Jang, and K. H. Kim, “Combined two-photon microscopy and optical coherence tomography using individually optimized sources,” Opt. Express 19(14), 13089–13096 (2011).
[PubMed]

2010 (1)

2009 (1)

L. L. Ma, M. D. Feldman, J. M. Tam, A. S. Paranjape, K. K. Cheruku, T. A. Larson, J. O. Tam, D. R. Ingram, V. Paramita, J. W. Villard, J. T. Jenkins, T. Wang, G. D. Clarke, R. Asmis, K. Sokolov, B. Chandrasekar, T. E. Milner, and K. P. Johnston, “Small multifunctional nanoclusters (nanoroses) for targeted cellular imaging and therapy,” ACS Nano 3(9), 2686–2696 (2009).
[Crossref] [PubMed]

2008 (5)

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F. A. Jaffer, D. E. Kim, L. Quinti, C. H. Tung, E. Aikawa, A. N. Pande, R. H. Kohler, G. P. Shi, P. Libby, and R. Weissleder, “Optical visualization of cathepsin K activity in atherosclerosis with a novel, protease-activatable fluorescence sensor,” Circulation 115(17), 2292–2298 (2007).
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2004 (3)

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2002 (3)

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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2001 (1)

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1999 (1)

1998 (2)

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1995 (1)

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1994 (2)

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1993 (1)

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1966 (1)

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Aglyamov, S. R.

S. Sethuraman, S. R. Aglyamov, J. H. Amirian, R. W. Smalling, and S. Y. Emelianov, “Intravascular photoacoustic imaging using an IVUS imaging catheter,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 54(5), 978–986 (2007).
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Ahn, G. O.

Ahn, J.

Aikawa, E.

F. A. Jaffer, D. E. Kim, L. Quinti, C. H. Tung, E. Aikawa, A. N. Pande, R. H. Kohler, G. P. Shi, P. Libby, and R. Weissleder, “Optical visualization of cathepsin K activity in atherosclerosis with a novel, protease-activatable fluorescence sensor,” Circulation 115(17), 2292–2298 (2007).
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Aikawa, M.

Y. Fukumoto, P. Libby, E. Rabkin, C. C. Hill, M. Enomoto, Y. Hirouchi, M. Shiomi, and M. Aikawa, “Statins alter smooth muscle cell accumulation and collagen content in established atheroma of watanabe heritable hyperlipidemic rabbits,” Circulation 103(7), 993–999 (2001).
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Akiyama, Y.

T. Niidome, M. Yamagata, Y. Okamoto, Y. Akiyama, H. Takahashi, T. Kawano, Y. Katayama, and Y. Niidome, “PEG-modified gold nanorods with a stealth character for in vivo applications,” J. Control. Release 114(3), 343–347 (2006).
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Allport, J. R.

M. F. Kircher, J. Grimm, F. K. Swirski, P. Libby, R. E. Gerszten, J. R. Allport, and R. Weissleder, “Noninvasive in vivo imaging of monocyte trafficking to atherosclerotic lesions,” Circulation 117(3), 388–395 (2008).
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Amblard, F.

Amirbekian, V.

F. Hyafil, J. C. Cornily, J. E. Feig, R. Gordon, E. Vucic, V. Amirbekian, E. A. Fisher, V. Fuster, L. J. Feldman, and Z. A. Fayad, “Noninvasive detection of macrophages using a nanoparticulate contrast agent for computed tomography,” Nat. Med. 13(5), 636–641 (2007).
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Amirian, J.

Amirian, J. H.

S. Sethuraman, S. R. Aglyamov, J. H. Amirian, R. W. Smalling, and S. Y. Emelianov, “Intravascular photoacoustic imaging using an IVUS imaging catheter,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 54(5), 978–986 (2007).
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Aretz, H. T.

G. J. Tearney, H. Yabushita, S. L. Houser, H. T. Aretz, I. K. Jang, K. H. Schlendorf, C. R. Kauffman, M. Shishkov, E. F. Halpern, and B. E. Bouma, “Quantification of macrophage content in atherosclerotic plaques by optical coherence tomography,” Circulation 107(1), 113–119 (2003).
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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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M. M. Arnida, M. M. Janát-Amsbury, A. Ray, C. M. Peterson, and H. Ghandehari, “Geometry and surface characteristics of gold nanoparticles influence their biodistribution and uptake by macrophages,” Eur. J. Pharm. Biopharm. 77(3), 417–423 (2011).
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J. E. Phipps, D. Vela, T. Hoyt, D. Halaney, J. J. Mancuso, L. M. Buja, R. Asmis, T. E. Milner, and M. D. Feldman, “Macrophages and intravascular optical coherence tomography bright spots: a quantitative study,” JACC Cardiovasc. Imaging 8(1), 63–72 (2015).
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Bansal, V.

R. Shukla, V. Bansal, M. Chaudhary, A. Basu, R. R. Bhonde, and M. Sastry, “Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: a microscopic overview,” Langmuir 21(23), 10644–10654 (2005).
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Bartlett, L. A.

G. J. Tearney, S. Waxman, M. Shishkov, B. J. Vakoc, M. J. Suter, M. I. Freilich, A. E. Desjardins, W. Y. Oh, L. A. Bartlett, M. Rosenberg, and B. E. Bouma, “Three-dimensional coronary artery microscopy by intracoronary optical frequency domain imaging,” JACC Cardiovasc. Imaging 1(6), 752–761 (2008).
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Bartsch, G. E.

W. Insull and G. E. Bartsch., “Cholesterol, triglyceride, and phospholipid content of intima, media, and atherosclerotic fatty streak in human thoracic aorta,” J. Clin. Invest. 45(4), 513–523 (1966).
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A. Tawakol, R. Q. Migrino, G. G. Bashian, S. Bedri, D. Vermylen, R. C. Cury, D. Yates, G. M. LaMuraglia, K. Furie, S. Houser, H. Gewirtz, J. E. Muller, T. J. Brady, and A. J. Fischman, “In vivo 18F-fluorodeoxyglucose positron emission tomography imaging provides a noninvasive measure of carotid plaque inflammation in patients,” J. Am. Coll. Cardiol. 48(9), 1818–1824 (2006).
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Basu, A.

R. Shukla, V. Bansal, M. Chaudhary, A. Basu, R. R. Bhonde, and M. Sastry, “Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: a microscopic overview,” Langmuir 21(23), 10644–10654 (2005).
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Beaudoin, A.

A. Beaudoin, “New technique for revealing latent fingerprints on wet, porous surfaces: Oil Red O,” J. Forensic Ident. 54(4), 413–421 (2004).

Beaurepaire, E.

T. Boulesteix, A. M. Pena, N. Pagès, G. Godeau, M. P. Sauviat, E. Beaurepaire, and M. C. Schanne-Klein, “Micrometer scale ex vivo multiphoton imaging of unstained arterial wall structure,” Cytometry A 69A(1), 20–26 (2006).
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J. Bec, D. M. Ma, D. R. Yankelevich, J. Liu, W. T. Ferrier, J. Southard, and L. Marcu, “Multispectral fluorescence lifetime imaging system for intravascular diagnostics with ultrasound guidance: in vivo validation in swine arteries,” J. Biophotonics 7(5), 281–285 (2014).
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A. C. van der Wal, A. E. Becker, C. M. van der Loos, and P. K. Das, “Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology,” Circulation 89(1), 36–44 (1994).
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Beckers, L.

M. van Zandvoort, W. Engels, K. Douma, L. Beckers, M. Oude Egbrink, M. Daemen, and D. W. Slaaf, “Two-photon microscopy for imaging of the (atherosclerotic) vascular wall: A proof of concept study,” J. Vasc. Res. 41(1), 54–63 (2004).
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Bedri, S.

A. Tawakol, R. Q. Migrino, G. G. Bashian, S. Bedri, D. Vermylen, R. C. Cury, D. Yates, G. M. LaMuraglia, K. Furie, S. Houser, H. Gewirtz, J. E. Muller, T. J. Brady, and A. J. Fischman, “In vivo 18F-fluorodeoxyglucose positron emission tomography imaging provides a noninvasive measure of carotid plaque inflammation in patients,” J. Am. Coll. Cardiol. 48(9), 1818–1824 (2006).
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Benjamin, E. J.

A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, M. J. Blaha, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, S. E. Judd, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, R. H. Mackey, D. J. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, R. W. Neumar, G. Nichol, D. K. Pandey, N. P. Paynter, M. J. Reeves, P. D. Sorlie, J. Stein, A. Towfighi, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2014 update: a report from the American Heart Association,” Circulation 129(3), e28–e292 (2014).
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Berry, J. D.

A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, M. J. Blaha, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, S. E. Judd, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, R. H. Mackey, D. J. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, R. W. Neumar, G. Nichol, D. K. Pandey, N. P. Paynter, M. J. Reeves, P. D. Sorlie, J. Stein, A. Towfighi, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2014 update: a report from the American Heart Association,” Circulation 129(3), e28–e292 (2014).
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Beversluis, M. R.

M. R. Beversluis, A. Bouhelier, and L. Novotny, “Continuum generation from single gold nanostructures through near-field mediated intraband transitions,” Phys. Rev. B 68(11), 115433 (2003).
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Bhonde, R. R.

R. Shukla, V. Bansal, M. Chaudhary, A. Basu, R. R. Bhonde, and M. Sastry, “Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: a microscopic overview,” Langmuir 21(23), 10644–10654 (2005).
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Blaha, M. J.

A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, M. J. Blaha, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, S. E. Judd, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, R. H. Mackey, D. J. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, R. W. Neumar, G. Nichol, D. K. Pandey, N. P. Paynter, M. J. Reeves, P. D. Sorlie, J. Stein, A. Towfighi, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2014 update: a report from the American Heart Association,” Circulation 129(3), e28–e292 (2014).
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Boppart, S. A.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, “Integrated structural and functional optical imaging combining spectral-domain optical coherence and multiphoton microscopy,” Appl. Phys. Lett. 88(5), 053901 (2006).
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Figures (6)

Fig. 1
Fig. 1 Schematic diagram of the dual-modality fiber-based OCT-TPL imaging system consisting of OCT and TPL modules and scanning optics. Light from OCT and TPL modules are combined by dichroic mirrors (blue) and a photonic crystal fiber (yellow). Top-view and beam profile of the PCF are shown in the top-right corner. PCF: photonic crystal fiber; PMT: photomultiplier tube; BP: band pass; SP: short pass; BS: beamsplitter.
Fig. 2
Fig. 2 (a) Schematic diagram of the custom-designed pulse compensator comprised of a transmission diffraction grating, a focusing lens and a mirror. (b) Zemax simulation of optical path length and GDD with ray tracing for the pulse compensator configured in (a). Ray colors in (b) represent spectral bandwidth of the TPL excitation laser centered at 800 nm (i.e., 795-805 nm). (c,d) Temporal intensity and phase measurement of pulse duration at the output of TPL excitation laser (800 nm) and on the sample after employing the pulse compensator, respectively. Pulse intensity and phase were characterized using an ultrashort-laser-pulse measurement device (Grenouille, SwampOptics, Atlanta, GA).
Fig. 3
Fig. 3 Dual-modality OCT-TPL imaging of a stainless steel ruler. En face OCT (a,d), co-registered TPL (b,e), and merged OCT-TPL (c,f) images of numeral “8” and scale bars, respectively, on the ruler. (g) 3D OCT image set merged with the TPL image, showing composition of the ruler in the context of its surface structure. Red indicates TPL emission in (c,f,g).
Fig. 4
Fig. 4 Dual-modality OCT-TPL imaging of a human coronary artery. TPL (a), en face OCT (b), merged en face OCT-TPL (c), merged 3D OCT-TPL (d) images of the plaque region. Red in (c,d) indicates TPL signal measured at emission wavelengths shorter than 640 nm while green in (c) represents back scattered OCT signal. The inset image in (d) shows the merged 3D OCT-TPL image at a different angle. (e) B-scan OCT image at the white dashed line in (a). Higher intensity regions of the TPL emission signal profile (red curve in (e), a.u.) at the white dashed line in (a) correspond to lower intensity regions (yellow dashed boxes “a,b,c”) in the B-scan OCT image. Yellow arrows point to small regions of lower scattering intensity in dashed box “c”.
Fig. 5
Fig. 5 Dual-modality OCT-TPL imaging of a human coronary artery and corresponding histology. TPL (a), en face OCT (b), merged en face OCT-TPL (c), merged 3D OCT-TPL (d) images of the plaque region. Red in (c,d) indicates TPL signal measured at emission wavelengths shorter than 640 nm while green in (c) represents back scattered OCT signal. The inset image in (d) shows the merged 3D OCT-TPL image at a different angle. (e,f) ORO and Tri-Elastic stains of a histological tissue section at the white dashed line in (a), showing lipid deposits (red) and collagen (green)/elastin (black) fibers respectively. (g) B-scan OCT image at the white dashed line in (a). Lower intensity regions (yellow dashed boxes “a,b” in (g)) are represented by higher intensity regions (yellow dashed boxes “a,b” in (a)) along the white dashed line in the TPL image and are consistent with histology (yellow dashed boxes “a,b” in (e)).
Fig. 6
Fig. 6 (a) TPL image of the plaque region. (b) ORO stain of a histological tissue section at the white dashed line in (a), showing a lipid pool (red) deep in the tissue. (c) B-scan OCT image at the white dashed line in (a). Lower intensity regions (yellow dashed boxes “a,b”) in the B-scan OCT image (c) are represented by higher intensity regions along the white dashed line in the TPL image (yellow dashed boxes “a,b” in (a)) and consistent with the lipid locations in the histology image (b).

Equations (1)

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GDD= λ 3 π c 2 s 2 cos 2 θ o (fz)

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