Quantitative nonlinear optical assessment of atherosclerosis progression in rabbits.

Quantification of atherosclerosis has been a challenging task owing to its complex pathology. In this study, we validated a quantitative approach for assessing atherosclerosis progression in a rabbit model using a numerical matrix, optical index for plaque burden, derived directly from the nonlinear optical microscopic images captured on the atherosclerosis-affected blood vessel. A positive correlation between this optical index and the severity of atherosclerotic lesions, represented by the age of the rabbits, was established based on data collected from 21 myocardial infarction-prone Watanabe heritable hyperlipidemic rabbits with age ranging between new-born and 27 months old. The same optical index also accurately identified high-risk locations for atherosclerotic plaque formation along the entire aorta, which was validated by immunohistochemical fluorescence imaging.

[1]  F. Grosveld,et al.  Atherosclerotic Lesion Size and Vulnerability Are Determined by Patterns of Fluid Shear Stress , 2006, Circulation.

[2]  W. Webb,et al.  Multiphoton microscopy in biological research. , 2001, Current opinion in chemical biology.

[3]  Graham A Wright,et al.  Innovations in imaging for chronic total occlusions: a glimpse into the future of angiography's blind-spot. , 2008, European heart journal.

[4]  R. Ross,et al.  Smooth muscle cells and the pathogenesis of the lesions of atherosclerosis. , 1993, British heart journal.

[5]  J. Hodgson,et al.  Intracoronary ultrasound imaging: correlation of plaque morphology with angiography, clinical syndrome and procedural results in patients undergoing coronary angioplasty. , 1993, Journal of the American College of Cardiology.

[6]  P. Fitzgerald,et al.  Intravascular ultrasound: state of the art and future directions. , 1998, The American journal of cardiology.

[7]  R. Abbate,et al.  Role of hemodynamic shear stress in cardiovascular disease. , 2011, Atherosclerosis.

[8]  T. Kita,et al.  Cellular Pathology of Progressive Atherosclerosis in the WHHL Rabbit: An Animal Model of Familial Hypercholesterolemia , 1983, Arteriosclerosis.

[9]  D. Schneck,et al.  In vitro studies of local blood flow disturbance in a region of separation. , 1968, Journal of atherosclerosis research.

[10]  H SCHARFSTEIN,et al.  Changes of Boundary Layer Flow in Model Systems: Implications For Initiation Of Endothelial Injury , 1963, Circulation research.

[11]  Majid Naji,et al.  Portable, miniaturized, fibre delivered, multimodal CARS exoscope. , 2013, Optics express.

[12]  R. Megens.  Vital imaging of large arteries using two-photon laser scanning microscopy : focus on the arterial wall , 2008 .

[13]  J. Tarbell.  Mass transport in arteries and the localization of atherosclerosis. , 2003, Annual review of biomedical engineering.

[14]  W D Wagner,et al.  A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. , 1994, Circulation.

[15]  Alex Boeglin,et al.  Polarization state studies in second harmonic generation signals to trace atherosclerosis lesions. , 2011, Optics express.

[16]  Jianglin Fan,et al.  Development of an Animal Model for Spontaneous Myocardial Infarction (WHHLMI Rabbit) , 2003 .

[17]  Adrian F. Pegoraro,et al.  Differentiating atherosclerotic plaque burden in arterial tissues using femtosecond CARS-based multimodal nonlinear optical imaging , 2010, Biomedical optics express.

[18]  Yasuhiro Honda,et al.  Frontiers in intravascular imaging technologies. , 2008, Circulation.

[19]  P. Stone,et al.  Relation of vessel wall shear stress to atherosclerosis progression in human coronary arteries. , 1993, Arteriosclerosis and thrombosis : a journal of vascular biology.

[20]  D. Ku,et al.  Pulsatile Flow and Atherosclerosis in the Human Carotid Bifurcation: Positive Correlation between Plaque Location and Low and Oscillating Shear Stress , 1985, Arteriosclerosis.

[21]  Andrew Ridsdale,et al.  Multimodal nonlinear optical imaging of atherosclerotic plaque development in myocardial infarction-prone rabbits. , 2010, Journal of biomedical optics.

[22]  上田 高志,et al.  Arterioscler Thromb Vasc Biol誌掲載論文 強い生理的光曝露によるPGC-1αを介したVEGF発現上昇と脈絡膜新生血管の増強作用 (日本人のヒット論文 : 本音で語る苦労話(第2回)) , 2013 .

[23]  Ji-Xin Cheng,et al.  Imaging and Quantitative Analysis of Atherosclerotic Lesions by CARS-Based Multimodal Nonlinear Optical Microscopy , 2009, Arteriosclerosis, thrombosis, and vascular biology.

[24]  Joseph M Schmitt,et al.  Current and future developments in intracoronary optical coherence tomography imaging. , 2009, EuroIntervention : journal of EuroPCR in collaboration with the Working Group on Interventional Cardiology of the European Society of Cardiology.

[25]  D. Ku.  BLOOD FLOW IN ARTERIES , 1997 .

[26]  J. Coucher,et al.  Expression of intercellular adhesion molecule-1 in atherosclerotic plaques. , 1992, The American journal of pathology.

[27]  E. Boerwinkle,et al.  Circulating adhesion molecules VCAM-1, ICAM-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease cases: the Atherosclerosis Risk In Communities (ARIC) study. , 1997, Circulation.

[28]  W. Denk,et al.  Deep tissue two-photon microscopy , 2005, Nature Methods.

[29]  J. Scoazec,et al.  Differential upregulation of cellular adhesion molecules at the sites of oxidative stress in experimental acute pancreatitis. , 2001, The Journal of surgical research.

[30]  P. Serruys,et al.  Proliferation and extracellular matrix synthesis of smooth muscle cells cultured from human coronary atherosclerotic and restenotic lesions. , 1994, Journal of the American College of Cardiology.

[31]  Gangjun Liu,et al.  Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner. , 2012, Journal of biomedical optics.

[32]  S. Alper,et al.  Hemodynamic shear stress and its role in atherosclerosis. , 1999, JAMA.

[33]  Ji-Xin Cheng,et al.  Label-free molecular imaging of atherosclerotic lesions using multimodal nonlinear optical microscopy. , 2007, Journal of biomedical optics.

[34]  P. Libby.  Changing concepts of atherogenesis , 2000, Journal of internal medicine.

[35]  Bruce J Tromberg,et al.  Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy. , 2004, Biophysical journal.

[36]  Jane A Dickerson,et al.  Current Applications of Liquid Chromatography / Mass Spectrometry in Pharmaceutical Discovery After a Decade of Innovation , 2008 .

[37]  R. Ross,et al.  Response to injury and atherogenesis. , 1977, The American journal of pathology.

[38]  W. Webb,et al.  Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[39]  X. Xie,et al.  Towards CARS Endoscopy. , 2006, Optics express.

[40]  Yujie Zhou,et al.  Identification and quantification of coronary atherosclerotic plaques: a comparison of 64-MDCT and intravascular ultrasound. , 2008, AJR. American journal of roentgenology.

[41]  Karel Svoboda,et al.  ScanImage: Flexible software for operating laser scanning microscopes , 2003, Biomedical engineering online.

[42]  R. Virmani,et al.  The thin-cap fibroatheroma: a type of vulnerable plaque: The major precursor lesion to acute coronary syndromes , 2001, Current opinion in cardiology.

[43]  Conor L Evans,et al.  Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  A. Pena,et al.  Second harmonic imaging and scoring of collagen in fibrotic tissues. , 2007, Optics express.

[45]  Brett E. Bouma,et al.  In Vivo Characterization of Coronary Atherosclerotic Plaque by Use of Optical Coherence Tomography , 2005, Circulation.

[46]  Haohua Tu,et al.  Coherent anti‐Stokes Raman scattering microscopy: overcoming technical barriers for clinical translation , 2014, Journal of biophotonics.

[47]  M. Davies,et al.  The expression of the adhesion molecules ICAM‐1, VCAM‐1, PECAM, and E‐selectin in human atherosclerosis , 1993, The Journal of pathology.

[48]  Mark Hewko,et al.  Collagen morphology and texture analysis: from statistics to classification , 2013, Scientific Reports.

[49]  D. Rosenthal,et al.  Cell Adhesion Molecules , 1991, International journal of dermatology.

[50]  W. Stehbens.  Turbulence of blood flow. , 1959, Quarterly journal of experimental physiology and cognate medical sciences.

[51]  T. T. Le,et al.  Label-free Imaging of Arterial Cells and Extracellular Matrix Using a Multimodal CARS Microscope. , 2008, Optics communications.

[52]  Jianglin Fan,et al.  Correlation of vulnerable coronary plaques to sudden cardiac events. Lessons from a myocardial infarction-prone animal model (the WHHLMI rabbit). , 2004, Journal of atherosclerosis and thrombosis.

[53]  W D Wagner,et al.  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. , 1995, Arteriosclerosis, thrombosis, and vascular biology.

[54]  R. Virmani,et al.  Vascular reactivity during the progression of atherosclerotic plaque. A study in Watanabe heritable hyperlipidemic rabbits. , 1990, Circulation research.

[55]  W. Webb,et al.  Nonlinear magic: multiphoton microscopy in the biosciences , 2003, Nature Biotechnology.

[56]  P. Serruys,et al.  Optical coherence tomography assessment of vulnerable plaque rupture: predilection for the plaque 'shoulder'. , 2008, European heart journal.

[57]  Jerome Mertz,et al.  Nonlinear microscopy: new techniques and applications , 2004, Current Opinion in Neurobiology.

[58]  R. Schroter,et al.  Arterial Wall Shear and Distribution of Early Atheroma in Man , 1969, Nature.

[59]  A. Blann,et al.  Circulating ICAM-1 and VCAM-1 in Peripheral Artery Disease and Hypercholesterolaemia: Relationship to the Location of Atherosclerotic Disease, Smoking, and in the Prediction of Adverse Events , 1998, Thrombosis and Haemostasis.

[60]  A. Barakat,et al.  Unsteady and three-dimensional simulation of blood flow in the human aortic arch. , 2002, Journal of biomechanical engineering.

[61]  V. Gahtan,et al.  Localization of atherosclerosis: role of hemodynamics. , 1999, Archives of surgery.

[62]  R. Sacco,et al.  Aortic Arch Plaques and Risk of Recurrent Stroke and Death , 2009, Circulation.

[63]  X. Xie,et al.  Coherent Anti-Stokes Raman Scattering Microscopy: Instrumentation, Theory, and Applications , 2004 .

[64]  E. Andreeva,et al.  Collagen-synthesizing cells in initial and advanced atherosclerotic lesions of human aorta. , 1997, Atherosclerosis.

[65]  B L Langille,et al.  Expression of ICAM-1 and VCAM-1 and monocyte adherence in arteries exposed to altered shear stress. , 1995, Arteriosclerosis, thrombosis, and vascular biology.