Super-resolution ultrasound imaging method for microvasculature in vivo with a high temporal accuracy

Traditional ultrasound imaging techniques are limited in spatial resolution to visualize angiogenic vasa vasorum that is considered as an important marker for atherosclerotic plaque progression and vulnerability. The recently introduced super-resolution imaging technique based on microbubble center localization has shown potential to achieve unprecedented high spatial resolution beyond the acoustic diffraction limit. However, a major drawback of the current super-resolution imaging approach is low temporal resolution because it requires a large number of imaging frames. In this study, a new imaging sequence and signal processing approach for super-resolution ultrasound imaging are presented to improve temporal resolution by employing deconvolution and spatio-temporal-interframe-correlation based data acquisition. In vivo feasibility of the developed technology is demonstrated and evaluated in imaging vasa vasorum in the rabbit atherosclerosis model. The proposed method not only identifies a tiny vessel with a diameter of 41 μm, 5 times higher spatial resolution than the acoustic diffraction limit at 7.7 MHz, but also significantly improves temporal resolution that allows for imaging vessels over cardiac motion.

[1]  David J Mikulis,et al.  Intracranial vasa vasorum: insights and implications for imaging. , 2013, Radiology.

[2]  Paul A. Dayton,et al.  Real‐time ultrasound angiography using superharmonic dual‐frequency (2.25 MHz/30 MHz) cylindrical array: In vitro study , 2018, Ultrasonics.

[3]  Junsu Lee,et al.  A 35 MHz/105 MHz Dual-Element Focused Transducer for Intravascular Ultrasound Tissue Imaging Using the Third Harmonic , 2018, Sensors.

[4]  Trevor Coward,et al.  An In-Vitro Study , 2016 .

[5]  D S Biggs,et al.  Acceleration of iterative image restoration algorithms. , 1997, Applied optics.

[6]  Kerstin Pingel,et al.  50 Years of Image Analysis , 2012 .

[7]  Chao Zhang,et al.  Relationship between Enhanced Intensity of Contrast Enhanced Ultrasound and Microvessel Density of Aortic Atherosclerostic Plaque in Rabbit Model , 2014, PloS one.

[8]  E L Ritman,et al.  Impact of coronary vasa vasorum functional structure on coronary vessel wall perfusion distribution. , 2003, American journal of physiology. Heart and circulatory physiology.

[9]  Junyan Xu,et al.  Vasa Vasorum in Atherosclerosis and Clinical Significance , 2015, International journal of molecular sciences.

[10]  Amir Lerman,et al.  The Vasa Vasorum in Atherosclerosis: The Vessel Within the Vascular Wall. , 2015, Journal of the American College of Cardiology.

[11]  Charlie Demené,et al.  Spatiotemporal Clutter Filtering of Ultrafast Ultrasound Data Highly Increases Doppler and fUltrasound Sensitivity , 2015, IEEE Transactions on Medical Imaging.

[12]  Michael J Rust,et al.  Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM) , 2006, Nature Methods.

[13]  C. Dunsby,et al.  3-D In Vitro Acoustic Super-Resolution and Super-Resolved Velocity Mapping Using Microbubbles , 2015, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[14]  Qifa Zhou,et al.  Multi-frequency intravascular ultrasound (IVUS) imaging , 2015, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[15]  X. Zhuang,et al.  Statistical deconvolution for superresolution fluorescence microscopy. , 2012, Biophysical journal.

[16]  Xiaoning Jiang,et al.  Design factors of intravascular dual frequency transducers for super-harmonic contrast imaging and acoustic angiography , 2015, Physics in medicine and biology.

[17]  R. Prescott,et al.  Edinburgh Artery Study: prevalence of asymptomatic and symptomatic peripheral arterial disease in the general population. , 1991, International journal of epidemiology.

[18]  Yongmin Kim,et al.  Adaptive clutter filtering for ultrasound color flow imaging. , 2003, Ultrasound in medicine & biology.

[19]  G. Schmitz,et al.  Imaging tumor vascularity by tracing single microbubbles , 2011, 2011 IEEE International Ultrasonics Symposium.

[20]  Angels Betriu,et al.  Left carotid adventitial vasa vasorum signal correlates directly with age and with left carotid intima-media thickness in individuals without atheromatous risk factors , 2015, Cardiovascular Ultrasound.

[21]  J. Lippincott-Schwartz,et al.  Imaging Intracellular Fluorescent Proteins at Nanometer Resolution , 2006, Science.

[22]  Hiroshi Okamoto,et al.  In vivo assessment of vasa vasorum neovascularization using intravascular ultrasound: A comparison between acute coronary syndrome and stable angina pectoris. , 2017, Journal of cardiology.

[23]  Timo Liimatainen,et al.  High-resolution ultrasound perfusion imaging of therapeutic angiogenesis. , 2008, JACC. Cardiovascular imaging.

[24]  Patrick W Serruys,et al.  PCSK9 in relation to coronary plaque inflammation: Results of the ATHEROREMO-IVUS study. , 2016, Atherosclerosis.

[25]  Kun Sun,et al.  Feasibility Study on Prenatal Cardiac Screening Using Four-Dimensional Ultrasound with Spatiotemporal Image Correlation: A Multicenter Study , 2016, PloS one.

[26]  Diane R. Eaker,et al.  Quantification of Vasa Vasorum Density in Multi-Slice Computed Tomographic Coronary Angiograms: Role of Computed Tomographic Image Voxel Size , 2010, Journal of computer assisted tomography.

[27]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[28]  Diego Ardissino,et al.  [From vulnerable plaque to vulnerable patient]. , 2010, Giornale italiano di cardiologia.

[29]  Jonathan R Lindner,et al.  Temporal characterization of the functional density of the vasa vasorum by contrast-enhanced ultrasonography maximum intensity projection imaging. , 2010, JACC. Cardiovascular imaging.

[30]  Renu Virmani,et al.  Intraplaque hemorrhage and progression of coronary atheroma. , 2003, The New England journal of medicine.

[31]  Yonina C. Eldar,et al.  > Replace This Line with Your Paper Identification Number (double-click Here to Edit) < , 2022 .

[32]  Akira Taruya,et al.  Vasa Vasorum Restructuring in Human Atherosclerotic Plaque Vulnerability: A Clinical Optical Coherence Tomography Study. , 2015, Journal of the American College of Cardiology.

[33]  William H. Richardson,et al.  Bayesian-Based Iterative Method of Image Restoration , 1972 .

[34]  F Viñals,et al.  Spatio‐temporal image correlation (STIC): a new tool for the prenatal screening of congenital heart defects , 2003, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[35]  Robert J. Eckersley,et al.  In Vivo Acoustic Super-Resolution and Super-Resolved Velocity Mapping Using Microbubbles , 2015, IEEE Transactions on Medical Imaging.

[36]  M. Tanter,et al.  Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging , 2015, Nature.

[37]  Juan J. Badimon,et al.  Plaque Neovascularization Is Increased in Ruptured Atherosclerotic Lesions of Human Aorta: Implications for Plaque Vulnerability , 2004, Circulation.

[38]  Paul Beard,et al.  Imaging techniques: Super-resolution ultrasound , 2015, Nature.

[39]  L. Lucy An iterative technique for the rectification of observed distributions , 1974 .

[40]  Erik L Ritman,et al.  Correlation of Vasa Vasorum Neovascularization and Plaque Progression in Aortas of Apolipoprotein E−/−/Low-Density Lipoprotein−/− Double Knockout Mice , 2005, Arteriosclerosis, thrombosis, and vascular biology.

[41]  Dan Adam,et al.  Contrast-enhanced ultrasound imaging of the vasa vasorum: from early atherosclerosis to the identification of unstable plaques. , 2010, JACC. Cardiovascular imaging.

[42]  Evelyn Regar,et al.  In vivo detection of high-risk coronary plaques by radiofrequency intravascular ultrasound and cardiovascular outcome: results of the ATHEROREMO-IVUS study. , 2014, European heart journal.

[43]  Zahi A Fayad,et al.  Atherothrombosis and high-risk plaque: Part II: approaches by noninvasive computed tomographic/magnetic resonance imaging. , 2005, Journal of the American College of Cardiology.

[44]  Tai-kyong Song,et al.  Evaluation of flow estimation methods for 3D color Doppler imaging , 2010, 2010 IEEE International Ultrasonics Symposium.

[45]  Chih-Chung Huang,et al.  40 MHz high‐frequency ultrafast ultrasound imaging , 2017, Medical physics.

[46]  Amir Lerman,et al.  IVUS detection of vasa vasorum blood flow distribution in coronary artery vessel wall. , 2012, JACC. Cardiovascular imaging.

[47]  Linda Lavery,et al.  Quantification of plaque neovascularization using contrast ultrasound: a histologic validation. , 2011, European heart journal.