Deep Learning of Spatiotemporal Filtering for Fast Super-Resolution Ultrasound Imaging

Super-resolution ultrasound (SR-US) imaging is a new technique that breaks the diffraction limit and allows visualization of microvascular structures down to tens of micrometers. The image processing methods for the spatiotemporal filtering needed in SR-US, such as singular value decomposition (SVD), are computationally burdensome and performed offline. Deep learning has been applied to many biomedical imaging problems, and trained neural networks have been shown to process an image in milliseconds. The goal of this study was to evaluate the effectiveness of deep learning to realize a spatiotemporal filter in the context of SR-US processing. A 3-D convolutional neural network (3DCNN) was trained on <italic>in vitro</italic> and <italic>in vivo</italic> data sets using SVD as ground truth in tissue clutter reduction. <italic>In vitro</italic> data were obtained from a tissue-mimicking flow phantom, and <italic>in vivo</italic> data were collected from murine tumors of breast cancer. Three training techniques were studied: training with <italic>in vitro</italic> data sets, training with <italic>in vivo</italic> data sets, and transfer learning with initial training on <italic>in vitro</italic> data sets followed by fine-tuning with <italic>in vivo</italic> data sets. The neural network trained with <italic>in vitro</italic> data sets followed by fine-tuning with <italic>in vivo</italic> data sets had the highest accuracy at 88.0%. The SR-US images produced with deep learning allowed visualization of vessels as small as <inline-formula> <tex-math notation="LaTeX">$25~\mu \text{m}$ </tex-math></inline-formula> in diameter, which is below the diffraction limit (wavelength of <inline-formula> <tex-math notation="LaTeX">$110~\mu \text{m}$ </tex-math></inline-formula> at 14 MHz). The performance of the 3DCNN was encouraging for real-time SR-US imaging with an average processing frame rate for <italic>in vivo</italic> data of 51 Hz with GPU acceleration.

[1]  Kenneth Hoyt,et al.  Ultrasound imaging of breast tumor perfusion and neovascular morphology. , 2015, Ultrasound in medicine & biology.

[2]  F. Herth,et al.  Real-time endobronchial ultrasound guided transbronchial needle aspiration for sampling mediastinal lymph nodes , 2006, Thorax.

[3]  John A. Hossack,et al.  The Singular Value Filter: A General Filter Design Strategy for PCA-Based Signal Separation in Medical Ultrasound Imaging , 2011, IEEE Transactions on Medical Imaging.

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

[5]  Kenneth Hoyt,et al.  Toward optimization of in vivo super‐resolution ultrasound imaging using size‐selected microbubble contrast agents , 2017, Medical physics.

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

[7]  Billy Y. S. Yiu,et al.  A GPU-Parallelized Eigen-Based Clutter Filter Framework for Ultrasound Color Flow Imaging , 2017, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[8]  Guigang Zhang,et al.  Deep Learning , 2016, Int. J. Semantic Comput..

[9]  Paul A. Dayton,et al.  3-D Ultrasound Localization Microscopy for Identifying Microvascular Morphology Features of Tumor Angiogenesis at a Resolution Beyond the Diffraction Limit of Conventional Ultrasound , 2017, Theranostics.

[10]  Armando Manduca,et al.  Ultrasound Small Vessel Imaging With Block-Wise Adaptive Local Clutter Filtering , 2017, IEEE Transactions on Medical Imaging.

[11]  C Dunsby,et al.  Acoustic super-resolution with ultrasound and microbubbles , 2013, Physics in medicine and biology.

[12]  Armando Manduca,et al.  Accelerated Singular Value-Based Ultrasound Blood Flow Clutter Filtering With Randomized Singular Value Decomposition and Randomized Spatial Downsampling , 2017, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[13]  Guang-Zhong Yang,et al.  Deep Learning for Health Informatics , 2017, IEEE Journal of Biomedical and Health Informatics.

[14]  John A Hossack,et al.  Real-time targeted molecular imaging using singular value spectra properties to isolate the adherent microbubble signal , 2012, Physics in medicine and biology.

[15]  Ming Yang,et al.  3D Convolutional Neural Networks for Human Action Recognition , 2010, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[16]  Hassan Rivaz,et al.  Suppressing Clutter Components In Ultrasound Color Flow Imaging Using Robust Matrix Completion Algorithm: Simulation And Phantom Study , 2019, 2019 IEEE 16th International Symposium on Biomedical Imaging (ISBI 2019).

[17]  Katherine W Ferrara,et al.  Ultrasound localization microscopy to image and assess microvasculature in a rat kidney , 2017, Scientific Reports.

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

[19]  Armando Manduca,et al.  Improved Super-Resolution Ultrasound Microvessel Imaging With Spatiotemporal Nonlocal Means Filtering and Bipartite Graph-Based Microbubble Tracking , 2018, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[20]  I. Kaplan,et al.  Real time MRI-ultrasound image guided stereotactic prostate biopsy. , 2002, Magnetic resonance imaging.

[21]  Ronald M. Summers,et al.  Deep Convolutional Neural Networks for Computer-Aided Detection: CNN Architectures, Dataset Characteristics and Transfer Learning , 2016, IEEE Transactions on Medical Imaging.

[22]  Helmut Ermert,et al.  Initial experiences with real-time elastography guided biopsies of the prostate. , 2005, The Journal of urology.

[23]  Mickael Tanter,et al.  Ultrasound Localization Microscopy and Super-Resolution: A State of the Art , 2018, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[24]  Kenneth Hoyt,et al.  Deep learning in spatiotemporal filtering for super-resolution ultrasound imaging , 2019, 2019 IEEE International Ultrasonics Symposium (IUS).

[25]  Yonina C. Eldar,et al.  Super-Resolution Ultrasound Localization Microscopy Through Deep Learning , 2018, IEEE Transactions on Medical Imaging.

[26]  Yonina C. Eldar,et al.  Deep Convolutional Robust PCA with Application to Ultrasound Imaging , 2019, ICASSP 2019 - 2019 IEEE International Conference on Acoustics, Speech and Signal Processing (ICASSP).

[27]  Yonina C. Eldar,et al.  Deep Learning in Ultrasound Imaging , 2019, Proceedings of the IEEE.

[28]  Ki Jinn Chin,et al.  Needle Visualization in Ultrasound-Guided Regional Anesthesia: Challenges and Solutions , 2008, Regional Anesthesia & Pain Medicine.

[29]  Kenneth Hoyt,et al.  Deep 3D convolutional neural networks for fast super-resolution ultrasound imaging , 2019, Medical Imaging.

[30]  Mickael Tanter,et al.  Microvascular flow dictates the compromise between spatial resolution and acquisition time in Ultrasound Localization Microscopy , 2019, Scientific Reports.

[31]  Kenneth Hoyt,et al.  Recent developments in dynamic contrast-enhanced ultrasound imaging of tumor angiogenesis. , 2014, Imaging in medicine.

[32]  Jian Sun,et al.  Deep Residual Learning for Image Recognition , 2015, 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR).

[33]  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.

[34]  K W Ferrara,et al.  Evaluation of tumor angiogenesis with US: imaging, Doppler, and contrast agents. , 2000, Academic radiology.

[35]  L Pourcelot,et al.  Clinical use of ultrasound tissue harmonic imaging. , 1999, Ultrasound in medicine & biology.

[36]  Kurt Hornik,et al.  Multilayer feedforward networks are universal approximators , 1989, Neural Networks.

[37]  Yonina C. Eldar,et al.  Deep Learning for Super-resolution Vascular Ultrasound Imaging , 2019, ICASSP 2019 - 2019 IEEE International Conference on Acoustics, Speech and Signal Processing (ICASSP).

[38]  Kenneth Hoyt,et al.  Super‐Resolution Ultrasound Imaging of Skeletal Muscle Microvascular Dysfunction in an Animal Model of Type 2 Diabetes , 2019, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[39]  Kenneth Hoyt,et al.  Monitoring early tumor response to vascular targeted therapy using super-resolution ultrasound imaging , 2017, 2017 IEEE International Ultrasonics Symposium (IUS).

[40]  P. Scardino,et al.  The appearance of prostate cancer on transrectal ultrasonography: correlation of imaging and pathological examinations. , 1989, The Journal of urology.

[41]  Debabrata Ghosh,et al.  Hyposialylated IgG activates endothelial IgG receptor Fc&ggr;RIIB to promote obesity-induced insulin resistance , 2017, The Journal of clinical investigation.

[42]  Yoshua Bengio,et al.  How transferable are features in deep neural networks? , 2014, NIPS.