Ultrafast ultrasound localization microscopy method for spinal cord mircovasculature imaging

Yu Jun-Jin; Guo Xing-Yi; Sui Yi-Hui; Song Jian-Ping; Ta De-An; Mei Yong-Feng; Xu Kai-Liang

doi:10.7498/aps.71.20220629

Abstract

Function of spinal cord is crucial to nerve conduction pathway. Traumatic spinal cord injury often results in a vasculature disruption after primary insult and further leads to abnormal responses of the intact vessels in neighboring tissue during secondary injury. Therefore, the vasculature and blood supply play significant roles in evaluating the spinal cord function . Ultrasound localization microscopy (ULM) overcomes the shortcomings of extensively used angiography, such as computed tomography angiography (CTA) and magnetic resonance angiography (MRA), in terms of limited resolution, radiation and poor-portability, which meets the needs of comprehensive intraoperative examination and prognosis tracking. In this study, an L22-14vX probe with a transmission frequency of 15.625 MHz is utilized, yielding an imaging wavelength of 100 μm. The ULM is conducted based on ultrafast ultrasound technology with multiple tilted plane-wave illuminations. Robust principal component analysis (RPCA) based spatial-temporal clutter filtering method is used for separating the microbubble signals from tissue signals and high frequency noise. Through microbubble localization, trajectory tracking and mapping, subwavelength super-resolution ultrasound imaging is finally achieved. The whole process of microbubble localization and vessel reconstruction are monitored through measuring the time dependent microbubble detections and saturation. Saturation curve corresponds to the time dependent total area covered by microbubble detections on the image. Quantification analysis is carried out for evaluating the imaging results including resolution measurements based on the Fourier ring correlation (FRC) and full-width at half-maximum (FWHM). The in-vivo experimental results show that ULM can be used to obtain super-resolution vasculature imaging in rat spinal cord. The velocity distributed from 1 mm/s to 50 mm/s can be detected. Within the same vessel, the velocity of a point is inversely correlated with the distance from the point to the center of the vessel. The velocity in the center of the vessel is larger than that at the wall of the vessel. The larger vessels support higher flow in the center of the vessel. The FWHM results indicate that ultrafast Doppler displays vessels in diameters between 135 μm and 270 μm while ULM displays them in diameters between 28 μm and 35 μm. The FRC-based resolution evaluation shows that the ULM achieves a super resolution of 16 μm, much less than the imaging wavelength of 100 μm. Yet, long acquisition time is required to detect microbubbles in the smallest vessels, leading to long reconstruction of the microvasculature, which is still a problem worth studying . Compromise between saturation and acquisition time needs considering. Generally speaking, microbubbles are more likely to flow in large vessels, leading to relatively short reconstruction time of large vessels. When saturation curve almost converges, the imaging improvement with new vessels is not so significant that the detail sacrifice of some small microvessels can reduce acquisition time (i.e. most of microvasculature can still be gained when the saturation curve does not converge). Besides, the increase of microbubble concentration and advanced track identification and extraction may also accelerate the saturation rate of convergence with acquisition time decreasing. In conclusion, ULM can be used to obtain a super-resolution imaging of spinal cord microvasculature, giving a 10-fold improvement in resolution in comparison with ultrafast Doppler imaging. Relevant results can facilitate the super-resolution ULM imaging of spinal cord which may promote the function diagnosis, treatment intervention, disability prevention, and prognosis recovery of spinal cord injury.

Keywords:

ultrasound localization microscopy (ULM) /
ultrafast ultrasound /
super-resolution /
spinal cord microvasculature

Authors and contacts

1.
Center for Biomedical Engineering, School of Information Science and Technology, Fudan University, Shanghai 200438, China
2.
Academy for Engineering and Technology, Fudan University, Shanghai 200438, China
3.
Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai 200040, China
4.
Department of Materials Science, Fudan University, Shanghai 200438, China

Corresponding author: Xu Kai-Liang, xukl@fudan.edu.cn

Funds: Project supported by the National Natural Science Foundation of China (Grant Nos. 11974081, 51961145108, 11827808), the Natural Science Foundation of Shanghai, China (Grant No. 19ZR1402700), and the Shanghai Rising Star Program, China (Grant No. 20QC1400200).

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Cited By

图 1 超分辨率超快超声工作流程

Figure 1. Workflow of Ultrafast Ultrasound Localization Microscopy.

DownLoad: Full-Size Img PowerPoint

图 2 基于FRC曲线的分辨率测定

Figure 2. Resolution measurement based on FRC curve.

DownLoad: Full-Size Img PowerPoint

图 3 ULM处理过程结果　(a) 第150个数据块中第200帧回波信号的B超图像; (b) 第150个数据块中第200帧分离出的微泡回波信号; (c) 第150个数据块中第300帧微泡定位结果; (d) 第150个数据块中第301帧微泡定位结果

Figure 3. Results during ULM processing: (a) B-mode image of the 200^th frame of block 150; (b) isolated signal of microbubbles after filtering from the 200^th frame of block 150; (c) localization of microbubble centers in the 300^th frame of block 150; (d) localization of microbubble centers in the 301^th frame of block 150.

DownLoad: Full-Size Img PowerPoint

图 4 超快超分辨率超声成像结果　(a) 脊髓血流密度图; (b) 脊髓血流方向图; (c) 脊髓血流速度图

Figure 4. ULM Results: (a) Intensity map of spinal cord; (b) direction map of spinal cord; (c) velocity map of spinal cord.

DownLoad: Full-Size Img PowerPoint

图 5 超快多普勒超声成像结果　(a) 功率多普勒血流图; (b) 彩色多普勒血流图

Figure 5. Results of ultrafast Doppler imaging: (a) Power Doppler; (b) color Doppler.

DownLoad: Full-Size Img PowerPoint

图 6 微泡定位统计　(a) 瞬时微泡数量; (b) 累计微泡数量; (c) 饱和度随时间变化图曲线

Figure 6. Quantification of microbubble localization: (a) Instantaneous detections; (b) accumulated detections; (c) saturation curve along time.

DownLoad: Full-Size Img PowerPoint

图 7 超快多普勒与超快超分辨率超声成像结果分辨率测算　(a) 脊髓超快功率多普勒血流局部放大图; (b) 图(a)中部分血管剖面FWHM结果; (c) 脊髓超分辨率血流密度局部放大图; (d) 图(c)中部分血管剖面FWHM结果; (e) 脊髓超分辨率血流方向局部图; (f) 超分辨率血流密度图基于FRC的分辨率结果

Figure 7. Resolution measurements of ultrafast Doppler imaging and ULM: (a) Zoom in of power Doppler; (b) FWHM of vessels from panel (a); (c) zoom in of ULM intensity map; (d) FWHM of vessels from panel (c); (e) zoom in of ULM direction map; (f) resolution of ULM intensity map based on FRC curve.

DownLoad: Full-Size Img PowerPoint

表 1 ULM参数统计结果

Table 1. Results of ULM parameter measurement.

参数	值
微泡保留比例/%	14.7
半高全宽/μm	28—50
轨迹保留比例/%	1.7
传统定义分辨率/μm	28
饱和度/%	32
FRC分辨率 –2$ \sigma $/μm	13
血流速度/(mm·s^–1)	1—50
FRC分辨率 –1/2 bit/μm	16

DownLoad: CSV

[1]	Kwon B K, Tetzlaff W, Grauer J N, Beiner J, Vaccaro A R 2004 Spine J. 4 451 Google Scholar
[2]	Ahuja C S, Wilson J R, Nori S, Kotter M R N, Druschel C, Curt A, Fehlings M G 2017 Nat. Rev. Dis. Primers 3 17018 Google Scholar
[3]	Fawcett J W, Schwab M E, Montani L, Brazda N, Muller H W 2012 Handb. Clin. Neurol. 109 503
[4]	Ruedinger K L, Schafer S, Speidel M A, Strother C M 2021 AJNR Am. J. Neuroradiol. 42 214 Google Scholar
[5]	Vargas M I, Bing F, Gariani J, Dietemann J L 2016 Neurovascular Imaging (New York: Springer) pp. 1063-1093
[6]	Tanter M, Fink M 2014 IEEE Trans. Ultrason. Ferroelectr. Freq. Control 61 102 Google Scholar
[7]	Betzig E, Patterson G H, Sougrat R, Lindwasser O W, Olenych S, Bonifacino J S, Davidson M W, Lippincott-Schwartz J H, Hess H F 2006 Science 313 1642 Google Scholar
[8]	Couture O, Besson B, Montaldo G, Fink M, Tanter M 2011 IEEE International Ultrasonics Symposium (IUS) Caribe Royale, Orlando, Florida, USA, October 18–21, 2011, p1285
[9]	钟传钰, 郑元义 2021 中国医学影像技术 37 1799 Google Scholar Zhong C, Zheng Y 2021 Chin. J. Med. Imaging Technol. 37 1799 Google Scholar
[10]	Couture O, Hingot V, Heiles B, Muleki-Seya P, Tanter M 2018 IEEE Trans. Ultrason. Ferroelectr. Freq. Control 65 1304 Google Scholar
[11]	Errico C, Pierre J, Pezet S, Desailly Y, Lenkei Z, Couture O, Tanter M 2015 Nature 527 499 Google Scholar
[12]	Christensen-Jeffries K, Browning R J, Tang M X, Dunsby C, Eckersley R J 2015 IEEE Trans. Med. Imaging 34 433 Google Scholar
[13]	Opacic T, Dencks S, Theek B, Piepenbrock M, Ackermann D, Rix A, Lammers T, Stickeler E, Delorme S, Schmitz G, Kiessling F 2018 Nat. Commun. 9 1527 Google Scholar
[14]	Andersen S B, Taghavi I, Hoyos C A V, Sogaard S B, Gran F, Lonn L, Hansen K L, Jensen J A, Nielsen M B, Sorensen C M 2020 Diagnostics 10 862
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[16]	Zhu J, Rowland E M, Harput S, Riemer K, Leow C H, Clark B, Cox K, Lim A, Christensen-Jeffries K, Zhang G, Brown J, Dunsby C, Eckersley R J, Weinberg P D, Tang M X 2019 Radiology 291 642 Google Scholar
[17]	Qian X, Huang C, Li R, Song B, Tchelepi H, Shung K K, Chen S, Humayun M, Zhou Q 2021 IEEE Trans. Biomed. Eng. 69 1585
[18]	Song P, Manduca A, Trzasko J D, Daigle R E, Chen S 2018 IEEE Trans. Ultrason. Ferroelectr. Freq. Control 65 2264 Google Scholar
[19]	Hingot V, Errico C, Heiles B, Rahal L, Tanter M, Couture O 2019 Sci. Rep. 9 2456 Google Scholar
[20]	Hingot V, Chavignon A, Heiles B, Couture O 2021 IEEE Trans. Med. Imaging 40 3812 Google Scholar
[21]	Liu X, Zhou T, Lu M, Yang Y, He Q, Luo J 2020 IEEE Trans. Med. Imaging 39 3064 Google Scholar
[22]	Xu K, Guo X, Sui Y, Hingot V, Couture O, Ta D, Wang W 2021 IEEE International Ultrasonics Symposium (IUS) Xi’an, China, September 11–16, 2021 p1
[23]	Soloukey S, Vincent A, Satoer D D, Mastik F, Smits M, Dirven C M F, Strydis C, Bosch J G, van der Steen A F W, De Zeeuw C I, Koekkoek S K E, Kruizinga P 2019 Front. Neurosci. 13 1384 Google Scholar
[24]	Khaing Z Z, Cates L N, DeWees D M, Hannah A, Mourad P, Bruce M, Hofstetter C P 2018 J. Neurosurg. Spine 29 306 Google Scholar
[25]	臧佳琦,许凯亮,韩清见,陆起涌,梅永丰,他得安 2021 物理学报 70 114304 Google Scholar Zang J Q, Xu K L, Han Q J, Lu Q Y, Mei Y F, Ta D A 2021 Acta Phys. Sin. 70 114304 Google Scholar
[26]	Sui Y, Yan S, Zang J, Liu X, Ta D, Wang W, Xu K 2021 IEEE International Ultrasonics Symposium (IUS) Xi’an, China, September 11–16, 2021 p1
[27]	Pezet S, Beliard B, Ahmanna C, Tiran E, Kanté K, Deffieux T, Tanter M, Nothias F, Soares S 2022 Sci. Rep. 12 6574
[28]	Desailly Y, Tissier A M, Correas J M, Wintzenrieth F, Tanter M, Couture O 2017 Phys. Med. Biol. 62 31 Google Scholar
[29]	Hingot V, Errico C, Tanter M, Couture O 2017 Ultrasonics 77 17 Google Scholar
[30]	Candès E J, Li X, Ma Y, Wright J 2011 J. ACM 58 1
[31]	Bayat M, Fatemi M 2018 IEEE International Conference on Acoustics, Speech and Signal Processing (ICASSP) Calgary, AB, Canada, April 15–20, 2018 p1080
[32]	Boyd S 2010 Foundations and Trends® in Machine Learning 3 1 Google Scholar
[33]	Christensen-Jeffries K, Couture O, Dayton P A, Eldar Y C, Hynynen K, Kiessling F, O'Reilly M, Pinton G F, Schmitz G, Tang M X, Tanter M, van Sloun R J G 2020 Ultrasound Med. Biol. 46 865 Google Scholar
[34]	Heiles B, Correia M, Hingot V, Pernot M, Provost J, Tanter M, Couture O 2019 IEEE Trans. Med. Imaging 38 2005 Google Scholar
[35]	Nieuwenhuizen R P, Lidke K A, Bates M, Puig D L, Grunwald D, Stallinga S, Rieger B 2013 Nat. Methods 10 557 Google Scholar
[36]	Banterle N, Bui K H, Lemke E A, Beck M 2013 J. Struct. Biol. 183 363 Google Scholar
[37]	Viessmann O M, Eckersley R J, Christensen-Jeffries K, Tang M X, Dunsby C 2013 Phys. Med. Biol. 58 6447 Google Scholar
[38]	Tang J, Kilic K, Szabo T L, Boas D A 2021 IEEE Trans. Med. Imaging 40 758 Google Scholar
[39]	Bar-Zion A, Solomon O, Tremblay-Darveau C, Adam D, Eldar Y C 2018 IEEE Trans. Ultrason. Ferroelectr. Freq. Control 65 2365 Google Scholar
[40]	Milecki L, Poree J, Belgharbi H, Bourquin C, Damseh R, Delafontaine-Martel P, Lesage F, Gasse M, Provost J 2021 IEEE Trans. Med. Imaging 40 1428 Google Scholar
[41]	van Sloun R J G, Solomon O, Bruce M, Khaing Z Z, Wijkstra H, Eldar Y C, Mischi M 2021 IEEE Trans. Med. Imaging 40 829 Google Scholar
[42]	Guasch L, Calderon Agudo O, Tang M X, Nachev P, Warner M 2020 NPJ Digit. Med. 3 28 Google Scholar
[43]	李云清, 江晨, 李颖, 徐峰, 许凯亮, 他得安, 黎仲勋 2019 物理学报 68 184302 Google Scholar Li Y Q, Jiang C, Li Y, Xu F, Xu K L, Ta D A, Le L H 2019 Acta Phys. Sin. 68 184302 Google Scholar
[44]	Jiang C, Li Y, Xu K, Ta D 2021 IEEE Trans. Ultrason. Ferroelectr. Freq. Control 68 72 Google Scholar

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Vol. 71, Issue 17 - 2022-09-05

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