Transcranial ultrafast ultrasound localization microscopy of brain vasculature in patients.
Journal
Nature biomedical engineering
ISSN: 2157-846X
Titre abrégé: Nat Biomed Eng
Pays: England
ID NLM: 101696896
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
20
05
2020
accepted:
05
02
2021
pubmed:
17
3
2021
medline:
13
4
2021
entrez:
16
3
2021
Statut:
ppublish
Résumé
Changes in cerebral blood flow are associated with stroke, aneurysms, vascular cognitive impairment, neurodegenerative diseases and other pathologies. Brain angiograms, typically performed via computed tomography or magnetic resonance imaging, are limited to millimetre-scale resolution and are insensitive to blood-flow dynamics. Here we show that ultrafast ultrasound localization microscopy of intravenously injected microbubbles enables transcranial imaging of deep vasculature in the adult human brain at microscopic resolution and the quantification of haemodynamic parameters. Adaptive speckle tracking to correct for micrometric brain-motion artefacts and ultrasonic-wave aberrations induced during transcranial propagation allowed us to map the vascular network of tangled arteries to functionally characterize blood-flow dynamics at a resolution of up to 25 μm and to detect blood vortices in a small deep-seated aneurysm in a patient. Ultrafast ultrasound localization microscopy may facilitate the understanding of brain haemodynamics and of how vascular abnormalities in the brain are related to neurological pathologies.
Identifiants
pubmed: 33723412
doi: 10.1038/s41551-021-00697-x
pii: 10.1038/s41551-021-00697-x
pmc: PMC7610356
mid: EMS115989
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
219-228Subventions
Organisme : Swiss National Science Foundation
ID : 159654
Pays : Switzerland
Organisme : European Research Council
ID : 339244
Pays : International
Commentaires et corrections
Type : CommentIn
Références
Liesz, A. The vascular side of Alzheimer’s disease. Science 365, 223–224 (2019).
doi: 10.1126/science.aay2720
O’Brien, J. T. & Thomas, A. Vascular dementia. Lancet 386, 1698–1706 (2015).
doi: 10.1016/S0140-6736(15)00463-8
Betzig, E. et al. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642–1645 (2006).
doi: 10.1126/science.1127344
Rust, M. J., Bates, M. & Zhuang, X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3, 793–796 (2006).
doi: 10.1038/nmeth929
Errico, C. et al. Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging. Nature 527, 499–502 (2015).
doi: 10.1038/nature16066
Couture, O., Hingot, V., Heiles, B., Muleki-Seya, P. & Tanter, M. Ultrasound localization microscopy and super-resolution: a state of the art. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 65, 1304–1320 (2018).
doi: 10.1109/TUFFC.2018.2850811
Couture, O., Besson, B., Montaldo, G., Fink, M. & Tanter, M. Microbubble ultrasound super-localization imaging (MUSLI). In 2011 IEEE International Ultrasonics Symposium https://doi.org/10.1109/ULTSYM.2011.6293576 (IEEE, 2011).
Viessmann, O. M., Eckersley, R. J., Christensen-Jeffries, K., Tang, M. X. & Dunsby, C. Acoustic super-resolution with ultrasound and microbubbles. Phys. Med. Biol. 58, 6447–6458 (2013).
doi: 10.1088/0031-9155/58/18/6447
Siepmann, M., Schmitz, G., Bzyl, J., Palmowski, M. & Kiessling, F. Imaging tumor vascularity by tracing single microbubbles. In 2011 IEEE International Ultrasonics Symposium https://doi.org/10.1109/ULTSYM.2011.0476 (IEEE, 2011).
Demené, C. et al. Ultrafast Doppler reveals the mapping of cerebral vascular resistivity in neonates. J. Cereb. Blood Flow. Metab. https://doi.org/10.1038/jcbfm.2014.49 (2014).
Demene, C. et al. Functional ultrasound imaging of brain activity in human newborns. Sci. Transl. Med. 9, eaah6756 (2017).
doi: 10.1126/scitranslmed.aah6756
Demené, C., Mairesse, J., Baranger, J., Tanter, M. & Baud, O. Ultrafast Doppler for neonatal brain imaging. NeuroImage 185, 851–856 (2019).
doi: 10.1016/j.neuroimage.2018.04.016
Imbault, M., Chauvet, D., Gennisson, J.-L., Capelle, L. & Tanter, M. Intraoperative functional ultrasound imaging of human brain activity. Sci. Rep. 7, 7304 (2017).
doi: 10.1038/s41598-017-06474-8
Soloukey, S. et al. Functional ultrasound (fUS) during awake brain surgery: the clinical potential of intra-operative functional and vascular brain mapping. Front. Neurosci. 13, 1384 (2020).
doi: 10.3389/fnins.2019.01384
Bamber, J. C. in Physical Principles of Medical Ultrasonics (eds Hill, C. R. et al.) 93–166 (Wiley, 2005).
Tanter, M., Thomas, J.-L. & Fink, M. Time reversal and the inverse filter. J. Acoust. Soc. Am. 108, 223–234 (2000).
doi: 10.1121/1.429459
Zhu, Q. & Steinberg, B. D. Large-transducer measurements of wavefront distortion in the female breast. Ultrason. Imaging 14, 276–299 (1992).
doi: 10.1177/016173469201400304
Anderson, M. E., McKeag, M. S. & Trahey, G. E. The impact of sound speed errors on medical ultrasound imaging. J. Acoust. Soc. Am. 107, 3540–3548 (2000).
doi: 10.1121/1.429422
Fry, F. J. & Barger, J. E. Acoustical properties of the human skull. J. Acoust. Soc. Am. 63, 1576–1590 (1978).
doi: 10.1121/1.381852
Schneider, M. Characteristics of SonoVue
doi: 10.1111/j.1540-8175.1999.tb00144.x
Tanter, M. & Fink, M. Ultrafast imaging in biomedical ultrasound. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 61, 102–119 (2014).
doi: 10.1109/TUFFC.2014.2882
Papadacci, C., Pernot, M., Couade, M., Fink, M. & Tanter, M. High-contrast ultrafast imaging of the heart. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 61, 288–301 (2014).
doi: 10.1109/TUFFC.2014.6722614
Demene, C. et al. Spatiotemporal clutter filtering of ultrafast ultrasound data highly increases Doppler and fUltrasound sensitivity. IEEE Trans. Med. Imaging 34, 2271–2285 (2015).
doi: 10.1109/TMI.2015.2428634
Flax, S. W. & O’Donnell, M. Phase-aberration correction using signals from point reflectors and diffuse scatterers: basic principles. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 35, 758–767 (1988).
doi: 10.1109/58.9333
Prada, C., Wu, F. & Fink, M. The iterative time reversal mirror: a solution to self‐focusing in the pulse echo mode. J. Acoust. Soc. Am. 90, 1119–1129 (1991).
doi: 10.1121/1.402301
Tinevez, J.-Y. A simple particle tracking algorithm for MATLAB that can deal with gaps: tinevez/simpletracker (MathWorks, 2019).
Szabo, T. L. Diagnostic Ultrasound Imaging: Inside Out 2nd edn (Elsevier, 2014).
Paszkowiak, J. J. & Dardik, A. Arterial wall shear stress: observations from the bench to the bedside. Vasc. Endovascular Surg. https://doi.org/10.1177/153857440303700107 (2003).
Febina, J., Sikkandar, M. Y. & Sudharsan, N. M. Wall shear stress estimation of thoracic aortic aneurysm using computational fluid dynamics. Comput. Math. Methods Med. 2018, 7126532 (2018).
doi: 10.1155/2018/7126532
Goudot, G. et al. Wall shear stress measurement by ultrafast vector flow imaging for atherosclerotic carotid stenosis. Ultraschall Med. https://doi.org/10.1055/a-1060-0529 (2019).
Scott, R. M. & Smith, E. R. Moyamoya disease and Moyamoya syndrome. N. Engl. J. Med. 360, 1226–1237 (2009).
doi: 10.1056/NEJMra0804622
Lee, C.-H., Jeon, S.-H., Wang, S.-J., Shin, B.-S. & Kang, H. G. Factors associated with temporal window failure in transcranial Doppler sonography. Neurol. Sci. 41, 3293–3299 (2020).
doi: 10.1007/s10072-020-04459-6
Heiles, B. et al. Ultrafast 3D ultrasound localization microscopy using a 32 × 32 matrix array. IEEE Trans. Med. Imaging https://doi.org/10.1109/TMI.2018.2890358 (2019).
Morel, D. Human pharmacokinetics and safety evaluation of SonoVue, a new contrast agent for ultrasound imaging. Invest. Radiol. 35, 80–85 (2000).
doi: 10.1097/00004424-200001000-00009
Martin, K. The acoustic safety of new ultrasound technologies. Ultrasound 18, 110–118 (2010).
doi: 10.1258/ult.2010.010024
Bigelow, T. A. et al. The thermal index. J. Ultrasound Med. 30, 714–734 (2011).
doi: 10.7863/jum.2011.30.5.714
Gateau, J. et al. Transcranial ultrasonic therapy based on time reversal of acoustically induced cavitation bubble signature. IEEE Trans. Biomed. Eng. 57, 134–144 (2010).
doi: 10.1109/TBME.2009.2031816
O’Reilly, M. A. & Hynynen, K. A super-resolution ultrasound method for brain vascular mapping. Med. Phys. 40, 110701 (2013).
doi: 10.1118/1.4823762
Soulioti, D. E., Espíndola, D., Dayton, P. A. & Pinton, G. F. Super-resolution imaging through the human skull. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 67, 25–36 (2020).
doi: 10.1109/TUFFC.2019.2937733
Kasai, C., Namekawa, K., Koyano, A. & Omoto, R. Real-time two-dimensional blood flow imaging using an autocorrelation technique. IEEE Trans. Sonics Ultrason. 32, 458–464 (1985).
doi: 10.1109/T-SU.1985.31615
Bercoff, J., Tanter, M. & Fink, M. Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51, 396–409 (2004).
doi: 10.1109/TUFFC.2004.1295425
Jerman, T., Pernuš, F., Likar, B. & Špiclin, Ž. Enhancement of vascular structures in 3D and 2D angiographic images. IEEE Trans. Med. Imaging 35, 2107–2118 (2016).
doi: 10.1109/TMI.2016.2550102
Jerman, T., Pernuš, F., Likar, B. & Špiclin, Ž. Beyond Frangi: an improved multiscale vesselness filter. Proc. SPIE 9413, 94132A (2015).
Frangi, A. F., Niessen, W. J., Hoogeveen, R. M., Van Walsum, T. & Viergever, M. A. Model-based quantitation of 3-D magnetic resonance angiographic images. IEEE Trans. Med. Imaging 18, 946–956 (1999).
doi: 10.1109/42.811279
Hingot, V. et al. Microvascular flow dictates the compromise between spatial resolution and acquisition time in ultrasound localization microscopy. Sci. Rep. 9, 2456 (2019).
doi: 10.1038/s41598-018-38349-x
Errico, C. et al. Transcranial functional ultrasound imaging of the brain using microbubble-enhanced ultrasensitive Doppler. NeuroImage 124, 752–761 (2016).
doi: 10.1016/j.neuroimage.2015.09.037