Cited by 144Ultrasound and Hyperthermia ApplicationsBarrier Structure and Function StudiesDrug Transport and Resistance Mechanisms

Applications of focused ultrasound-mediated blood-brain barrier opening

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Gorick, Catherine M., Breza, Victoria R., Nowak, Katherine M., Cheng, Vinton W.T., Fisher, Delaney G., Debski, Anna C., Hoch, Matthew R., Demir, Zehra E.F. +4 more·2022·Advanced Drug Delivery Reviews

Abstract

The blood brain barrier (BBB) plays a critically important role in the regulation of central nervous system (CNS) homeostasis, but also represents a major limitation to treatments of brain pathologies. In recent years, focused ultrasound (FUS) in conjunction with gas-filled microbubble contrast agents has emerged as a powerful tool for transiently and non-invasively disrupting the BBB in a targeted and image-guided manner, allowing for localized delivery of drugs, genes, or other therapeutic agents. Beyond the delivery of known therapeutics, FUS-mediated BBB opening also demonstrates the potential for use in neuromodulation and the stimulation of a range of cell- and tissue-level physiological responses that may prove beneficial in disease contexts. Clinical trials investigating the safety and efficacy of FUS-mediated BBB opening are well underway, and offer promising non-surgical approaches to treatment of devastating pathologies. This article reviews a range of pre-clinical and clinical studies demonstrating the tremendous potential of FUS to fundamentally change the paradigm of treatment for CNS diseases.

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  • Gas-filled microbubbles with ultrasound open BBB in image-guided and targeted manner, ensuring local drug delivery.

    “gas-filled microbubble has emerged as a contrast agent in conjunction with ultrasound for opening the BBB in an image-guided and targeted manner, ensuring the local delivery of drugs.”

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  1. [1]Daneman R, Prat A, The Blood-Brain Barrier, Cold Spring Harb. Perspect. Biol 7 (1) (2015) a020412. 25561720 PMC4292164
  2. [2]Fu BM, Transport Across the Blood-Brain Barrier, in: 2018: pp. 235– 259. 10.1007/978-3-319-96445-4_13. 30315549 · DOI
  3. [3]Wolburg H, Lippoldt A, Tight junctions of the blood–brain barrier, Vascul. Pharmacol 38 (2002) 323– 337, 10.1016/S1537-1891(02)00200-8. 12529927 · DOI
  4. [4]Segarra M, Aburto MR, Acker-Palmer A, Blood-Brain Barrier Dynamics to Maintain Brain Homeostasis, Trends Neurosci. 44 (2021) 393– 405, 10.1016/j.tins.2020.12.002. 33423792 · DOI
  5. [5]Abbott NJ, Patabendige AAK, Dolman DEM, Yusof SR, Begley DJ, Structure and function of the blood–brain barrier, Neurobiol. Dis 37 (2010) 13– 25, 10.1016/j.nbd.2009.07.030. 19664713 · DOI · Paper page
  6. [6]Armulik A, Genové G, Mäe M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C, Pericytes regulate the blood–brain barrier, Nature. 468 (2010) 557– 561, 10.1038/nature09522. 20944627 · DOI · Paper page
  7. [7]Pardridge WM, The blood-brain barrier: Bottleneck in brain drug development, NeuroRX. 2 (2005) 3– 14, 10.1602/neurorx.2.1.3. 15717053 PMC539316 · DOI · Paper page
  8. [8]Löscher W, Potschka H, Blood-brain barrier active efflux transporters: ATP-binding cassette gene family, NeuroRX. 2 (2005) 86– 98, 10.1602/neurorx.2.1.86. 15717060 PMC539326 · DOI
  9. [9]Bosma EK, van Noorden CJF, Schlingemann RO, Klaassen I, The role of plasmalemma vesicle-associated protein in pathological breakdown of blood–brain and blood–retinal barriers: potential novel therapeutic target for cerebral edema and diabetic macular edema, Fluids Barriers CNS. 15 (2018) 24, 10.1186/s12987-018-0109-2. 30231925 PMC6146740 · DOI
  10. [10]Sheikov N, McDannold N, Vykhodtseva N, Jolesz F, Hynynen K, Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles, Ultrasound Med. Biol 30 (2004) 979– 989, 10.1016/j.ultrasmedbio.2004.04.010. 15313330 · DOI
  11. [11]Timbie KF, Mead BP, Price RJ, Drug and gene delivery across the blood–brain barrier with focused ultrasound, J. Control. Release 219 (2015) 61– 75, 10.1016/j.jconrel.2015.08.059. 26362698 PMC4656107 · DOI
  12. [12]Song K-H, Harvey BK, Borden MA, State-of-the-art of microbubble-assisted blood-brain barrier disruption, Theranostics. 8 (2018) 4393– 4408, 10.7150/thno.26869. 30214628 PMC6134932 · DOI
  13. [13]Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA, Noninvasive MR Imaging–guided Focal Opening of the Blood-Brain Barrier in Rabbits, Radiology. 220 (2001) 640– 646, 10.1148/radiol.2202001804. 11526261 · DOI
  14. [14]Çavuşoğlu M, Zhang J, Ielacqua GD, Pellegrini G, Signorell RD, Papachristodoulou A, Brambilla D, Roth P, Weller M, Rudin M, Martin E, Leroux JC, Werner B, Closed-loop cavitation control for focused ultrasound-mediated blood–brain barrier opening by long-circulating microbubbles, Phys. Med. Biol, 64 (2019), 10.1088/1361-6560/aafaa5. 30577029 · DOI
  15. [15]McDannold N, Arvanitis CD, Vykhodtseva N, Livingstone MS, Temporary Disruption of the Blood–Brain Barrier by Use of Ultrasound and Microbubbles: Safety and Efficacy Evaluation in Rhesus Macaques, Cancer Res. 72 (2012) 3652– 3663. 10.1158/0008-5472.CAN-12-0128. 22552291 PMC3533365 · DOI
  16. [16]Gray M, Vasilyeva AV, Brans V, Stride E, Studying Cavitation Enhanced Therapy, J. Vis. Exp (170) (2021), 10.3791/61989. 33900296 · DOI
  17. [17]Rabut C, Yoo S, Hurt RC, Jin Z, Li H, Guo H, Ling B, Shapiro MG, Ultrasound Technologies for Imaging and Modulating Neural Activity, Neuron. 108 (2020) 93– 110, 10.1016/j.neuron.2020.09.003. 33058769 PMC7577369 · DOI
  18. [19]Wu S-Y, Sanchez CS, Samiotaki G, Buch A, Ferrera VP, Konofagou EE, Characterizing Focused-Ultrasound Mediated Drug Delivery to the Heterogeneous Primate Brain In Vivo with Acoustic Monitoring, Sci. Rep 6 (2016) 37094, 10.1038/srep37094. 27853267 PMC5112571 · DOI
  19. [20]Pouliopoulos AN, Kwon N, Jensen G, Meaney A, Niimi Y, Burgess MT, Ji R, McLuckie AJ, Munoz FA, Kamimura HAS, Teich AF, Ferrera VP, Konofagou EE, Safety evaluation of a clinical focused ultrasound system for neuronavigation guided blood-brain barrier opening in non-human primates, Sci. Rep 11 (2021) 15043, 10.1038/s41598-021-94188-3. 34294761 PMC8298475 · DOI
  20. [21]Chen KT, Chai WY, Lin YJ, Lin CJ, Chen PY, Tsai HC, Huang CY, Kuo JS, Liu HL, Wei KC, Neuronavigation-guided focused ultrasound for transcranial blood-brain barrier opening and immunostimulation in brain tumors, Sci. Adv 7 (2021), 10.1126/SCIADV.ABD0772. PMC7864566 33547073 · DOI
  21. [22]Konofagou EE, Tunga Y-S, Choia J, Deffieuxa T, Baseria B, Vlachosa F, Ultrasound-Induced Blood-Brain Barrier Opening, Curr. Pharm. Biotechnol 13 (2012) 1332, 10.2174/138920112800624364. 22201586 PMC4038976 · DOI
  22. [23]Chen W, Hu Y, Ju D, Gene therapy for neurodegenerative disorders: advances, insights and prospects, Acta Pharm. Sin. B 10 (8) (2020) 1347– 1359. 32963936 PMC7488363
  23. [24]Ebrahimi Z, Talaei S, Aghamiri S, Goradel NH, Jafarpour A, Negahdari B, Overcoming the blood–brain barrier in neurodegenerative disorders and brain tumours, IET Nanobiotechnology. 14 (2020) 441– 448, 10.1049/IET-NBT.2019.0351. 32755952 PMC8676526 · DOI
  24. [26]Hooper C, Killick R, Lovestone S, The GSK3 hypothesis of Alzheimer’s disease, J. Neurochem 104 (2008) 1433, 10.1111/J.1471-4159.2007.05194.X. 18088381 PMC3073119 · DOI · Paper page
  25. [27]Hsu P-H, Lin Y-T, Chung Y-H, Lin K-J, Yang L-Y, Yen T-C, Liu H-L, Focused Ultrasound-Induced Blood-Brain Barrier Opening Enhances GSK-3 Inhibitor Delivery for Amyloid-Beta Plaque Reduction, Sci Rep 8 (1) (2018). PMC6110796 30150769
  26. [28]Xhima K, Markham-Coultes K, Nedev H, Heinen S, Saragovi HU, Hynynen K, Aubert I, Focused ultrasound delivery of a selective TrkA agonist rescues cholinergic function in a mouse model of Alzheimer’s disease, Sci. Adv 6 (2020), 10.1126/SCIADV.AAX6646/SUPPL_FILE/AAX6646_SM.PDF. PMC6976301 32010781 · DOI
  27. [29]K X, K M-C, RH K, HU S, K H, I A, Ultrasound delivery of a TrkA agonist confers neuroprotection to Alzheimer-associated pathologies, Brain. 139 (2021) 16– 17. 10.1093/BRAIN/AWAB460. PMC9420023 34919633 · DOI · Paper page
  28. [30]Dubey S, Heinen S, Krantic S, JoAnne McLaurin DR, Branch K, Hynynen IA, Clinically approved IVIg delivered to the hippocampus with focused ultrasound promotes neurogenesis in a model of Alzheimer’s disease, Proc. Natl. Acad. Sci. U. S. A 117 (2020) 32691– 32700, 10.1073/PNAS.1908658117/-/DCSUPPLEMENTAL. 33288687 PMC7768694 · DOI
  29. [31]Sun T, Shi Q, Zhang Y, Power C, Hoesch C, Antonelli S, Schroeder MK, Caldarone BJ, Taudte N, Schenk M, Hettmann T, Schilling S, McDannold NJ, Lemere CA, Focused ultrasound with anti-pGlu3 Aβ enhances efficacy in Alzheimer’s disease-like mice via recruitment of peripheral immune cells, J. Control. Release 336 (2021) 443– 456, 10.1016/J.JCONREL.2021.06.037. 34186148 PMC8373822 · DOI
  30. [33]Weber-Adrian D, Kofoed RH, Chan JWY, Silburt J, Noroozian Z, Kügler S, Hynynen K, Aubert I, Strategy to enhance transgene expression in proximity of amyloid plaques in a mouse model of Alzheimer’s disease, Theranostics. 9 (2019) 8127– 8137, 10.7150/THNO.36718. 31754385 PMC6857057 · DOI
  31. [34]Kofoed RH, Heinen S, Silburt J, Dubey S, Dibia CL, Maes M, Simpson EM, Hynynen K, Aubert I, Transgene distribution and immune response after ultrasound delivery of rAAV9 and PHP.B to the brain in a mouse model of amyloidosis, Mol. Ther. - Methods Clin. Dev 23 (2021) 390– 405, 10.1016/J.OMTM.2021.10.001. 34761053 PMC8560718 · DOI
  32. [36]Janowicz PW, Leinenga G, Götz J, Nisbet RM, Ultrasound-mediated blood-brain barrier opening enhances delivery of therapeutically relevant formats of a tau-specific antibody, Sci. Rep 9 (2019), 10.1038/s41598-019-45577-2. PMC6592925 31239479 · DOI
  33. [37]Xhima K, Nabbouh F, Hynynen K, Aubert I, Tandon A, Noninvasive delivery of an α-synuclein gene silencing vector with magnetic resonance-guided focused ultrasound, Mov. Disord 33 (2018) 1567– 1579, 10.1002/mds.101. 30264465 PMC6282171 · DOI
  34. [38]Lin CJ, Lin CY, Lin YT, Huang CY, Wei KC, Chen JC, Lee-Chen GJ, Liu HL, Microbubble-facilitated ultrasound pulsation promotes direct α-synuclein gene delivery, Biochem. Biophys. Res. Commun 517 (2019) 77– 83, 10.1016/J.BBRC.2019.07.017. 31327496 · DOI
  35. [39]Yan Y, Chen Y, Liu Z, Cai F, Niu W, Song L, Liang H, Su Z, Yu B, Yan F, Brain Delivery of Curcumin Through Low-Intensity Ultrasound-Induced Blood-Brain Barrier Opening via Lipid-PLGA Nanobubbles, Int. J. Nanomedicine 16 (2021) 7433– 7447, 10.2147/IJN.S327737. 34764649 PMC8575349 · DOI
  36. [40]Lin CY, Hsieh HY, Chen CM, Wu SR, Tsai CH, Huang CY, Hua MY, Wei KC, Yeh CK, Liu HL, Non-invasive, neuron-specific gene therapy by focused ultrasound-induced blood-brain barrier opening in Parkinson’s disease mouse model, J. Control. Release 235 (2016) 72– 81, 10.1016/j.jconrel.2016.05.052. 27235980 · DOI
  37. [41]Fan C-H, Ting C-Y, Lin C-Y, Chan H-L, Chang Y-C, Chen Y-Y, Liu H-L, Yeh CK, Noninvasive, Targeted and Non-Viral Ultrasound-Mediated GDNF-Plasmid Delivery for Treatment of Parkinson’s Disease, Sci Rep 6 (1) (2016). PMC4726227 26786201
  38. [42]Long L, Cai X, Guo R, Wang P, Wu L, Yin T, Liao S, Lu Z, Treatment of Parkinson’s disease in rats by Nrf2 transfection using MRI-guided focused ultrasound delivery of nanomicrobubbles, Biochem. Biophys. Res. Commun 482 (2017) 75– 80, 10.1016/J.BBRC.2016.10.141. 27810365 · DOI
  39. [43]Mead BP, Kim N, Miller GW, Hodges D, Mastorakos P, Klibanov AL, Mandell JW, Hirsh J, Suk JS, Hanes J, Price RJ, Novel Focused Ultrasound Gene Therapy Approach Noninvasively Restores Dopaminergic Neuron Function in a Rat Parkinson’s Disease Model, Nano Lett. 17 (2017) 3533– 3542, 10.1021/ACS.NANOLETT.7B00616/SUPPL_FILE/NL7B00616_SI_001.PDF. 28511006 PMC5539956 · DOI
  40. [44]Yue P, Miao W, Gao L, Zhao X, Teng J, Ultrasound-triggered effects of the microbubbles coupled to GDNF plasmid-loaded PEGylated liposomes in a rat model of Parkinson’s disease, Front. Neurosci 12 (2018) 222, 10.3389/FNINS.2018.00222/BIBTEX. 29686604 PMC5900787 · DOI
  41. [45]Wu CY, Huang RY, Liao EC, Lin YC, Ho YJ, Chang CW, Chan HL, Huang YZ, Hsieh TH, Fan CH, Yeh CK, A preliminary study of Parkinson’s gene therapy via sono-magnetic sensing gene vector for conquering extra/intracellular barriers in mice, Brain Stimul. 13 (2020) 786– 799, 10.1016/J.BRS.2020.02.024. 32289709 · DOI
  42. [46]Karakatsani ME, Wang S, Samiotaki G, Kugelman T, Olumolade OO, Acosta C, Sun T, Han Y, Kamimura HAS, Jackson-Lewis V, Przedborski S, Konofagou E, Amelioration of the nigrostriatal pathway facilitated by ultrasound-mediated neurotrophic delivery in early Parkinson’s disease, J. Control. Release 303 (2019) 289– 301, 10.1016/J.JCONREL.2019.03.030. 30953664 PMC6618306 · DOI
  43. [47]Ji R, Smith M, Niimi Y, Karakatsani ME, Murillo MF, Jackson-Lewis V, Przedborski S, Konofagou EE, Focused ultrasound enhanced intranasal delivery of brain derived neurotrophic factor produces neurorestorative effects in a Parkinson’s disease mouse model, Sci Rep 9 (1) (2019). PMC6920380 31852909
  44. [48]Chen H, Yang GZX, Getachew H, Acosta C, Sierra Sanchez C, Konofagou EE, Focused ultrasound-enhanced intranasal brain delivery of brain-derived neurotrophic factor, Sci Rep 6 (1) (2016). PMC4921840 27345430
  45. [49]Bunevicius A, McDannold NJ, Golby AJ, Focused Ultrasound Strategies for Brain Tumor Therapy, Oper. Neurosurg Operative Surg 19 (1) (2020) 9– 18. PMC7293897 31853548
  46. [50]Wu SK, Tsai CL, Huang Y, Hynynen K, Focused Ultrasound and Microbubbles-Mediated Drug Delivery to Brain Tumor, Pharmaceutics. 13 (2020) 1– 15, 10.3390/PHARMACEUTICS13010015. 33374205 PMC7823947 · DOI
  47. [51]Dréan A, Lemaire N, Bouchoux G, Goldwirt L, Canney M, Goli L, Bouzidi A, Schmitt C, Guehennec J, Verreault M, Sanson M, Delattre JY, Mokhtari K, Sottilini F, Carpentier A, Idbaih A, Temporary blood-brain barrier disruption by low intensity pulsed ultrasound increases carboplatin delivery and efficacy in preclinical models of glioblastoma, J. Neurooncol 144 (2019) 33– 41, 10.1007/S11060-019-03204-0. 31197598 · DOI
  48. [52]Wei H-J, Upadhyayula PS, Pouliopoulos AN, Englander ZK, Zhang X, Jan C-I, Guo J, Mela A, Zhang Z, Wang TJC, Bruce JN, Canoll PD, Feldstein NA, Zacharoulis S, Konofagou EE, Wu C-C, Focused Ultrasound-Mediated Blood-Brain Barrier Opening Increases Delivery and Efficacy of Etoposide for Glioblastoma Treatment, Int. J. Radiat. Oncol 110 (2021) 539– 550, 10.1016/j.ijrobp.2020.12.019. PMC8553628 33346092 · DOI
  49. [53]Rallis KS, Yau THL, Sideris M, Chemoradiotherapy in Cancer Treatment: Rationale and Clinical Applications, Anticancer Res. 41 (2021) 1– 7, 10.21873/ANTICANRES.14746. 33419794 · DOI
  50. [54]Song Z, Huang X, Wang J, Cai F, Zhao P, Yan F, Targeted Delivery of Liposomal Temozolomide Enhanced Anti-Glioblastoma Efficacy through Ultrasound-Mediated Blood-Brain Barrier Opening, Pharmaceutics. 13 (2021) 1270, 10.3390/pharmaceutics13081270. 34452234 PMC8401148 · DOI
  51. [55]Zhang DY, Dmello C, Chen L, Arrieta VA, Gonzalez-Buendia E, Robert Kane J, Magnusson LP, Baran A, David James C, Horbinski C, Carpentier A, Desseaux C, Canney M, Muzzio M, Stupp R, Sonabend AM, Ultrasound-mediated Delivery of Paclitaxel for Glioma: A Comparative Study of Distribution, Toxicity, and Efficacy of Albumin-bound Versus Cremophor Formulations, Clin. Cancer Res 26 (2020) 477– 486. 10.1158/1078-0432.CCR-19-2182. 31831565 PMC7050644 · DOI
  52. [56]Curley CT, Mead BP, Negron K, Kim N, Garrison WJ, Wilson Miller G, Kingsmore KM, Andrew Thim E, Song J, Munson JM, Klibanov AL, Suk JS, Hanes J, Price RJ, Augmentation of brain tumor interstitial flow via focused ultrasound promotes brain-penetrating nanoparticle dispersion and transfection, Sci. Adv 6 (2020) aay1344, 10.1126/sciadv.aay1344. PMC7195188 32494662 · DOI
  53. [57]Yang Q, Zhou Y, Chen J, Huang N, Wang Z, Cheng Y, Gene Therapy for Drug- Resistant Glioblastoma via Lipid-Polymer Hybrid Nanoparticles Combined with Focused Ultrasound, Int. J. Nanomedicine 16 (2021) 185– 199, 10.2147/IJN.S286221. 33447034 PMC7802796 · DOI
  54. [58]Fan C-H, Wang T-W, Hsieh Y-K, Wang C-F, Gao Z, Kim A, Nagasaki Y, Yeh C-K, Enhancing Boron Uptake in Brain Glioma by a Boron-Polymer/Microbubble Complex with Focused Ultrasound, ACS Appl. Mater. Interfaces 11 (2019) 11144– 11156, 10.1021/acsami.8b22468. 30883079 · DOI
  55. [59]White PJ, Zhang YZ, Power C, Vykhodtseva N, McDannold N, Observed Effects of Whole-Brain Radiation Therapy on Focused Ultrasound Blood-Brain Barrier Disruption, Ultrasound Med. Biol 46 (2020) 1998– 2006, 10.1016/J.ULTRASMEDBIO.2020.04.013. 32451192 PMC7329597 · DOI
  56. [60]Sheybani ND, Breza VR, Paul S, McCauley KS, Berr SS, Miller GW, Neumann KD, Price RJ, ImmunoPET-informed sequence for focused ultrasound-targeted mCD47 blockade controls glioma, J. Control. Release 331 (2021) 19– 29, 10.1016/j.jconrel.2021.01.023. 33476735 PMC7946780 · DOI
  57. [61]Brighi C, Reid L, White AL, Genovesi LA, Kojic M, Millar A, Bruce Z, Day BW, Rose S, Whittaker AK, Puttick S, MR-guided focused ultrasound increases antibody delivery to nonenhancing high-grade glioma, Neuro-Oncology Adv. 2 (2020), 10.1093/noajnl/vdaa030. PMC7212871 32642689 · DOI
  58. [62]Zhu L, Nazeri A, Pacia CP, Yue Y, Chen H, Sherman JH, Focused ultrasound for safe and effective release of brain tumor biomarkers into the peripheral circulation, PLoS One. 15 (6) (2020) e0234182. 32492056 PMC7269259
  59. [63]Zhu L, Cheng G, Ye D, Nazeri A, Yue Y, Liu W, Wang X, Dunn GP, Petti AA, Leuthardt EC, Chen H, Focused Ultrasound-enabled Brain Tumor Liquid Biopsy, Sci. Rep 8 (2018) 6553, 10.1038/s41598-018-24516-7. 29700310 PMC5919906 · DOI
  60. [64]Pacia CP, Zhu L, Yang Y, Yue Y, Nazeri A, Michael Gach H, Talcott MR, Leuthardt EC, Chen H, Feasibility and safety of focused ultrasound-enabled liquid biopsy in the brain of a porcine model, Sci Rep 10 (1) (2020). PMC7198482 32366915
  61. [65]Zhang Y, Buckmaster PS, Qiu L, Wang J, Keunen O, Ghobadi SN, Huang A, Hou Q, Li N, Narang S, Habte FG, Bertram EH, Lee KS, Wintermark M, Non-invasive, neurotoxic surgery reduces seizures in a rat model of temporal lobe epilepsy, Exp. Neurol, 343(2021), 10.1016/J.EXPNEUROL.2021.113761. PMC8937852 33991523 · DOI
  62. [66]Zhang Y, Liao C, Qu H, Huang S, Jiang H, Zhou H, Abrams E, Habte FG, Yuan L, Bertram EH, Lee KS, Pauly KB, Buckmaster PS, Wintermark M, Testing Different Combinations of Acoustic Pressure and Doses of Quinolinic Acid for Induction of Focal Neuron Loss in Mice Using Transcranial Low-Intensity Focused Ultrasound, Ultrasound Med. Biol 45 (2019) 129– 136, 10.1016/J.ULTRASMEDBIO.2018.08.023. 30309748 PMC6289648 · DOI
  63. [67]Wang Y, Anzivino MJ, Zhang Y, Bertram EH, Woznak J, Klibanov AL, Dumont E, Wintermark M, Lee KS, Noninvasive disconnection of targeted neuronal circuitry sparing axons of passage and nonneuronal cells, J. Neurosurg (2021) 1– 11, 10.3171/2021.7.JNS21123. PMC9117563 34798617 · DOI
  64. [68]Wang F, Li N, Wei X, Jia X, Liu H, Wang Y, Shi Y, Pan M, Wang Y, Yin Y, Yan F, Chen Y, MRI-Guided Focused Ultrasound-Induced Blood Brain Barrier Disruption to Deliver Glial Cell Line Derived Neurotropic Factor Proteins into Brain to Treat Rat Depression, J. Biomed. Nanotechnol 16 (2020) 626– 639, 10.1166/JBN.2020.2914. 32919483 · DOI
  65. [69]Tsai SJ, Transcranial focused ultrasound as a possible treatment for major depression, Med. Hypotheses 84 (2015) 381– 383, 10.1016/J.MEHY.2015.01.030. 25665863 · DOI
  66. [70]Burgess A, Ayala-Grosso CA, Ganguly M, Jordão JF, Aubert I, Hynynen K, Jordã JF, Aubert I, Hynynen K, Jord??o JF, Aubert I, Hynynen K, Targeted delivery of neural stem cells to the brain using MRI-guided focused ultrasound to disrupt the blood-brain barrier, PLoS One. 6 (2011) e27877-. 10.1371/journal.pone.0027877. 22114718 PMC3218061 · DOI
  67. [71]Ahmed N, Gandhi D, Melhem ER, Frenkel V, MRI Guided Focused Ultrasound-Mediated Delivery of Therapeutic Cells to the Brain: A Review of the State-of-the-Art Methodology and Future Applications, Front. Neurol 12. (2021), 10.3389/FNEUR.2021.669449. PMC8248790 34220679 · DOI
  68. [72]Bin Shen W, Anastasiadis P, Nguyen B, Yarnell D, Yarowsky PJ, Frenkel V, Fishman PS, Magnetic Enhancement of Stem Cell-Targeted Delivery into the Brain Following MR-Guided Focused Ultrasound for Opening the Blood-Brain Barrier, Cell Transplant. 26 (2017) 1235– 1246, 10.1177/0963689717715824. 28933214 PMC5657739 · DOI
  69. [73]Lee J, Chang WS, Shin J, Seo Y, Kong C, Song B-W, Na YC, Kim BS, Chang JW, Non-invasively enhanced intracranial transplantation of mesenchymal stem cells using focused ultrasound mediated by overexpression of cell-adhesion molecules, Stem Cell Res. 43 (2020) 101726. 32028085
  70. [74]Lynch M, Heinen S, Markham-Coultes K, O’reilly M, Van Slyke P, Dumont DJ, Hynynen K, Aubert I, Vasculotide restores the blood-brain barrier after focused ultrasound-induced permeability in a mouse model of alzheimer’s disease, Int. J. Med. Sci 18 (2021) 482– 493, 10.7150/IJMS.36775. 33390817 PMC7757142 · DOI
  71. [75]Scarcelli T, Jordao JF, O’Reilly MA, Ellens N, Hynynen K, Aubert I, Stimulation of Hippocampal Neurogenesis by Transcranial Focused Ultrasound and Microbubbles in Adult Mice, Brain Stimulation 7 (2) (2014) 304– 307. 24629831 PMC4103630
  72. [76]Mathew AS, Gorick CM, Price RJ, Single-cell mapping of focused ultrasound-transfected brain, Gene Ther. (2021) 1– 9. 10.1038/s41434-021-00226-0. PMC8325700 33526842 · DOI
  73. [77]Mooney SJ, Shah K, Yeung S, Burgess A, Aubert I, Hynynen K, Deli MA, Focused ultrasound-induced neurogenesis requires an increase in blood-brain barrier permeability, PLoS One. 11 (7) (2016) e0159892. 27459643 PMC4961388
  74. [78]Shin J, Kong C, Lee J, Choi BY, Sim J, Koh CS, Park M, Na YC, Suh SW, Chang WS, Chang JW, Focused ultrasound-induced blood-brain barrier opening improves adult hippocampal neurogenesis and cognitive function in a cholinergic degeneration dementia rat model, Alzheimer’s Res. Ther 11 (2019) 1– 15, 10.1186/s13195-019-0569-x. 31881998 PMC6933667 · DOI
  75. [79]McMahon D, Mah E, Hynynen K, Angiogenic response of rat hippocampal vasculature to focused ultrasound-mediated increases in blood-brain barrier permeability, Sci. Rep 8 (2018), 10.1038/S41598-018-30825-8. PMC6093874 30111814 · DOI
  76. [80]Todd N, Zhang Y, Livingstone M, Borsook D, McDannold N, The neurovascular response is attenuated by focused ultrasound-mediated disruption of the blood-brain barrier, Neuroimage. 201 (2019), 10.1016/j.neuroimage.2019.116010. PMC6765430 31302253 · DOI
  77. [81]Leinenga G, Götz J, Scanning ultrasound removes amyloid-β and restores memory in an Alzheimer’s disease mouse model, Sci. Transl. Med 7 (2015) 278ra33, 10.1126/scitranslmed.aaa2512. 25761889 · DOI · Paper page
  78. [82]Park SH, Baik K, Jeon S, Chang WS, Ye BS, Chang JW, Extensive frontal focused ultrasound mediated blood–brain barrier opening for the treatment of Alzheimer’s disease: a proof-of-concept study, Transl. Neurodegener 10 (2021) 1– 11, 10.1186/S40035-021-00269-8/TABLES/4. 34740367 PMC8570037 · DOI
  79. [83]Burgess A, Nhan T, Moffatt C, Klibanov AL, Hynynen K, Analysis of focused ultrasound-induced blood-brain barrier permeability in a mouse model of Alzheimer’s disease using two-photon microscopy, J. Control. Release 192 (2014) 243– 248, 10.1016/j.jconrel.2014.07.051. 25107692 · DOI
  80. [84]Marty B, Larrat B, Van Landeghem M, Robic C, Robert P, Port M, Le Bihan D, Pernot M, Tanter M, Lethimonnier F, Mériaux S, Dynamic study of blood-brain barrier closure after its disruption using ultrasound: a quantitative analysis, J. Cereb. Blood Flow Metab 32 (2012) 1948– 1958, 10.1038/JCBFM.2012.100. 22805875 PMC3463875 · DOI
  81. [85]O’Reilly MA, Hough O, Hynynen K, Blood-Brain Barrier Closure Time After Controlled Ultrasound-Induced Opening Is Independent of Opening Volume, J. Ultrasound Med 36 (2017) 475– 483, 10.7863/ULTRA.16.02005. 28108988 PMC5319892 · DOI
  82. [86]Leinenga G, Koh WK, Götz J, Scanning ultrasound in the absence of blood-brain barrier opening is not sufficient to clear β-amyloid plaques in the APP23 mouse model of Alzheimer’s disease, Brain Res. Bull 153 (2019) 8– 14, 10.1016/J.BRAINRESBULL.2019.08.002. 31400496 · DOI · Paper page
  83. [87]D’Haese PF, Ranjan M, Song A, Haut MW, Carpenter J, Dieb G, Najib U, Wang P, Mehta RI, Chazen JL, Hodder S, Claassen D, Kaplitt M, Rezai AR, β-Amyloid Plaque Reduction in the Hippocampus After Focused Ultrasound-Induced Blood-Brain Barrier Opening in Alzheimer’s Disease, Front. Hum. Neurosci 14 (2020), 10.3389/fnhum.2020.593672. PMC7575813 33132889 · DOI · Paper page
  84. [88]Jordão JF, Thévenot E, Markham-Coultes K, Scarcelli T, Weng YQ, Xhima K, O’Reilly M, Huang Y, McLaurin JA, Hynynen K, Aubert I, Amyloid-β plaque reduction, endogenous antibody delivery and glial activation by brain-targeted, transcranial focused ultrasound, Exp. Neurol 248 (2013) 16– 29, 10.1016/J.EXPNEUROL.2013.05.008. 23707300 PMC4000699 · DOI · Paper page
  85. [89]Lee Y, Choi Y, Park E-J, Kwon S, Kim H, Lee JY, Lee DS, Improvement of glymphatic-lymphatic drainage of beta-amyloid by focused ultrasound in Alzheimer’s disease model, Sci Rep 10 (1) (2020). PMC7527457 32999351
  86. [90]Todd N, Angolano C, Ferran C, Devor A, Borsook D, McDannold N, Secondary effects on brain physiology caused by focused ultrasound-mediated disruption of the blood–brain barrier, J. Control. Release 324 (2020) 450– 459, 10.1016/j.jconrel.2020.05.040. 32470359 PMC7429281 · DOI
  87. [91]Wang Y, Martinez-Vicente M, Krüger U, Kaushik S, Wong E, Mandelkow EM, Cuervo AM, Mandelkow E, Synergy and antagonism of macroautophagy and chaperone-mediated autophagy in a cell model of pathological tau aggregation, Autophagy. 6 (2010) 182– 183, 10.4161/auto.6.1.10815. 20023429 · DOI · Paper page
  88. [93]Karakatsani ME, Kugelman T, Ji R, Murillo M, Wang S, Niimi Y, Small SA, Duff KE, Konofagou EE, Unilateral focused ultrasound-induced blood-brain barrier opening reduces phosphorylated Tau from the rTg4510 mouse model, Theranostics. 9 (2019) 5396– 5411, 10.7150/thno.28717. 31410223 PMC6691580 · DOI
  89. [94]Wang JB, Di Ianni T, Vyas DB, Huang Z, Park S, Hosseini-Nassab N, Aryal M, Airan RD, Focused Ultrasound for Noninvasive, Focal Pharmacologic Neurointervention, Front. Neurosci 14 (2020) 675, 10.3389/FNINS.2020.00675/BIBTEX. 32760238 PMC7372945 · DOI
  90. [95]Todd N, Zhang Y, Power C, Becerra L, Borsook D, Livingstone M, McDannold N, Modulation of brain function by targeted delivery of GABA through the disrupted blood-brain barrier, Neuroimage. 189 (2019) 267– 275, 10.1016/J.NEUROIMAGE.2019.01.037. 30659957 PMC6422703 · DOI
  91. [96]Constans C, Ahnine H, Santin M, Lehericy S, Tanter M, Pouget P, Aubry JF, Non-invasive ultrasonic modulation of visual evoked response by GABA delivery through the blood brain barrier, J. Control. Release 318 (2020) 223– 231, 10.1016/J.JCONREL.2019.12.006. 31816362 · DOI
  92. [97]Rich MC, Sherwood J, Bartley AF, Whitsitt QA, Lee M, Willoughby WR, Dobrunz LE, Bao Y, Lubin FD, Bolding M, Focused ultrasound blood brain barrier opening mediated delivery of MRI-visible albumin nanoclusters to the rat brain for localized drug delivery with temporal control, J. Control. Release 324 (2020) 172– 180, 10.1016/J.JCONREL.2020.04.054. 32376461 PMC8890744 · DOI
  93. [98]Airan RD, Meyer RA, Ellens NPK, Rhodes KR, Farahani K, Pomper MG, Kadam SD, Green JJ, Noninvasive Targeted Transcranial Neuromodulation via Focused Ultrasound Gated Drug Release from Nanoemulsions, Nano Lett. 17 (2017) 652– 659, 10.1021/ACS.NANOLETT.6B03517. 28094959 PMC5362146 · DOI
  94. [99]Wang JB, Aryal M, Zhong Q, Vyas DB, Airan RD, Noninvasive Ultrasonic Drug Uncaging Maps Whole-Brain Functional Networks, Neuron. 100 (2018) 728– 738.e7, 10.1016/J.NEURON.2018.10.042. 30408444 PMC6274638 · DOI
  95. [100]Chu P-C, Liu H-L, Lai H-Y, Lin C-Y, Tsai H-C, Pei Y-C, Neuromodulation accompanying focused ultrasound-induced blood-brain barrier opening, Sci Rep 5 (1) (2015). PMC4614673 26490653
  96. [101]Park SH, Kim MJ, Jung HH, Chang WS, Choi HS, Rachmilevitch I, Zadicario E, Chang JW, One-Year Outcome of Multiple Blood-Brain Barrier Disruptions With Temozolomide for the Treatment of Glioblastoma, Front. Oncol 10 (2020), 10.3389/FONC.2020.01663. PMC7511634 33014832 · DOI
  97. [102]Ibsen S, Tong A, Schutt C, Esener S, Chalasani SH, Sonogenetics is a non- invasive approach to activating neurons in Caenorhabditis elegans, Nat. Commun 6 (2015) 8264, 10.1038/ncomms9264. 26372413 PMC4571289 · DOI
  98. [103]Huang Y-S, Fan C-H, Hsu N, Chiu N-H, Wu C-Y, Chang C-Y, Wu B-H, Hong S-R, Chang Y-C, Yan-Tang Wu A, Guo V, Chiang Y-C, Hsu W-C, Chen L, Pin-Kuang Lai C, Yeh C-K, Lin Y-C, Sonogenetic Modulation of Cellular Activities Using an Engineered Auditory-Sensing Protein, Nano Lett. 20 (2020) 1089– 1100, 10.1021/acs.nanolett.9b04373. 31884787 · DOI
  99. [104]Yang Y, Pacia CP, Ye D, Zhu L, Baek H, Yue Y, Yuan J, Miller MJ, Cui J, Culver JP, Bruchas MR, Chen H, Sonothermogenetics for noninvasive and cell-type specific deep brain neuromodulation, Brain Stimul. 14 (2021) 790– 800, 10.1016/j.brs.2021.04.021. 33989819 PMC8995105 · DOI
  100. [105]Cubillos-Ruiz A, Guo T, Sokolovska A, Miller PF, Collins JJ, Lu TK, Lora JM, Engineering living therapeutics with synthetic biology, Nat. Rev. Drug Discov 20 (2021) 941– 960, 10.1038/s41573-021-00285-3. 34616030 · DOI
  101. [106]Amrahli M, Centelles M, Cressey P, Prusevicius M, Gedroyc W, Xu XY, So PW, Wright M, Thanou M, Mr-labelled liposomes and focused ultrasound for spatiotemporally controlled drug release in triple negative breast cancers in mice, Nanotheranostics. 5 (2021) 125– 142, 10.7150/ntno.52168. 33457192 PMC7806456 · DOI
  102. [107]Babakhanian M, Yang L, Nowroozi B, Saddik G, Boodaghians L, Blount P, Grundfest W, Effects of Low Intensity Focused Ultrasound on Liposomes Containing Channel proteins, Sci. Rep 8 (2018) 17250, 10.1038/s41598-018-35486-1. 30467339 PMC6250712 · DOI
  103. [108]Szablowski JO, Harb M, Focused Ultrasound Induced Blood-Brain Barrier Opening for Targeting Brain Structures and Evaluating Chemogenetic Neuromodulation, J. Vis. Exp (2020), 10.3791/61352. 33427233 · DOI
  104. [109]Szablowski JO, Bar-Zion A, Shapiro MG, Achieving Spatial and Molecular Specificity with Ultrasound-Targeted Biomolecular Nanotherapeutics, Acc. Chem. Res 52 (2019) 2427– 2434, 10.1021/acs.accounts.9b00277. 31397992 PMC7462121 · DOI
  105. [110]Menard C, Russo SJ, Non-invasive chemogenetics, Nat. Biomed. Eng 2 (2018) 467– 468, 10.1038/s41551-018-0269-z. 30948827 · DOI
  106. [111]Szablowski JO, Lee-Gosselin A, Lue B, Malounda D, Shapiro MG, Acoustically targeted chemogenetics for the non-invasive control of neural circuits, Nat. Biomed. Eng 2 (2018) 475– 484, 10.1038/s41551-018-0258-2. 30948828 · DOI
  107. [112]Abedi MH, Lee J, Piraner DI, Shapiro MG, Thermal Control of Engineered T-cells, ACS Synth. Biol 9 (2020) 1941– 1950, 10.1021/acssynbio.0c00238. 32786924 · DOI
  108. [113]Wu Y, Liu Y, Huang Z, Wang X, Jin Z, Li J, Limsakul P, Zhu L, Allen M, Pan Y, Bussell R, Jacobson A, Liu T, Chien S, Wang Y, Control of the activity of CAR-T cells within tumours via focused ultrasound, Nat. Biomed. Eng 5 (2021) 1336– 1347, 10.1038/s41551-021-00779-w. 34385696 PMC9015817 · DOI
  109. [114]Pan Y, Yoon S, Sun J, Huang Z, Lee C, Allen M, Wu Y, Chang Y-J, Sadelain M, Shung KK, Chien S, Wang Y, Mechanogenetics for the remote and noninvasive control of cancer immunotherapy, Proc. Natl. Acad. Sci 115 (2018) 992– 997, 10.1073/pnas.1714900115. 29343642 PMC5798350 · DOI
  110. [115]Wu Y, Huang Z, Harrison R, Liu L, Zhu L, Situ Y, Wang Y, Engineering CART cells for enhanced efficacy and safety, APL Bioeng. 6 (1) (2022) 011502. 35071966 PMC8769768
  111. [117]Lockman PR, Mittapalli RK, Taskar KS, Rudraraju V, Gril B, Bohn KA, Adkins CE, Roberts A, Thorsheim HR, Gaasch JA, Huang S, Palmieri D, Steeg PS, Smith QR, Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer, Clin. Cancer Res 16 (2010) 5664– 5678. 10.1158/1078-0432.CCR-10-1564. 20829328 PMC2999649 · DOI
  112. [118]Juillerat-Jeanneret L, The targeted delivery of cancer drugs across the blood–brain barrier: chemical modifications of drugs or drug-nanoparticles?, Drug Discov Today. 13 (2008) 1099– 1106, 10.1016/J.DRUDIS.2008.09.005. 18848640 · DOI
  113. [120]Idbaih A, Canney M, Belin L, Desseaux C, Vignot A, Bouchoux G, Asquier N, Law-Ye B, Leclercq D, Bissery A, De Rycke Y, Trosch C, Capelle L, Sanson M, Hoang-Xuan K, Dehais C, Houillier C, Laigle-Donadey F, Mathon B, Andre A, Lafon C, Chapelon JY, Delattre JY, Carpentier A, Safety and Feasibility of Repeated and Transient Blood–Brain Barrier Disruption by Pulsed Ultrasound in Patients with Recurrent Glioblastoma, Clin. Cancer Res 25 (2019) 3793– 3801. 10.1158/1078-0432.CCR-18-3643. 30890548 · DOI
  114. [121]Mainprize T, Lipsman N, Huang Y, Meng Y, Bethune A, Ironside S, Heyn C, Alkins R, Trudeau M, Sahgal A, Perry J, Hynynen K, Blood-Brain Barrier Opening in Primary Brain Tumors with Non-invasive MR-Guided Focused Ultrasound: A Clinical Safety and Feasibility Study, Sci. Rep 9 (2019), 10.1038/S41598-018-36340-0. PMC6344541 30674905 · DOI
  115. [122]Meng Y, Reilly RM, Pezo RC, Trudeau M, Sahgal A, Singnurkar A, Perry J, Myrehaug S, Pople CB, Davidson B, Llinas M, Hyen C, Huang Y, Hamani C, Suppiah S, Hynynen K, Lipsman N, MR-guided focused ultrasound enhances delivery of trastuzumab to Her2-positive brain metastases, Sci. Transl. Med 13 (2021), 10.1126/SCITRANSLMED.ABJ4011/SUPPL_FILE/SCITRANSLMED.ABJ4011_SM.PDF. 34644145 · DOI
  116. [123]Anastasiadis P, Gandhi D, Guo Y, Ahmed AK, Bentzen SM, Arvanitis C, Woodworth GF, Localized blood-brain barrier opening in infiltrating gliomas with MRI-guided acoustic emissions-controlled focused ultrasound, Proc. Natl. Acad. Sci. U. S. A 118 (2021), 10.1073/PNAS.2103280118/-/DCSUPPLEMENTAL. PMC8449371 34504017 · DOI
  117. [124]Park SH, Kim MJ, Jung HH, Chang WS, Choi HS, Rachmilevitch I, Zadicario E, Chang JW, Safety and feasibility of multiple blood-brain barrier disruptions for the treatment of glioblastoma in patients undergoing standard adjuvant chemotherapy, J. Neurosurg 134 (2020) 475– 483, 10.3171/2019.10.JNS192206. 31899873 · DOI
  118. [125]Meng Y, Pople CB, Suppiah S, Llinas M, Huang Y, Sahgal A, Perry J, Keith J, Davidson B, Hamani C, Amemiya Y, Seth A, Leong H, Heyn CC, Aubert I, Hynynen K, Lipsman N, MR-guided focused ultrasound liquid biopsy enriches circulating biomarkers in patients with brain tumors, Neuro Oncol. 23 (2021) 1789– 1797, 10.1093/NEUONC/NOAB057. 33693781 PMC8485448 · DOI
  119. [126]Lipsman N, Meng Y, Bethune AJ, Huang Y, Lam B, Masellis M, Herrmann N, Heyn C, Aubert I, Boutet A, Smith GS, Hynynen K, Black SE, Blood–brain barrier opening in Alzheimer’s disease using MR-guided focused ultrasound, Nat. Commun 91 (9) (2018) 1– 8, 10.1038/s41467-018-04529-6. PMC6060168 30046032 · DOI · Paper page
  120. [127]Mehta RI, Carpenter JS, Mehta RI, Haut MW, Ranjan M, Najib U, Lockman P, Wang P, D’Haese PF, Rezai AR, Blood-Brain Barrier Opening with MRI-guided Focused Ultrasound Elicits Meningeal Venous Permeability in Humans with Early Alzheimer Disease, Radiology. 298 (2021) 654– 662, 10.1148/RADIOL.2021200643. 33399511 PMC7924515 · DOI · Paper page
  121. [128]Martínez-Fernández R, Máñez-Miró JU, Rodríguez-Rojas R, del Álamo M, Shah BB, Hernández-Fernández F, Pineda-Pardo JA, Monje MHG, Fernández-Rodríguez B, Sperling SA, Mata-Marín D, Guida P, Alonso-Frech F, Obeso I, Gasca-Salas C, Vela-Desojo L, Elias WJ, Obeso JA, Randomized Trial of Focused Ultrasound Subthalamotomy for Parkinson’s Disease, N. Engl. J. Med 383 (2020) 2501– 2513, 10.1056/NEJMOA2016311/SUPPL_FILE/NEJMOA2016311_DATA-SHARING.PDF. 33369354 · DOI
  122. [129]Gasca-Salas C, Fernández-Rodríguez B, Pineda-Pardo JA, Rodríguez-Rojas R, Obeso I, Hernández-Fernández F, del Álamo M, Mata D, Guida P, Ordás-Bandera C, Montero-Roblas JI, Martínez-Fernández R, Foffani G, Rachmilevitch I, Obeso JA, Blood-brain barrier opening with focused ultrasound in Parkinson’s disease dementia, Nat. Commun, 12 (2021), 10.1038/S41467-021-21022-9. PMC7859400 33536430 · DOI · Paper page
  123. [130]Abrahao A, Meng Y, Llinas M, Huang Y, Hamani C, Mainprize T, Aubert I, Heyn C, Black SE, Hynynen K, Lipsman N, Zinman L, First-in-human trial of blood-brain barrier opening in amyotrophic lateral sclerosis using MR-guided focused ultrasound, Nat. Commun 10 (2019), 10.1038/S41467-019-12426-9. PMC6763482 31558719 · DOI · Paper page
  124. [131]Keller SB, Averkiou MA, The Role of Ultrasound in Modulating Interstitial Fluid Pressure in Solid Tumors for Improved Drug Delivery, Bioconjug. Chem 33 (6) (2022) 1049– 1056. 34514776
  125. [132]Hersh DS, Nguyen BA, Dancy JG, Adapa AR, Winkles JA, Woodworth GF, Kim AJ, Frenkel V, Pulsed ultrasound expands the extracellular and perivascular spaces of the brain, Brain Res. 1646 (2016) 543– 550, 10.1016/j.brainres.2016.06.040. 27369449 PMC5499235 · DOI
  126. [133]Hersh DS, Anastasiadis P, Mohammadabadi A, Nguyen BA, Guo S, Winkles JA, Kim AJ, Gullapalli R, Keller A, Frenkel V, Woodworth GF, Ceña V, MR-guided transcranial focused ultrasound safely enhances interstitial dispersion of large polymeric nanoparticles in the living brain, PLoS One. 13 (2) (2018) e0192240. 29415084 PMC5802894
  127. [134]Wang S, Karakatsani ME, Fung C, Sun T, Acosta C, Konofagou E, Direct brain infusion can be enhanced with focused ultrasound and microbubbles, J. Cereb. Blood Flow Metab 37 (2017) 706– 714, 10.1177/0271678X16637881. 26969468 PMC5381459 · DOI
  128. [136]Mead BP, Curley CT, Kim N, Negron K, Garrison WJ, Song JI, Rao D, Miller GW, Mandell JW, Purow BW, Suk JS, Hanes J, Price RJ, Focused Ultrasound Preconditioning for Augmented Nanoparticle Penetration and Efficacy in the Central Nervous System, Small. 15(49) (2019) 1903460. PMC7084172 31642183
  129. [137]Aryal M, Azadian MM, Hart AR, Macedo N, Zhou Q, Rosenthal EL, Airan RD, Noninvasive ultrasonic induction of cerebrospinal fluid flow enhances intrathecal drug delivery, J. Control. Release 349 (2022) 434– 442, 10.1016/J.JCONREL.2022.06.067. 35798095 · DOI
  130. [138]Yoo S-S, Kim H-C, Kim J, Kim E, Kowsari K, Van Reet J, Yoon K, Enhancement of cerebrospinal fluid tracer movement by the application of pulsed transcranial focused ultrasound, Sci. Reports 121 (12) (2022) 1– 13, 10.1038/s41598-022-17314-9. PMC9334279 35902724 · DOI
  131. [139]Curley CT, Stevens AD, Mathew AS, Stasiak K, Garrison WJ, Wilson Miller G, Sheybani ND, Engelhard VH, Bullock TNJ, Price RJ, Immunomodulation of intracranial melanoma in response to blood-tumor barrier opening with focused ultrasound, Theranostics. 10 (2020) 8821– 8833, 10.7150/thno.47983. 32754281 PMC7392000 · DOI
  132. [140]Gorick CM, Mathew AS, Garrison WJ, Thim EA, Fisher DG, Copeland CA, Song JI, Klibanov AL, Miller GW, Price RJ, Sonoselective transfection of cerebral vasculature without blood–brain barrier disruption, Proc. Natl. Acad. Sci. U.S.A 117(11) (2020) 5644– 5654. 32123081 PMC7084076
  133. [141]Zafar A, Quadri SA, Farooqui M, Ortega-Gutierrez S, Hariri OR, Zulfiqar M, Ikram A, Khan MA, Suriya SS, Nunez-Gonzalez JR, Posse S, Mortazavi MM, Yonas H, MRI-Guided High-Intensity Focused Ultrasound as an Emerging Therapy for Stroke: A Review, J. Neuroimaging 29 (2019) 5– 13, 10.1111/JON.12568. 30295987 · DOI
  134. [142]Wu S-K, Yang M-T, Kang K-H, Liou H-C, Lu D-H, Fu W-M, Lin W-L, Karamyan V, Targeted Delivery of Erythropoietin by Transcranial Focused Ultrasound for Neuroprotection against Ischemia/Reperfusion-Induced Neuronal Injury: A Long-Term and Short-Term Study, PLoS One. 9 (2) (2014) e90107. 24587228 PMC3938648
  135. [143]Rodríguez-Frutos B, Otero-Ortega L, Ramos-Cejudo J, Martínez-Sánchez P, Barahona-Sanz I, Navarro-Hernanz T, Gómez-de Frutos MDC, Díez-Tejedor E, Gutiérrez-Fernández M, Enhanced brain-derived neurotrophic factor delivery by ultrasound and microbubbles promotes white matter repair after stroke, Biomaterials. 100 (2016) 41– 52. 27240161
  136. [144]Vernooij MW, Ikram MA, Tanghe HL, Vincent AJPE, Hofman A, Krestin GP, Niessen WJ, Breteler MMB, van der Lugt A, Incidental Findings on Brain MRI in the General Population, N. Engl. J. Med 357 (2007) 1821– 1828, 10.1056/nejmoa070972. 17978290 · DOI
  137. [145]Del Curling O, Kelly DL, Elster AD, Craven TE, An analysis of the natural history of cavernous angiomas, J. Neurosurg 75 (1991) 702– 708, 10.3171/jns.1991.75.5.0702. 1919691 · DOI
  138. [146]Ene C, Kaul A, Kim L, Natural history of cerebral cavernous malformations, in: Handb. Clin. Neurol., Handb Clin Neurol, 2017: pp. 227– 232. 10.1016/B978-0-444-63640-9.00021-7. 28552144 · DOI
  139. [147]Haasdijk RA, Cheng C, Maat-Kievit AJ, Duckers HJ, Cerebral cavernous malformations: From molecular pathogenesis to genetic counselling and clinical management, Eur.J. Hum. Genet 20 (2012) 134– 140, 10.1038/ejhg.2011.155. 21829231 PMC3260921 · DOI
  140. [148]Snellings DA, Hong CC, Ren AA, Lopez-Ramirez MA, Girard R, Srinath A, Marchuk DA, Ginsberg MH, Awad IA, Kahn ML, Cerebral Cavernous Malformation: From Mechanism to Therapy, Circ. Res 129 (2021) 195– 215, 10.1161/CIRCRESAHA.121.318174. 34166073 PMC8922476 · DOI

Cited by

Sorted by citations

Authors
Gorick, C. M., Breza, V. R., Nowak, K. M., Cheng, V. W. T., Fisher, D. G., Debski, A. C., Hoch, M. R., Demir, Z. E. F., Tran, N. M., Schwartz, M. R., Sheybani, N. D., & Price, R. J.
Affiliations
  • University of Virginia (US)
  • University of Leeds (GB)
Corresponding author
Price, Richard J.
Venue
Advanced Drug Delivery Reviews
Publisher
Elsevier BV
Published
2022-12
Volume
191
Pages
114583
ISSN
0169-409X (ISSN-L)
OpenAlex
W4306804981
Cited by
144
References
6
Citations by year
2026: 42 · 2025: 41 · 2024: 41 · 2023: 20
FWCI
2.27
Type
journal article
Language
en
Open access
Locations
  • Advanced Drug Delivery Reviews (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
Funders
  • National Institutes of Health (R01EB030744, R21NS118278)
  • National Institutes of Health Office of the Director (DP5OD031846)
  • National Institute of Neurological Disorders and Stroke (R01NS111102)
  • National Institute of Biomedical Imaging and Bioengineering (R01EB030409)
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › Ultrasound and Hyperthermia Applications
  • Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
  • Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
Keywords
focused ultrasound, blood-brain barrier opening, microbubbles, gene delivery, neuromodulation, neuropathology, image-guided therapy
MeSH terms
Biological Transport, Blood-Brain Barrier, Contrast Media, Humans, Magnetic Resonance Imaging, Drug Delivery Systems, Microbubbles

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