743
Views
69
CrossRef citations to date
0
Altmetric
Reviews

Drug delivery across the blood–brain barrier using focused ultrasound

&

Bibliography

  • Abbott NJ, Patabendige AA, Doman DE, et al. Structure and function of the blood-brain barrier. Neurobiol Dis 2004;37:13–25
  • Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2006;57:173–85
  • Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006;7:41–53
  • Pardridge WM. The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2005;2:3–14
  • Gustavsson A, Svensson M, Jacobi F, et al. Cost of disorders of the brain in Europe 2010. Eur Neuropsychopharmacol 2011;21:718–79
  • Marks WJ Jr, Ostrem JL, Verhagen L, et al. Safety and tolerability of intraputaminal delivery of CERE-120 (adeno-associated virus serotype 2-neurturin) to patients with idiopathic Parkinson's disease: an open label, phase I trial. Lancet Neurol 2008;7:400–8
  • Gross RE Watts RL, Hauser RA, et al. Intrastriatal transplantation of microcarrier-bound human retinal pigment epithelial cells versus sham surgery in patients with advanced Parkinson's disease: a double-blind, randomised, controlled trial. Lancet Neurol 2011;10:509–19
  • Matsukado K, Sugita M, Black KL. Intracarotid low dose bradykinin infusion selectively increase tumor permeability through activation of bradykinin. Brain Res 1998;792:10–15
  • Rapoport SI. Advances in osmotic opening of the blood-brain barrier to enhance CNS chemotherapy. Expert Opin Investig Drugs 2001;10:1809–18
  • Pardridge WM, Boado RJ. Reengineering biopharmaceuticals for targeted delivery across the blood-brain barrier. Methods Enzymol 2012;503:269–92
  • Lochhead JJ, Thorne RG. Intranasal delivery of biologics to the central nervous system. Adv Drug Deliv Rev 2012;64:614–28
  • Pardridge WM. Drug transport across the blood-brain barrier. J Cereb Blood Flow Metab 2012;32:1959–72
  • Bakay L, Ballantine HT Jr, Hueter TF, Sosa D. Ultrasonically produced changes in the blood-brain barrier. AMA Arch Neurol Psychiatry 1956;76:457–67
  • Shealy CN, Crafts D. Selective alteration of the blood-brain barrier. J Neurosurg 1965;23:484–7
  • Ng KY, Cho CW, Henthorn TK, Tanguay RL. Effect of heat preconditioning on the uptake and permeability of R123 in brain microvessel endothelial cells during mild heat treatment. J Pharm Sci 2004;93:896–907
  • McDannold N, Vykhodsteva N, Jolesz FA, Hynynen K. MRI investigation of the threshold for thermally induced blood-brain barrier disruption and brain tissue damage in the rabbit. Magn Reson Med 2004;51:913–23
  • Vykhodtseva N, Hynynen K, Damianou C. Histologic effects of high intensity pulsed ultrasound exposure with subharmonic emission in rabbit brain in vivo. Ultrasound Med Biol 1995;21:969–79
  • Mesiwala AH, Farrell L, Wenzel HJ, et al. High-intensity focused ultrasound selectively disrupts the blood-brain barrier in vivo. Ultrasound Med Biol 2002;28:389–400
  • Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA. Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 2001;220:640–6
  • Hynynen K. MRI-guided focused ultrasound treatments. Ultrasonics 2010;50:221–9
  • Liu HL, Pan CH, Ting CY, Hsiao MJ. Opening of the blood-brain barrier by low-frequency (28kHz) ultrasound: a novel pinhole assisted mechanical scanning device. Ultrasound Med Biol 2010;36:325–35
  • Bing KF, Howles GP, Qi Y, et al. Blood-brain barrier (BBB) disruption using a diagnostic ultrasound scanner and Definity in mice. Ultrasound Med Biol 2009;35:1298–308
  • McDannold N, Vykhodtseva N, Hynynen K. Blood-brain barrier disruption by focused ultrasound and circulating preformed microbubbles appears to be characterized by the mechanical index. Ultrasound Med Biol 2008;34:834–40
  • McDannold N, Vykhodtseva N, Hynynen K. Effects of acoustic parameters and ultrasound. Ultrasound Med Biol 2008;34:930–7
  • Choi JJ, Selert K, Gao Z, et al. Noninvasive and localized blood-brain barrier disruption using focused ultrasound can be achieved at short pulses lengths and low repetition frequencies. J Cereb Blood Flow Metab 2011;31:725–37
  • O'Reilly MA, Waspe AC, Ganguly M, Hynynen K. Focused ultrasound disruption of the blood-brain barrier using closely-timed short pulses: influence of sonication parameters and injection rate. Ultrasound Med Biol 2010;37:587–94
  • Goertz DE, Wright C, Hynynen K. Contrast agent kinetics in the rabbit brain during exposure to therapeutic ultrasound. Ultrasound Med Biol 2010;36:916–24
  • McDannold N, Vykhodtseva N, Hynynen K. Use of ultrasound pulses combined with Definity for targeted blood-brain barrier disruption; a feasibility study. Ultrasound Med Biol 2007;33:584–90
  • Yang FY, Fu WM, Chen WS, et al. Quantitative evaluation of the use of microbubbles with transcranial focused ultrasound on blood-brain barrier disruption. Ultrason Sonochem 2008;15:636–43
  • Weng JC, Wu SK, Yang FY, Tseng WY. Pulse sequence and timing of contrast-enhanced MRI for assessing blood-brain barrier disruption after transcranial focused ultrasound in the presence of haemorrhage. J Magn Reson Imaging 2010;31:1323–30
  • Choi JJ, Feshitan JA, Baseri B, et al. Microbubble-size dependence of focused ultrasound-induced blood-brain barrier opening in mice in vivo. IEEE Trans Biomed Eng 2010;57:145–54
  • Vlachos F, Tung YS, Konofagou EE. Permeability dependence study of the focused ultrasound-induced blood-brain barrier opening at distinct pressures and microbubble diameters using DCE-MRI. Magn Reson Med 2011;66:821–30
  • O'Reilly MA, Hynynen K. Blood-brain barrier: real-time feedback-controlled focused ultrasound disruption by using an acoustic emissions-based controller. Radiology 2012;263:96–106
  • Burgess A, Ayala-Grosso CA, Ganguly M, et al. Targeted delivery of neural stem cells to the brain using MRI-guided focused ultrasound to disrupt the blood-brain barrier. PLoS One 2011;6:e27877
  • Treat LH, McDannold N, Vykhodtseva N, et al. Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound. Int J Cancer 2007;121:901–7
  • Jordão JF, Ayala-Grosso CA, Markham K, et al. Antibodies targeted to the brain with image-guided focused ultrasound reduces amyloid-beta plaque load in the TgCRND8 mouse model of Alzheimer's disease. PLoS One 2010;5:e10549
  • Howles GP, Bing KF, Qui Y, et al. Contrast-enhanced in vivo magnetic resonance microscopy of the mouse brain enabled by noninvasive opening of the blood-brain barrier with ultrasound. Magn Reson Med 2010;64:995–1004
  • Hosseinkhah N, Hynynen K. A three-dimensional model of an ultrasound contrast agent gas bubble and its mechanical effects on microvessels. Phys Med Biol 2012;57:785–808
  • Chen PY, Liu HL, Hua MY, et al. Novel magnetic/ultrasound focusing system enhances nanoparticle drug delivery for glioma treatment. Neuro Oncol 2010;12:1050–60
  • Nyborg WL. Biological effects of ultrasound: development of safety guidelines. Part II: general review. Ultrasound Med Biol 2001;27:301–33
  • Deng CX, Sieling F, Pan H, Cui J. Ultrasound-induced cell membrane porosity. Ultrasound Med Biol 2004;30:519–26
  • Sheikov N, McDannold N, Vykhodtseva N, et al. Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles. Ultrasound Med Biol 2004;30:979–89
  • Sheikov N, Mcdannold N, Sharma S, Hynynen K. Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium. Ultrasound Med Biol 2008;34:1093–104
  • Lionetti V, Fittipaldi A, Agostini S, et al. Enhanced caveolae-mediated endocytosis by diagnostic ultrasound in vitro. Ultrasound Med Biol 2009;35:136–43
  • Deng J, Huang Q, Wang F, et al. The role of caveolin-1 in blood-brain barrier disruption induced by focused ultrasound combined with microbubbles. J Mol Neurosci 2012;46:677–87
  • Alonso A, Reinz E, Fatar M, et al. Clearance of albumin following ultrasound-induced blood-brain barrier opening is mediated by glial but not neuronal cells. Brain Res 2011;1411:9–16
  • Raymond SB, Treat LH, Dewey JD, et al. Ultrasound enhanced delivery of molecular imaging and therapeutic agents in Alzheimer's disease mouse models. PLoS One 2008;3:e2175
  • Cho EE, Drazic J, Ganguly M, et al. Two-photon fluorescence microscopy study of cerebrovascular dynamics in ultrasound-induced blood–brain barrier opening. J Cereb Blood Flow Metab 2011;31:1852–62
  • Hynynen K, McDannold N, Vykhodtseva N, et al. Focal disruption of the blood-brain barrier due to 260-kHz ultrasound bursts: a method for molecular imaging and targeted drug delivery. J Neurosurg 2006;105:445–54
  • Liu HL, Hsu PH, Chu PC, et al. Magnetic resonance imaging enhanced by superparamagnetic iron oxide particles: usefulness for distinguishing between focused ultrasound-induced blood-brain barrier disruption and brain hemorrhage. J Magn Reson Imaging 2009;29:31–8
  • Liu HL, Wai YY, Hsu PH, et al. In vivo assessment of macrophage CNS infiltration during disruption of the blood-brain barrier with focused ultrasound: a magnetic resonance imaging study. J Cereb Blood Flow Metab 2010;30:177–86
  • Fan CH, Ting CY, Lin HJ, et al. SPIO-conjugated, doxorubicin-loaded microbubbles for concurrent MRI and focused-ultrasound enhanced brain-tumor drug delivery. Biomaterials 2013;34:3706–15
  • Treat LH, McDannold N, Zhang Y. Improved anti-tumor effect of liposomal doxorubicin after targeted blood-brain barrier disruption by MRI-guided focused ultrasound in rat glioma. Ultrasound Med Biol 2012;38:1716–25
  • Aryal M, Vykhodtseva N, Zhang YZ. Multiple treatments with liposomal doxorubicin and ultrasound-induced disruption of blood-tumor and blood-brain barriers improve outcomes in a rat glioma model. J Control Release 2013;169:103–11
  • Kinoshita M, McDannold N, Jolesz FA, Hynynen K. Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption. Proc Natl Acad Sci USA 2006;103:11719–23
  • Park EJ, Zhang YZ, Vykhodtseva N, McDannold N. Ultrasound-mediated blood-brain/blood-tumor barrier disruption improves outcomes with trastuzumab in a breast cancer brain metastasis model. J Control Release 2012;163:277–84
  • Mei J, Cheng Y, Song Y, et al. Experimental study on targeted methotrexate delivery to the rabbit brain via magnetic resonance imaging-guided focused ultrasound. J Ultrasound Med 2009;28:871–80
  • Cho CW, Liu W, Cobb N, et al. Ultrasound induced mild hyperthermia as a novel approach to increase drug uptake in brain microvessel endothelial cells. Pharm Res 2002;19:1123–9
  • Liu HL, Hua MY, Yang HW, et al. Magnetic resonance monitoring of focused ultrasound/magnetic nanoparticle targeting delivery of therapeutic agents to the brain. Proc Natl Acad Sci USA 2010;107:15205–10
  • Alkins R, Burgess A, Ganguly M, et al. Focused ultrasound delivers targeted immune cells to metastatic brain tumors. Cancer Res 2013;73:1892–9
  • Burgess A, Huang Y, Querbes W, et al. Focused ultrasound for targeted delivery of siRNA and efficient knockdown of Htt expression. J Control Release 2012;163:125–9
  • Choi JJ, Wang S, Brown TR, et al. Noninvasive and transient blood-brain barrier opening in the hippocampus o Alzheimer's double transgenic mice using focused ultrasound. Ultrason Imaging 2008;30:189–200
  • Baseri B, Choi JJ, Deffieux T. Activation of signaling pathways following localized delivery of systemically administered neurotrophic factors across the blood-brain barrier using focused ultrasound and microbubbles. Phys Med Biol 2012;57:65–81
  • Wang F, Shi Y, Lu L, et al. Targeted delivery of GDNF through the blood–brain barrier by MRI-guided focused ultrasound. PLoS One 2012;7:e52925
  • Etame AB, Diaz RJ, O'Reilly MA, et al. Enhanced delivery of gold nanoparticles with therapeutic potential into the brain using MRI-guided focused ultrasound. Nanomed 2012;8:1133–42
  • Thévenot E, Jordão JF, O'Reilly MA, et al. Targeted delivery of scAAV9 to the brain using MRI-guided focused ultrasound. Hum Gene Ther 2012;23:1144–55
  • Hsu PH, Wei KC, Huang CY, et al. Noninvasive and targeted gene delivery into the brain using microbubble-facilitated focused ultrasound. PLoS One 2013;8:e57682
  • Timbie K, Burke C, Nance E, et al. Ultrasound-targeted delivery of systemically administered therapeutic nanoparticles. J Acoust Soc Am 2013;134:4047
  • Tung YS, Marquet F, Teichert T, et al. Feasibility of noninvasive cavitation-guided blood-brain barrier opening using focused ultrasound and microbubbles in nonhuman primates. Appl Phys Lett 2011;98:163704
  • Marquet F, Tung YS, Teichert T, et al. Noninvasive, transient and selective blood-brain barrier opening in non-human primates in vivo. PLoS One 2011;6:e22598
  • 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 2012;72:3652–63
  • Hynynen K, Clement GT, McDannold N, et al. 500-element ultrasound phased array system for noninvasive focal surgery of the brain: a preliminary rabbit study with ex vivo human skulls. Magn Reson Med 2004;52:100–7
  • Jordão JF, Thévenot E, Markham-Coultes K, et al. Amyloid-beta plaque reduction, endogenous antibody delivery and glial activation by brain-targeted, transcranial focused ultrasound. Exp Neurol 2013;248:16–29
  • Scarcelli T, Jordão JF, Ellens N, et al. Effects of transcranial focused ultrasound on hippocampal neurogenesis in adult mice. Brain Stimulat 2014; In press
  • Jalali S, Huang Y, Dumont DJ, Hynynen K. Focused ultrasound-mediated BBB disruption is associated with an increase in activation of AKT: experimental study in rats. BMC Neurol 2010;10:114
  • Tufail Y, Matyushov A, Baldwin N, et al. Transcranial pulsed ultrasound stimulates intact brain circuits. Neuron 2010;66:681–94
  • Tyler WJ, Tufail Y, Finsterwald M, et al. Remote excitation of neuronal circuits using low-intensity, low-frequency ultrasound. PLoS One 2008;3:e3511
  • Legon W, Rowlands A, Opitz A, et al. Pulsed ultrasound differentially stimulates somatosensory circuits in humans as indicated by EEG and FMRI. PLoS One 2012;7:e51177
  • Deffieux T, Younan Y Wattiez N, et al. Low-intensity focused ultrasound modulates monkey visuomotor behavior. Curr Biol 2013;23(2):2430–3
  • Arvanitis CD, Livingstone MS, Vykhodtseva N, McDannold N. Controlled ultrasound-induced blood-brain barrier disruption using passive acoustic emissions monitoring. PLoS One 2012;7:e45783
  • Kaye EA, Chen J, Pauly KB. Rapid MR-ARFI method for focal spot localization during focused ultrasound therapy. Magn Reson Med 2011;65:738–43
  • Jones RM, O'Reilly MA, Hynynen K. Transcranial passive acoustic mapping wtih hemispherical sparse arrays using CT-based skull specific aberration corrections: a simulation study. Phys Med Biol 2013;58:4981–5005
  • O'Reilly MA, Jones RM, Hynynen K. Transcranial bubble activity mapping for therapy and imaging. J Acoust Soc Am 2013;134:3975

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.