Trans-cranial opening of the blood-brain barrier in targeted regions using astereotaxic brain atlas and focused ultrasound energy

Journal of Therapeutic Ultrasound

Volumn 2, Issue 1, 2014, Pages

  Bing, Chenchen ^a   Ladouceur Wodzak, Michelle ^a   Wanner, Clinton R ^a   Shelton, John M ^a   Richardson, James A ^a,b   Chopra, Rajiv ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

BBB opening; Drug delivery; Focused ultrasound; Stereotaxic system

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD BRAIN BARRIER OPENING; CONTROLLED STUDY; DRUG TARGETING; FEMALE; FOCUSED ULTRASOUND; HISTOLOGY; MOUSE; NEUROLOGICAL AND SENSORIAL PROCEDURES; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHANTOM; PRIORITY JOURNAL; RAT; STEREOTACTIC DEVICE; ULTRASOUND;

EID: 84978023700     PISSN: None     EISSN: 20505736     Source Type: Journal    
DOI: 10.1186/2050-5736-2-13     Document Type: Article

References (41)

1. McDannold N, Vykhodtseva N, Hynynen K. Targeted disruption of the blood-brain barrier with focused ultrasound:association with cavitation activity. Phys Med Biol 2006, 51(4):793-807. doi:10.1088/0031-9155/51/4/003, 10.1088/0031-9155/51/4/003, 16467579.
2. Abbott NJ, Chugani DC, Zaharchuk G, Rosen BR, Lo EH. Delivery of imaging agents into brain. Adv Drug Deliv Rev 1999, 37(1-3):253-77.
3. Kroll RA, Neuwelt EA. Outwitting the blood-brain barrier for therapeutic purposes: osmotic opening andother means. Neurosurgery 1998, 42(5):1083-99. discussion 99-100, 10.1097/00006123-199805000-00082, 9588554.
4. Pardridge WM. Blood-brain barrier drug targeting: the future of brain drug development. Mol Interv 2003, 3(2):90-105. doi:10.1124/mi.3.2.90, 10.1124/mi.3.2.90, 14993430.
5. Zhong P, Zhou Y, Zhu S. Dynamics of bubble oscillation in constrained media and mechanisms of vesselrupture in SWL. Ultrasound Med Biol 2001, 27(1):119-34. 10.1016/S0301-5629(00)00322-7, 11295278.
6. Qin S, Ferrara KW. Acoustic response of compliable microvessels containing ultrasound contrastagents. Phys Med Biol 2006, 51(20):5065-88. doi:10.1088/0031-9155/51/20/001, 10.1088/0031-9155/51/20/001, 2847449, 17019026.
7. Collis J, Manasseh R, Liovic P, Tho P, Ooi A, Petkovic-Duran K, Zhu Y. Cavitation microstreaming and stress fields created by microbubbles. Ultrasonics 2010, 50(2):273-9. doi:10.1016/j.ultras.2009.10.002, 10.1016/j.ultras.2009.10.002, 19896683.
8. McDannold N, Vykhodtseva N, Raymond S, Jolesz FA, Hynynen K. MRI-guided targeted blood-brain barrier disruption with focused ultrasound:histological findings in rabbits. Ultrasound Med Biol 2005, 31(11):1527-37. doi:10.1016/j.ultrasmedbio.2005.07.010, 10.1016/j.ultrasmedbio.2005.07.010, 16286030.
9. Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA. Noninvasive MR imaging-guided focal opening of the blood-brain barrier inrabbits. Radiology 2001, 220(3):640-6. doi:10.1148/radiol.2202001804, 10.1148/radiol.2202001804, 11526261.
10. Mesiwala AH, Farrell L, Wenzel HJ, Silbergeld DL, Crum LA, Winn HR, et al. High-intensity focused ultrasound selectively disrupts the blood-brain barrier invivo. Ultrasound Med Biol 2002, 28(3):389-400. 10.1016/S0301-5629(01)00521-X, 11978420.
11. Hynynen K, McDannold N, Sheikov NA, Jolesz FA, Vykhodtseva N. Local and reversible blood-brain barrier disruption by noninvasive focusedultrasound at frequencies suitable for trans-skull sonications. NeuroImage 2005, 24(1):12-20. doi:10.1016/j.neuroimage.2004.06.046, 10.1016/j.neuroimage.2004.06.046, 15588592.
12. Hynynen K, McDannold N, Vykhodtseva N, Raymond S, Weissleder R, Jolesz FA, Sheikov N. Focal disruption of the blood-brain barrier due to 260-kHz ultrasound bursts: amethod for molecular imaging and targeted drug delivery. J Neurosurg 2006, 105(3):445-54. doi:10.3171/jns.2006.105.3.445, 10.3171/jns.2006.105.3.445, 16961141.
13. Liu HL, Pan CH, Ting CY, Hsiao MJ. Opening of the blood-brain barrier by low-frequency (28-kHz) ultrasound: a novelpinhole-assisted mechanical scanning device. Ultrasound Med Biol 2010, 36(2):325-35. doi:10.1016/j.ultrasmedbio.2009.10.004, 10.1016/j.ultrasmedbio.2009.10.004, 20018435.
14. Liu HL, Chen HW, Kuo ZH, Huang WC. Design and experimental evaluations of a low-frequency hemispherical ultrasoundphased-array system for transcranial blood-brain barrier disruption. IEEE Trans Biomed Eng 2008, 55(10):2407-16. doi:10.1109/TBME.2008.925697.
15. Choi JJ, Pernot M, Small SA, Konofagou EE. Noninvasive, transcranial and localized opening of the blood-brain barrier usingfocused ultrasound in mice. Ultrasound Med Biol 2007, 33(1):95-104. doi:10.1016/j.ultrasmedbio.2006.07.018, 10.1016/j.ultrasmedbio.2006.07.018, 17189051.
16. Deffieux T, Konofagou EE. Numerical study of a simple transcranial focused ultrasound system applied toblood-brain barrier opening. IEEE Trans Ultrason Ferroelectr Freq Control 2010, 57(12):2637-53. doi:10.1109/TUFFC.2010.1738, 3968803, 21156360.
17. Chopra R, Curiel L, Staruch R, Morrison L, Hynynen K. An MRI-compatible system for focused ultrasound experiments in small animalmodels. Med Phys 2009, 36(5):1867-74. 10.1118/1.3115680, 2736709, 19544806.
18. O'Reilly MA, Waspe AC, Ganguly M, Hynynen K. Focused-ultrasound disruption of the blood-brain barrier using closely-timed shortpulses: influence of sonication parameters and injection rate. Ultrasound Med Biol 2011, 37(4):587-94. doi:10.1016/j.ultrasmedbio.2011.01.008, 10.1016/j.ultrasmedbio.2011.01.008, 3062725, 21376455.
19. McDannold N, Vykhodtseva N, Jolesz FA, Hynynen K. MRI investigation of the threshold for thermally induced blood-brain barrierdisruption and brain tissue damage in the rabbit brain. Magn Reson Med 2004, 51(5):913-23. doi:10.1002/mrm.20060, 10.1002/mrm.20060, 15122673.
20. Marquet F, Teichert T, Wu SY, Tung YS, Downs M, Wang S, Chen C, Ferrera V, Konofagou EE. Real-time, transcranial monitoring of safe blood-brain barrier opening innon-human primates. PLoS ONE 2014, 9(2):e84310. doi:10.1371/journal.pone.0084310, 10.1371/journal.pone.0084310, 3914779, 24505248.
21. Cho EE, Drazic J, Ganguly M, Stefanovic B, Hynynen K. Two-photon fluorescence microscopy study of cerebrovascular dynamics inultrasound-induced blood-brain barrier opening. J Cereb Blood Flow Metab 2011, 31(9):1852-62. doi:10.1038/jcbfm.2011.59, 10.1038/jcbfm.2011.59, 3185881, 21505473.
22. Raymond SB, Treat LH, Dewey JD, McDannold NJ, Hynynen K, Bacskai BJ. Ultrasound enhanced delivery of molecular imaging and therapeutic agents inAlzheimer's disease mouse models. PLoS ONE 2008, 3(5):e2175. doi:10.1371/journal.pone.0002175, 10.1371/journal.pone.0002175, 2364662, 18478109.
23. King RL, Liu Y, Maruvada S, Herman BA, Wear KA, Harris GR. Development and characterization of a tissue-mimicking material for high-intensityfocused ultrasound. IEEE Trans Ultrason Ferroelectr Freq Control 2011, 58(7):1397-405. doi:10.1109/TUFFC.2011.1959.
24. Shehan DC, Hrapchak BB. Theory and Practice of Histotechnology 1980, Columbus: Battelle Press, 2.
25. Woods AE. Laboratory Histopathology: a Complete Reerence 1996, Edinburgh: Churchill-Livingston Press.
26. Shelton JM, Grauer G, Richardson JA., Inventors Combination Low Magnification Dark-Field Illuminator and Bright-Field MicroscopySubstage Condenser with Descriptions and Modifications to Manufacture This Devicefrom Commercially Available Fiber-Optic Ringlights UTSD 1494 Inventors.
27. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclearDNA fragmentation. J Cell Biol 1992, 119(3):493-501. 10.1083/jcb.119.3.493, 2289665, 1400587.
28. O'Reilly MA, Muller A, Hynynen K. Ultrasound insertion loss of rat parietal bone appears to be proportional toanimal mass at submegahertz frequencies. Ultrasound Med Biol 2011, 37(11):1930-7. doi:10.1016/j.ultrasmedbio.2011.08.001, 10.1016/j.ultrasmedbio.2011.08.001, 3228246, 21925788.
29. Huang Y, Hynynen K. MR-guided focused ultrasound for brain ablation and blood-brain barrierdisruption. Methods Mol Biol. 2011, 711:579-93. doi:10.1007/978-1-61737-992-5_30, 10.1007/978-1-61737-992-5_30, 21279624.
30. McDannold N, Vykhodtseva N, Hynynen K. Blood-brain barrier disruption induced by focused ultrasound and circulatingpreformed microbubbles appears to be characterized by the mechanical index. Ultrasound Med Biol 2008, 34(5):834-40. doi:10.1016/j.ultrasmedbio.2007.10.016, 10.1016/j.ultrasmedbio.2007.10.016, 2442477, 18207311.
31. Mcdannold N, Vykhodtseva N, Hynynen K. Effects of acoustic parameters and ultrasound contrast agent dose onfocused-ultrasound induced blood-brain barrier disruption. Ultrasound Med Biol 2008, 34(6):930-7. doi:10.1016/j.ultrasmedbio.2007.11.009, 10.1016/j.ultrasmedbio.2007.11.009, 2459318, 18294757.
32. Bing KF, Howles GP, Qi Y, Palmeri ML, Nightingale KR. Blood-brain barrier (BBB) disruption using a diagnostic ultrasound scanner andDefinity® in mice. Ultrasound Med Biol 2009, 35(8):1298-308. doi:10.1016/j.ultrasmedbio.2009.03.012, 10.1016/j.ultrasmedbio.2009.03.012, 2729364, 19545939.
33. Chopra R, Vykhodtseva N, Hynynen K. Influence of exposure time and pressure amplitude on blood-brain-barrier openingusing transcranial ultrasound exposures. ACS Chem Neurosci 2010, 1(5):391-8. doi:10.1021/cn9000445, 10.1021/cn9000445, 2885821,2885821, 20563295.
34. Choi JJ, Feshitan JA, Baseri B, Wang S, Tung YS, Borden MA, Konofagou EE. Microbubble-size dependence of focused ultrasound-induced blood-brain barrieropening in mice in vivo. IEEE Trans Biomed Eng 2010, 57(1):145-54. doi:10.1109/TBME.2009.2034533, 3968777, 19846365.
35. Treat LH, McDannold N, Vykhodtseva N, Zhang Y, Tam K, Hynynen K. Targeted delivery of doxorubicin to the rat brain at therapeutic levels usingMRI-guided focused ultrasound. Int J Cancer J Int du cancer 2007, 121(4):901-7. doi:10.1002/ijc.22732.
36. Yang FY, Fu WM, Chen WS, Yeh WL, Lin WL. Quantitative evaluation of the use of microbubbles with transcranial focusedultrasound on blood-brain-barrier disruption. Ultrason Sonochem 2008, 15(4):636-43. doi:10.1016/j.ultsonch.2007.08.003, 10.1016/j.ultsonch.2007.08.003, 17910929.
37. Nhan T, Burgess A, Cho EE, Stefanovic B, Lilge L, Hynynen K. Drug delivery to the brain by focused ultrasound induced blood-brain barrierdisruption: quantitative evaluation of enhanced permeability of cerebralvasculature using two-photon microscopy. J Control Release 2013, 172(1):274-80. doi:10.1016/j.jconrel.2013.08.029, 10.1016/j.jconrel.2013.08.029, 24008151.
38. Hawkins BT, Egleton RD. Fluorescence imaging of blood-brain barrier disruption. J Neurosci Methods 2006, 151(2):262-7. doi:10.1016/j.jneumeth.2005.08.006, 10.1016/j.jneumeth.2005.08.006, 16181683.
39. Liu HL, Jan CK, Chu PC, Hong JC, Lee PY, Hsu JD, Lin CC, Huang CY, Chen PY, Wei KC. Design and experimental evaluation of a 256-channel dual-frequency ultrasoundphased-array system for transcranial blood-brain barrier opening and brain drugdelivery. IEEE Trans Biomed Eng 2014, 61(4):1350-60. doi:10.1109/TBME.2014.2305723.
40. Arvanitis CD, Livingstone MS, Vykhodtseva N, McDannold N. Controlled ultrasound-induced blood-brain barrier disruption using passiveacoustic emissions monitoring. PLoS ONE 2012, 7(9):e45783. doi:10.1371/journal.pone.0045783, 10.1371/journal.pone.0045783, 3454363, 23029240.
41. O'Reilly MA, Hynynen K. Blood-brain barrier: real-time feedback-controlled focused ultrasound disruptionby using an acoustic emissions-based controller. Radiology 2012, 263(1):96-106. doi:10.1148/radiol.11111417, 10.1148/radiol.11111417, 3309801, 22332065.