The kinetics of blood brain barrier permeability and targeted doxorubicin delivery into brain induced by focused ultrasound

Journal of Controlled Release

Volumn 162, Issue 1, 2012, Pages 134-142

  Park, Juyoung ^a   Zhang, Yongzhi ^a   Vykhodtseva, Natalia ^a   Jolesz, Ferenc A ^a   McDannold, Nathan J ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Blood brain barrier disruption; Dynamic contrast enhanced MRI; Focused ultrasound; Pharmacokinetic model

Indexed keywords

BLOOD-BRAIN BARRIER; CHEMOTHERAPY AGENTS; CONFIDENCE INTERVAL; DCE-MRI; DEFINITY; DOXORUBICIN; DYNAMIC CONTRAST ENHANCED MRI; EXPERIMENTAL GROUPS; FOCUSED ULTRASOUND; FUNCTION OF TIME; GD-DTPA; LINEAR CORRELATION; MICRO-BUBBLE; MICROBUBBLE AGENTS; MRI CONTRAST AGENTS; ORDERS OF MAGNITUDE; PHARMACOKINETIC MODEL; TARGETED DELIVERY; TIME INTERVAL; TIME POINTS; TRANSFER COEFFICIENT; ULTRASOUND CONTRAST AGENT; VASCULATURE;

BLOOD; CHEMOTHERAPY; DRUG DELIVERY; GADOLINIUM; MAGNETIC RESONANCE IMAGING; ULTRASONICS;

SONICATION;

DOXORUBICIN; GADOLINIUM PENTETATE; PERFLUTREN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG HALF LIFE; DRUG PENETRATION; FOCUSED ULTRASOUND; HEMISPHERE; HISTOLOGY; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; ULTRASOUND; ULTRASOUND TRANSDUCER;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BLOOD-BRAIN BARRIER; BRAIN; CAPILLARY PERMEABILITY; CONTRAST MEDIA; DOXORUBICIN; DRUG DELIVERY SYSTEMS; GADOLINIUM DTPA; MAGNETIC RESONANCE IMAGING; MALE; MICROBUBBLES; MODELS, BIOLOGICAL; RATS; RATS, SPRAGUE-DAWLEY; SONICATION;

EID: 84864653876     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.06.012     Document Type: Article

References (51)

1. K. Hynynen, N. McDannold, N.A. Sheikov, F.A. Jolesz, and N. Vykhodtseva Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications Neuroimage 24 1 2005 12 20
2. K. Hynynen, N. McDannold, N. Vykhodtseva, and F.A. Jolesz Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits Radiology 220 3 2001 640 646
3. K. Hynynen, N. McDannold, N. Vykhodtseva, S. Raymond, R. Weissleder, F.A. Jolesz, and N. Sheikov Focal disruption of the blood-brain barrier due to 260-kHz ultrasound bursts: a method for molecular imaging and targeted drug delivery J. Neurosurg. 105 3 2006 445 454
4. K. Hynynen, N. McDannold, N. Vykhodtseva, S. Raymond, R. Weissleder, F.A. Jolesz, and N. Sheikov Focal disruption of the blood-brain barrier due to 260-kHz ultrasound bursts: a method for molecular imaging and targeted drug delivery J. Neurosurg. 105 3 2006 445 454
5. N. McDannold, N. Vykhodtseva, and K. Hynynen Targeted disruption of the blood-brain barrier with focused ultrasound: association with cavitation activity Phys. Med. Biol. 51 4 2006 793 807
6. N. McDannold, N. Vykhodtseva, and K. Hynynen Effects of acoustic parameters and ultrasound contrast agent dose on focused-ultrasound induced blood-brain barrier disruption Ultrasound Med. Biol. 34 6 2008 930 937
7. M. Kinoshita, N. McDannold, F.A. Jolesz, and K. Hynynen Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption Proc. Natl. Acad. Sci. U. S. A. 103 31 2006 11719 11723
8. H.L. Liu, M.Y. Hua, P.Y. Chen, P.C. Chu, C.H. Pan, H.W. Yang, C.Y. Huang, J.J. Wang, T.C. Yen, and K.C. Wei Blood-brain barrier disruption with focused ultrasound enhances delivery of chemotherapeutic drugs for glioblastoma treatment Radiology 255 2 2010 415 425
9. J. Mei, Y. Cheng, Y. Song, Y. Yang, F. Wang, Y. Liu, and Z. Wang Experimental study on targeted methotrexate delivery to the rabbit brain via magnetic resonance imaging-guided focused ultrasound J. Ultrasound Med. 28 7 2009 871 880
10. L.H. Treat, N. McDannold, N. Vykhodtseva, Y. Zhang, K. Tam, and K. Hynynen Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound Int. J. Cancer 121 4 2007 901 907
11. N. Sheikov, N. McDannold, F. Jolesz, Y.Z. Zhang, K. Tam, and K. Hynynen Brain arterioles show more active vesicular transport of blood-borne tracer molecules than capillaries and venules after focused ultrasound-evoked opening of the blood-brain barrier Ultrasound Med. Biol. 32 9 2006 1399 1409
12. N. Sheikov, N. McDannold, N. Vykhodtseva, F. Jolesz, and K. Hynynen Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles Ultrasound Med. Biol. 30 7 2004 979 989
13. N. Sheikov, N. McDannold, S. Sharma, and K. Hynynen Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium Ultrasound Med. Biol. 34 7 2008 1093 1104
14. F.Y. Yang, T.T. Wong, M.C. Teng, R.S. Liu, M. Lu, H.F. Liang, and M.C. Wei Focused ultrasound and interleukin-4 receptor-targeted liposomal doxorubicin for enhanced targeted drug delivery and antitumor effect in glioblastoma multiforme J. Control. Release 160 3 2012 652 658
15. J.F. Jordao, C.A. Ayala-Grosso, K. Markham, Y. Huang, R. Chopra, J. McLaurin, K. Hynynen, and I. Aubert 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 5 5 2010 e10549
16. S.B. Raymond, L.H. Treat, J.D. Dewey, N.J. McDannold, K. Hynynen, and B.J. Bacskai Ultrasound enhanced delivery of molecular imaging and therapeutic agents in Alzheimer's disease mouse models PLoS One 3 5 2008 e2175
17. R.R. Lonser, R. Schiffman, R.A. Robison, J.A. Butman, Z. Quezado, M.L. Walker, P.F. Morrison, S. Walbridge, G.J. Murray, D.M. Park, R.O. Brady, and E.H. Oldfield Image-guided, direct convective delivery of glucocerebrosidase for neuronopathic Gaucher disease Neurology 68 4 2007 254 261
18. R.R. Lonser, K.E. Warren, J.A. Butman, Z. Quezado, R.A. Robison, S. Walbridge, R. Schiffman, M. Merrill, M.L. Walker, D.M. Park, D. Croteau, R.O. Brady, and E.H. Oldfield Real-time image-guided direct convective perfusion of intrinsic brainstem lesions. Technical note J. Neurosurg. 107 1 2007 190 197
19. M. Kinoshita, N. McDannold, F.A. Jolesz, and K. Hynynen Targeted delivery of antibodies through the blood-brain barrier by MRI-guided focused ultrasound Biochem. Biophys. Res. Commun. 340 4 2006 1085 1090
20. N. McDannold, N. Vykhodtseva, and K. Hynynen Blood-brain barrier disruption induced by focused ultrasound and circulating preformed microbubbles appears to be characterized by the mechanical index Ultrasound Med. Biol. 34 5 2008 834 840
21. N. Vykhodtseva, N. McDannold, and K. Hynynen Progress and problems in the application of focused ultrasound for blood-brain barrier disruption Ultrasonics 48 4 2008 279 296
22. F.Y. Yang, W.M. Fu, W.S. Chen, W.L. Yeh, and W.L. Lin Quantitative evaluation of the use of microbubbles with transcranial focused ultrasound on blood-brain-barrier disruption Ultrason. Sonochem. 15 4 2008 636 643
23. F.Y. Yang, W.M. Fu, R.S. Yang, H.C. Liou, K.H. Kang, and W.L. Lin Quantitative evaluation of focused ultrasound with a contrast agent on blood-brain barrier disruption Ultrasound Med. Biol. 33 9 2007 1421 1427
24. J.J. Choi, J.A. Feshitan, B. Baseri, S. Wang, Y.S. Tung, M.A. Borden, and E.E. Konofagou Microbubble-size dependence of focused ultrasound-induced blood-brain barrier opening in mice in vivo IEEE Trans. Biomed. Eng. 57 1 2010 145 154
25. R. Chopra, N. Vykhodtseva, and K. Hynynen Influence of exposure time and pressure amplitude on blood-brain-barrier opening using transcranial ultrasound exposures ACS Chem. Neurosci. 1 5 2010 391 398
26. P.S. Tofts, and A.G. Kermode Measurement of the blood-brain barrier permeability and leakage space using dynamic MR imaging. 1. Fundamental concepts Magn. Reson. Med. 17 2 1991 357 367
27. F. Vlachos, Y.S. Tung, and E. Konofagou Permeability dependence study of the focused ultrasound-induced blood-brain barrier opening at distinct pressures and microbubble diameters using DCE-MRI Magn. Reson. Med. 66 3 2011 821 830
28. F. Vlachos, Y.S. Tung, and E.E. Konofagou Permeability assessment of the focused ultrasound-induced blood-brain barrier opening using dynamic contrast-enhanced MRI Phys. Med. Biol. 55 18 2010 5451 5466
29. M. Pilatou, N. Vykhodtseva, and N. McDannold Blood-brain barrier disruption in rats induced by focused ultrasound under MRI guidance: a safety study MR-Guided Focused Ultrasound Symposium, Washington, DC 2008
30. S.B. Raymond, J. Skoch, K. Hynynen, and B.J. Bacskai Multiphoton imaging of ultrasound/Optison mediated cerebrovascular effects in vivo J. Cereb. Blood Flow Metab. 27 2 2007 393 403
31. H. von Holst, E. Knochenhauer, H. Blomgren, V.P. Collins, L. Ehn, M. Lindquist, G. Noren, and C. Peterson Uptake of adriamycin in tumour and surrounding brain tissue in patients with malignant gliomas Acta Neurochir. (Wien) 104 1-2 1990 13 16
32. N.R. Bachur, A.L. Moore, J.G. Bernstein, and A. Liu Tissue distribution and disposition of daunomycin (NCS-82151) in mice: fluorometric and isotopic methods Cancer Chemother. 54 2 1970 89 94
33. A. Rahman, D. Carmichael, M. Harris, and J.K. Roh Comparative pharmacokinetics of free doxorubicin and doxorubicin entrapped in cardiolipin liposomes Cancer Res. 46 5 1986 2295 2299
34. L. Bakay, H.T. Ballantine Jr., T.F. Hueter, and D. Sosa Ultrasonically produced changes in the blood-brain barrier AMA Arch. Neurol. Psychiatry 76 5 1956 457 467
35. V.S. Vexler, O. Clement, H. Schmitt-Willich, and R.C. Brasch Effect of varying the molecular weight of the MR contrast agent Gd-DTPA-polylysine on blood pharmacokinetics and enhancement patterns J. Magn. Reson. Imaging 4 3 1994 381 388
36. K.L. Li, X.P. Zhu, J. Waterton, and A. Jackson Improved 3D quantitative mapping of blood volume and endothelial permeability in brain tumors J. Magn. Reson. Imaging 12 2 2000 347 357
37. D.P. Barboriak, J.R. MacFall, A.O. Padua, G.E. York, B.L. Viglianti, and M.W. Dewhirst Standardized software for calculation of Ktrans and vp from dynamic T1-weighted MR images The International Society for Magnetic Resonance in Medicine Workshop McLean VA 2004
38. H. Daldrup, D.M. Shames, M. Wendland, Y. Okuhata, T.M. Link, W. Rosenau, Y. Lu, and R.C. Brasch Correlation of dynamic contrast-enhanced MR imaging with histologic tumor grade: comparison of macromolecular and small-molecular contrast media AJR Am. J. Roentgenol. 171 4 1998 941 949
39. M.A. O'Reilly, A. Muller, and K. Hynynen Ultrasound insertion loss of rat parietal bone appears to be proportional to animal mass at submegahertz frequencies Ultrasound Med. Biol. 37 11 2011 1930 1937
40. M.A. O'Reilly, Y. Huang, and K. Hynynen The impact of standing wave effects on transcranial focused ultrasound disruption of the blood-brain barrier in a rat model Phys. Med. Biol. 55 18 2010 5251 5267
41. F.Y. Yang, Y.S. Lin, K.H. Kang, and T.K. Chao Reversible blood-brain barrier disruption by repeated transcranial focused ultrasound allows enhanced extravasation J. Control. Release 150 1 2011 111 116
42. A. Di Marco, M. Gaetani, and B. Scarpinato Adriamycin (NSC-123,127): a new antibiotic with antitumor activity Cancer Chemother. 53 1 1969 33 37
43. G. Bonadonna, S. Monfardini, M. De Lena, F. Fossati-Bellani, and G. Beretta Phase I and preliminary phase II evaluation of adriamycin (NSC 123127) Cancer Res. 30 10 1970 2572 2582
44. K. Xiao, J. Luo, Y. Li, J.S. Lee, G. Fung, and K.S. Lam PEG-oligocholic acid telodendrimer micelles for the targeted delivery of doxorubicin to B-cell lymphoma J. Control. Release 155 2 2011 272 281
45. J.J. Wang, E. Cortes, L.F. Sinks, and J.F. Holland Therapeutic effect and toxicity of adriamycin in patients with neoplastic disease Cancer 28 4 1971 837 843
46. E. Middleman, J. Luce, and E. Frei III Clinical trials with adriamycin Cancer 28 4 1971 844 850
47. S. Monfardini, G. Bonadonna, S. Di Pietro, A. Guindani, F. Fossati-Bellani, and M. De Lena Clinical trials with adriamycin in leukemia and solid tumors Tumori 55 4 1969 197 216
48. L. Guo, L. Fan, Z. Pang, J. Ren, Y. Ren, J. Li, J. Chen, Z. Wen, and X. Jiang TRAIL and doxorubicin combination enhances anti-glioblastoma effect based on passive tumor targeting of liposomes J. Control. Release 154 1 2011 93 102
49. A.C. Stan, S. Casares, D. Radu, G.F. Walter, and T.D. Brumeanu Doxorubicin-induced cell death in highly invasive human gliomas Anticancer Res. 19 2A 1999 941 950
50. J. Cummings, and C.S. McArdle Studies on the in vivo disposition of adriamycin in human tumours which exhibit different responses to the drug Br. J. Cancer 53 6 1986 835 838
51. N. McDannold, N. Vykhodtseva, S. Raymond, F.A. Jolesz, and K. Hynynen MRI-guided targeted blood-brain barrier disruption with focused ultrasound: histological findings in rabbits Ultrasound Med. Biol. 31 11 2005 1527 1537