About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 627496, 13 pages
http://dx.doi.org/10.1155/2013/627496
Research Article

Pharmacodynamic Analysis of Magnetic Resonance Imaging-Monitored Focused Ultrasound-Induced Blood-Brain Barrier Opening for Drug Delivery to Brain Tumors

1Department of Electrical Engineering, Chang-Gung University, 259 Wen-Hwa 1st Road, Kwei-Shan, Tao-Yuan 333, Taiwan
2Department of Diagnostic Radiology, Chang-Gung University and Memorial Hospital, 5 Fu-shin Street, Kwei-Shan, Tao-Yuan 333, Taiwan
3Department of Medical Imaging and Radiological Sciences, Chang-Gung University, 259 Wen-Hwa 1st Road, Kwei-Shan, Tao-Yuan 333, Taiwan
4Department of Neurosurgery, Chang-Gung Memorial Hospital, 5 Fu-shin Street, Kwei-Shan, Tao-Yuan 333, Taiwan

Received 21 January 2013; Accepted 25 February 2013

Academic Editor: Fan-Lin Kong

Copyright © 2013 Po-Chun Chu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Hynynen, N. McDannold, N. Vykhodtseva, and F. A. Jolesz, “Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits,” Radiology, vol. 220, no. 3, pp. 640–646, 2001. View at Scopus
  2. 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, vol. 24, no. 1, pp. 12–20, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Hynynen, N. McDannold, N. Vykhodtseva et al., “Focal disruption of the blood-brain barrier due to 260-kHz ultrasound bursts: a method for molecular imaging and targeted drug delivery,” Journal of Neurosurgery, vol. 105, no. 3, pp. 445–454, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Kinoshita, N. McDannold, F. A. Jolesz, and K. Hynynen, “Targeted delivery of antibodies through the blood-brain barrier by MRI-guided focused ultrasound,” Biochemical and Biophysical Research Communications, vol. 340, no. 4, pp. 1085–1090, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. 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 in Medicine and Biology, vol. 34, no. 6, pp. 930–937, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. H. L. Liu, Y. Y. Wai, W. S. Chen et al., “Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging,” Ultrasound in Medicine and Biology, vol. 34, no. 4, pp. 598–606, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. H. L. Liu, P. H. Hsu, P. N. Chu 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,” Journal of Magnetic Resonance Imaging, vol. 29, no. 1, pp. 31–38, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. 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,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 31, pp. 11719–11723, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. 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,” International Journal of Cancer, vol. 121, no. 4, pp. 901–907, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Mei, Y. Cheng, Y. Song et al., “Experimental study on targeted methotrexate delivery to the rabbit brain via magnetic resonance imaging-guided focused ultrasound,” Journal of Ultrasound in Medicine, vol. 28, no. 7, pp. 871–880, 2009. View at Scopus
  11. H. L. Liu, M. Y. Hua, P. Y. Chen et al., “Blood-brain barrier disruption with focused ultrasound enhances delivery of chemotherapeutic drugs for glioblastoma treatment,” Radiology, vol. 255, no. 2, pp. 415–425, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. W. M. Pardridge, “The blood-brain barrier: bottleneck in brain drug development,” NeuroRx, vol. 2, no. 1, pp. 3–14, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Jemal, R. Siegel, E. Ward et al., “Cancer statistics, 2006,” CA: A Cancer Journal for Clinicians, vol. 56, no. 2, pp. 106–130, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. S. A. Grossman and J. F. Batara, “Current management of glioblastoma multiforme,” Seminars in Oncology, vol. 31, no. 5, pp. 635–644, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. L. H. Treat, N. McDannold, Y. Zhang, N. Vykhodtseva, and K. Hynynen, “Improved anti-tumor effect of liposomal doxorubicin after targeted blood-brain barrier disruption by MRI-guided focused ultrasound in rat glioma,” Ultrasound in Medicine and Biology, vol. 38, no. 10, pp. 1716–1725, 2012. View at Publisher · View at Google Scholar
  16. H. L. Liu, M. Y. Hua, H. W. Yang et al., “Magnetic resonance monitoring of focused ultrasound/magnetic nanoparticle targeting delivery of therapeutic agents to the brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 34, pp. 15205–15210, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Liu, G. Wen, X. F. Lv et al., “MR imaging of cerebral extraventricular neurocytoma: a report of 9 cases,” The American Journal of Neuroradiology, 2012. View at Publisher · View at Google Scholar
  18. 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 in Medicine and Biology, vol. 34, no. 5, pp. 834–840, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. N. Vykhodtseva, N. McDannold, and K. Hynynen, “Progress and problems in the application of focused ultrasound for blood-brain barrier disruption,” Ultrasonics, vol. 48, no. 4, pp. 279–296, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. 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,” Ultrasonics Sonochemistry, vol. 15, no. 4, pp. 636–643, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. 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 in Medicine and Biology, vol. 33, no. 9, pp. 1421–1427, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. J. J. Choi, J. A. Feshitan, B. Baseri et al., “Microbubble-size dependence of focused ultrasound-induced bloodBrain barrier opening in mice in vivo,” IEEE Transactions on Biomedical Engineering, vol. 57, no. 1, pp. 145–154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Chopra, N. Vykhodtseva, and K. Hynynen, “Influence of exposure time and pressure amplitude on blood-brain-barrier opening using transcranial ultrasound exposures,” ACS Chemical Neuroscience, vol. 1, no. 5, pp. 391–398, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Park, Y. Zhang, N. Vykhodtseva, F. A. Jolesz, and N. J. McDannold, “The kinetics of blood brain barrier permeability and targeted doxorubicin delivery into brain induced by focused ultrasound,” Journal of Controlled Release, vol. 162, no. 1, pp. 134–142, 2012. View at Publisher · View at Google Scholar
  25. P. S. Tofts and A. G. Kermode, “Measurement of the blood-brain barrier permeability and leakage space using dynamic MR imaging. 1. Fundamental concepts,” Magnetic Resonance in Medicine, vol. 17, no. 2, pp. 357–367, 1991. View at Scopus
  26. 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,” Magnetic Resonance in Medicine, vol. 66, no. 3, pp. 821–830, 2011. View at Publisher · View at Google Scholar
  27. I. M. Noebauer-Huhmann, P. Szomolanyi, V. Juras, O. Kraff, M. E. Ladd, and S. Trattnig, “Gadolinium-based magnetic resonance contrast agents at 7 tesla: in vitro T1 relaxivities in human blood plasma,” Investigative Radiology, vol. 45, no. 9, pp. 554–558, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. E. A. Neuwelt, P. A. Barnett, C. I. McCormick, L. G. Remsen, R. A. Kroll, and G. Sexton, “Differential permeability of a human brain tumor xenograft in the nude rat: impact of tumor size and method of administration on optimizing delivery of biologically diverse agents,” Clinical Cancer Research, vol. 4, no. 6, pp. 1549–1555, 1998. View at Scopus
  29. H. Sarin, A. S. Kanevsky, H. Wu et al., “Effective transvascular delivery of nanoparticles across the blood-brain tumor barrier into malignant glioma cells,” Journal of Translational Medicine, vol. 6, article 80, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. A. R. Padhani and J. E. Husband, “Dynamic contrast-enhanced MRI studies in oncology with an emphasis on quantification, validation and human studies,” Clinical Radiology, vol. 56, no. 8, pp. 607–620, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. P. S. Tofts, G. Brix, D. L. Buckley et al., “Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols,” Journal of Magnetic Resonance Imaging, vol. 10, no. 3, pp. 223–232, 1999. View at Publisher · View at Google Scholar
  32. H. Olsson, C. Halldin, C. G. Swahn, and L. Farde, “Quantification of [11C]FLB 457 binding to extrastriatal dopamine receptors in the human brain,” Journal of Cerebral Blood Flow and Metabolism, vol. 19, no. 10, pp. 1164–1173, 1999. View at Scopus
  33. K. W. Kang, D. S. Lee, J. H. Cho et al., “Quantification of F-18 FDG PET images in temporal lobe epilepsy patients using probabilistic brain atlas,” NeuroImage, vol. 14, no. 1, part 1, pp. 1–6, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. S. L. Bacharach, S. K. Libutti, and J. A. Carrasquillo, “Measuring tumor blood flow with H2O15: practical considerations,” Nuclear Medicine and Biology, vol. 27, no. 7, pp. 671–676, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. M. S. Alavijeh and A. M. Palmer, “Measurement of the pharmacokinetics and pharmacodynamics of neuroactive compounds,” Neurobiology of Disease, vol. 37, no. 1, pp. 38–47, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. H. F. Dvorak, L. F. Brown, M. Detmar, and A. M. Dvorak, “Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis,” The American Journal of Pathology, vol. 146, no. 5, pp. 1029–1039, 1995. View at Scopus
  37. L. E. Benjamin, D. Golijanin, A. Itin, D. Pode, and E. Keshet, “Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal,” Journal of Clinical Investigation, vol. 103, no. 2, pp. 159–165, 1999. View at Scopus
  38. J. S. Taylor, P. S. Tofts, R. Port et al., “MR imaging of tumor microcirculation: promise for the new millennium,” Journal of Magnetic Resonance Imaging, vol. 10, no. 6, pp. 903–907, 1999. View at Publisher · View at Google Scholar
  39. L. F. Brown, K. T. Yeo, B. Berse et al., “Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing,” Journal of Experimental Medicine, vol. 176, no. 5, pp. 1375–1379, 1992. View at Publisher · View at Google Scholar · View at Scopus
  40. 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 in Medicine and Biology, vol. 37, no. 11, pp. 1930–1937, 2011. View at Publisher · View at Google Scholar
  41. 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,” Physics in Medicine and Biology, vol. 55, no. 18, pp. 5251–5267, 2010. View at Publisher · View at Google Scholar · View at Scopus