Multi-modality safety assessment of blood-brain barrier opening using focused ultrasound and definity microbubbles: A short-term study

Ultrasound in Medicine and Biology

Volumn 36, Issue 9, 2010, Pages 1445-1459

  Baseri, Babak ^a   Choi, James J ^a   Tung, Yao Sheng ^a   Konofagou, Elisa E ^a,b  

^a Columbia University ^*  (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Blood brain barrier opening; Definity microbubbles; Focused ultrasound; Hippocampus; Histological damage; Safety assessment

Indexed keywords

BLOOD-BRAIN BARRIER; DEFINITY; FOCUSED ULTRASOUND; HIPPOCAMPUS; HISTOLOGICAL DAMAGE; SAFETY ASSESSMENTS;

BLOOD; DRUG DELIVERY; FLUORESCENCE; MAGNETIC RESONANCE IMAGING; RESONANCE; SONICATION; ULTRASONICS;

DAMAGE DETECTION;

DEXTRAN; ECHO CONTRAST MEDIUM; EOSIN; GADODIAMIDE; GADOLINIUM; HEMATOXYLIN; PERFLUTREN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN TISSUE; DENTATE GYRUS; DRUG DELIVERY SYSTEM; ERYTHROCYTE; FLUORESCENCE; FLUORESCENCE IMAGING; FOCUSED ULTRASOUND; HIPPOCAMPUS; HISTOLOGY; MALE; MICROBUBBLE; MOUSE; NERVE CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RISK ASSESSMENT; SOUND PRESSURE; STAINING; THALAMUS; TISSUE INJURY; TISSUE SECTION; ULTRASOUND;

ANIMALS; BLOOD-BRAIN BARRIER; DRUG DELIVERY SYSTEMS; MALE; MICE; MICE, INBRED C57BL; MICROBUBBLES; RADIOACTIVE TRACERS; SAFETY; TIME FACTORS;

EID: 77956023302     PISSN: 03015629     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ultrasmedbio.2010.06.005     Document Type: Article

References (50)

1. Abbott N.J., Ronnback L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006, 7:41-53.
2. Bakay L., Ballantine H.T., Hueter T.F., Sosa D. Ultrasonically produced changes in the blood-brain barrier. AMA Arch Neurol Psychiatry 1956, 76:457-467.
3. Ballantine H.T., Hueter T.F., Nauta W.J., Sosa D.M. Focal destruction of nervous tissue by focused ultrasound: Biophysical factors influencing its application. J Exp Med 1956, 104:337-360.
4. Bobo R.H., Laske D.W., Akbasak A., Morrison P.F., Dedrick R.L., Oldfield E.H. Convection-enhanced delivery of macromolecules in the brain. Proc Natl Acad Sci U S A 1994, 91:2076-2080.
5. Cammermeyer J. The post-mortem origin and mechanism of neuronal hyperchromatosis and nuclear pyknosis. Exp Neurol 1960, 2:379-405.
6. Cammermeyer J. Is the solitary dark neuron a manifestation of postmortem trauma to the brain inadequately fixed by perfusion?. Histochemistry 1978, 56:97-115.
7. Charriaut-Marlangue C., Remolleau S., Aggoun-Zouaoui D., Ben-Ari Y. Apoptosis and programmed cell death: A role in cerebral ischemia. Biomed Pharmacother 1998, 52:264-269.
8. Chen J., Jin K., Chen M., Pei W., Kawaguchi K., Greenberg D.A., Simon R.P. Early detection of DNA strand breaks in the brain after transient focal ischemia: Implications for the role of DNA damage in apoptosis and neuronal cell death. J Neurochem 1997, 69:232-245.
9. Choi J.J., Pernot M., Brown T.R., Small S.A., Konofagou E.E. Spatio-temporal analysis of molecular delivery through the blood-brain barrier using focused ultrasound. Phys Med Biol 2007, 52:5509-5530.
10. Choi J.J., Pernot M., Small S.A., Konofagou E.E. Noninvasive, transcranial and localized opening of the blood-brain barrier using focused ultrasound in mice. Ultrasound Med Biol 2007, 33:95-104.
11. Choi J.J., Wang S., Brown T.R., Small S.A., Duff K.E., Konofagou E.E. Noninvasive and transient blood-brain barrier opening in the hippocampus of Alzheimer's double transgenic mice using focused ultrasound. Ultrason Imaging 2008, 30:189-200.
12. Choi J.J., Wang S., Tung Y.S., Morrison B., Konofagou E.E. Molecules of various pharmacologically-relevant sizes can cross the ultrasound-induced blood-brain barrier opening in vivo. Ultrasound Med Biol 2010, 36:58-67.
13. Choi J.J., Feshitan J.A., Baseri B., Wang S., Borden M.A., Konofagou E.E. Microbubble-size dependence of focused ultrasound-induced blood-brain barrier opening in mice in vivo. IEEE Trans Biomed Eng 2010, 57:145-154.
14. Fischer H., Gottschlich R., Seelig A. Blood-brain barrier permeation: Molecular parameters governing passive diffusion. J Membr Biol 1998, 165:201-211.
15. Habgood M.D., Begley D.J., Abbott N.J. Determinants of passive drug entry into the central nervous system. Cell Mol Neurobiol 2000, 20:231-253.
16. Hynynen K. Ultrasound for drug and gene delivery to the brain. Adv Drug Deliv Rev 2008, 60:1209-1217.
17. Hynynen K., McDannold N., Sheikov N.A., Jolesz F.A., Vykhodtseva N. Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. Neuroimage 2005, 24:12-20.
18. Hynynen K., McDannold N., Vykhodtseva N., Jolesz F.A. Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 2001, 220:640-646.
19. Hynynen K., McDannold N., Vykhodtseva N., Raymond S., Weissleder R., Jolesz F.A., Sheikov N. 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, 105:445-454.
20. Jortner B.S. Neuropathological assessment in acute neurotoxic states. The ″ dark″ neuron. J Med CBR Def 2005, 3:1-5.
21. Kinoshita M., McDannold N., Jolesz F.A., 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 U S A 2006, 103:11719-11723.
22. Kinoshita M., McDannold N., Jolesz F.A., Hynynen K. Targeted delivery of antibodies through the blood-brain barrier by MRI-guided focused ultrasound. Biochem Biophys Res Commun 2006, 340:1085-1090.
23. Kogure T., Kogure K. Molecular and biochemical events within the brain subjected to cerebral ischemia (targets for therapeutical intervention). Clin Neurosci 1997, 4:179-183.
24. Konofagou E.E., Choi J.J., Baseri B., Tung Y.-S. Mechanism and safety of FUS-induced BBB opening. Int Soc Ther Ultrasound (ISTU) Proc 2009, 1215:172-175.
25. Kroll R.A., Neuwelt E.A. Outwitting the blood-brain barrier for therapeutic purposes: Osmotic opening and other means. Neurosurgery 1998, 42:1083-1099. discussion 1099-1100.
26. Leighton T.G. The acoustic bubble 1994, Academic, San Diego (CA).
27. Li Y., Powers C., Jiang N., Chopp M. Intact, injured, necrotic and apoptotic cells after focal cerebral ischemia in the rat. J Neurol Sci 1998, 156:119-132.
28. Lossinsky A.S., Vorbrodt A.W., Wisniewski H.M. Scanning and transmission electron microscopic studies of microvascular pathology in the osmotically impaired blood-brain barrier. J Neurocytol 1995, 24:795-806.
29. Macdonald R.L., Stoodley M. Pathophysiology of cerebral ischemia. Neurol Med Chir (Tokyo) 1998, 38:1-11.
30. McDannold N., Vykhodtseva N., Hynynen K. Targeted disruption of the blood-brain barrier with focused ultrasound: association with cavitation activity. Phys Med Biol 2006, 51:793-807.
31. 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, 33:584-590.
32. McDannold N., Vykhodtseva N., Hynynen K. Effects of acoustic parameters and ultrasound contrast agent dose on focused-ultrasound induced blood-brain barrier disruption. Ultrasound Med Biol 2008, 34:930-937.
33. McDannold N., Vykhodtseva N., Raymond S., Jolesz F.A., Hynynen K. MRI-guided targeted blood-brain barrier disruption with focused ultrasound: Histological findings in rabbits. Ultrasound Med Biol 2005, 31:1527-1537.
34. Mesiwala A.H., Farrell L., Wenzel H.J., Silbergeld D.L., Crum L.A., Winn H.R., Mourad P.D. High-intensity focused ultrasound selectively disrupts the blood-brain barrier in vivo. Ultrasound Med Biol 2002, 28:389-400.
35. Pardridge W.M. Drug and gene delivery to the brain: The vascular route. Neuron 2002, 36:555-558.
36. Pardridge W.M. The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2005, 2:3-14.
37. Rapoport S.I. Modulation of blood-brain barrier permeability. J Drug Target 1996, 3:417-425.
38. Raymond S.B., Treat L.H., Dewey J.D., McDannold N.J., Hynynen K., Bacskai B.J. Ultrasound enhanced delivery of molecular imaging and therapeutic agents in Alzheimer's disease mouse models. PLoS ONE 2008, 3:e2175.
39. Rosenblum W.I. Histopathologic clues to the pathways of neuronal death following ischemia/hypoxia. J Neurotrauma 1997, 14:313-326.
40. 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, 34:1093-1104.
41. 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 2004, 30:979-989.
42. Treat L.H., McDannold N., Vykhodtseva N., Zhang Y., Tam K., Hynynen K. Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound. Int J Cancer 2007, 121:901-907.
43. Tung Y.S., Choi J.J., Konofagou E.E. Identifying the inertial cavitation threshold of monodispersed microbubbles and skull effects using FUS. Int Soc Ther Ultrasound (ISTU) Proc 2009, 1215:186-189.
44. Tung Y.S., Choi J.J., Baseri B., Konofagou E.E. Identifying the inertial cavitation threshold and skull effects in a vessel phantom using focused ultrasound and microbubbles. Ultrasound Med Biol 2010, 36:840-852.
45. Tung YS, Vlachos F, Choi JJ, Selert K, Konofagou EE. In vivo transcranial cavitation detection during ultrasound-induced blood-brain barrier opening. IEEE Proc Symp Ultrason Ferroelectr Freq Control, San Diego, CA: 2010b (in press).
46. Wang S, Choi JJ, Tung YS, Morrison III B, Konofagou EE. Qualitative and quantitative analysis of the molecular delivery through the ultrasound-enhanced blood-brain barrier opening in the murine brain. IEEE Proc Symp Ultrason Ferroelectr Freq Control, Beijing, China, 2008.
47. Weaver M., Laske D.W. Transferrin receptor ligand-targeted toxin conjugate (Tf-CRM107) for therapy of malignant gliomas. J Neurooncol 2003, 65:3-13.
48. Xie F., Boska M.D., Lof J., Uberti M.G., Tsutsui J.M., Porter T.R. Effects of transcranial ultrasound and intravenous microbubbles on blood brain barrier permeability in a large animal model. Ultrasound Med Biol 2008, 34:2028-2034.
49. Yang F.Y., Fu W.M., Yang R.S., Liou H.C., Kang K.H., Lin W.L. Quantitative evaluation of focused ultrasound with a contrast agent on blood-brain barrier disruption. Ultrasound Med Biol 2007, 33:1421-1427.
50. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201.