Microbubbles traversing the blood-brain barrier for imaging and therapy

Medical and Biological Engineering and Computing

Volumn 47, Issue 8, 2009, Pages 839-849

  Meairs, Stephen ^a   Alonso, Angelika ^a   Fatar, Marc ^a   Kern, Rolf ^a   Hennerici, Michael ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Blood brain barrier; Microbubbles; Perfusion imaging; Safety; Stroke; Therapeutic ultrasound; Ultrasound

Indexed keywords

BLOOD-BRAIN BARRIER; MICROBUBBLES; PERFUSION IMAGING; SAFETY; STROKE; THERAPEUTIC ULTRASOUND; ULTRASOUND;

ACOUSTIC WAVES; BLOOD; BRAIN; CELL MEMBRANES; ENDOTHELIAL CELLS; IMAGING TECHNIQUES; MECHANISMS; ULTRASONIC APPLICATIONS; ULTRASONIC TRANSMISSION; ULTRASONICS;

ULTRASONIC IMAGING;

ECHO CONTRAST MEDIUM; SONOVUE;

ARTICLE; BLOOD BRAIN BARRIER; BLOOD CLOT LYSIS; BRAIN BLOOD FLOW; BRAIN HEMORRHAGE; BRAIN INFARCTION; BRAIN PERFUSION; CEREBROVASCULAR ACCIDENT; CONTRAST ENHANCEMENT; CYTOPLASM; DIAGNOSTIC VALUE; DRUG DELIVERY SYSTEM; ECHOENCEPHALOGRAPHY; ENDOTHELIUM CELL; ENDOTHELIUM INJURY; HUMAN; IMAGE ANALYSIS; IMAGE DISPLAY; MEDICAL RESEARCH; MEMBRANE PERMEABILITY; MICROBUBBLE; NONHUMAN; PATIENT SAFETY; TIGHT JUNCTION; TISSUE INJURY; TRANSCYTOSIS; ULTRASOUND THERAPY;

BLOOD-BRAIN BARRIER; CEREBROVASCULAR CIRCULATION; CONTRAST MEDIA; DRUG DELIVERY SYSTEMS; ECHOENCEPHALOGRAPHY; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MICROBUBBLES;

EID: 69049101973     PISSN: 01400118     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11517-009-0468-6     Document Type: Article

References (50)

1. Burns PN (1996) Harmonic imaging with ultrasound contrast agents. Clin Radiol 51(Suppl 1):50-55
2. Claudon M, Cosgrove D, Albrecht T, Bolondi L, Bosio M, Calliada F, Correas JM, Darge K, Dietrich C, D'Onofrio M, Evans DH, Filice C, Greiner L, Jager K, Jong N, Leen E, Lencioni R, Lindsell D, Martegani A, Meairs S, Nolsoe C, Piscaglia F, Ricci P, Seidel G, Skjoldbye B, Solbiati L, Thorelius L, Tranquart F, Weskott HP, Whittingham T (2008) Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) - update 2008. Ultraschall Med 29:28-44. doi: 10.1055/s-2007-963785
3. Culp WC, Porter TR, Lowery J, Xie F, Roberson PK, Marky L (2004) Intracranial clot lysis with intravenous microbubbles and transcranial ultrasound in swine. Stroke 35:2407-2411. doi: 10.1161/ 01.STR.0000140890.86779.79
4. Dallasta LM, Pisarov LA, Esplen JE, Werley JV, Moses AV, Nelson JA, Achim CL (1999) Blood-brain barrier tight junction disruption in human immunodeficiency virus-1 encephalitis. Am J Pathol 155:1915-1927
5. Davson H, Spaziani E (1959) The blood-brain barrier and the extracellular space of brain. J Physiol 149:135-143
6. Della MA, Meyer-Wiethe K, Allemann E, Seidel G (2005) Ultrasound contrast agents for brain perfusion imaging and ischemic stroke therapy. J Neuroimaging 15:217-232. doi: 10.1177/1051228405277342
7. Diels A, Pettenpohl J, Kern R, Kablau M, Sick C, Hennerici M, Meairs S (2007) Real-time microbubble refill kinetics in patients with MCA infarction. Cerebrovasc Dis 23(suppl 1):1-76
8. Ehrlich P (1885) Das Sauerstoffbedürfnis des Organismus. Eine farbenanalytische Studie. Hirschwald, Berlin
9. Eyding J, Krogias C, Wilkening W, Postert T (2004) Detection of cerebral perfusion abnormalities in acute stroke using phase inversion harmonic imaging (PIHI): Preliminary results. J Neurol Neurosurg Psychiatry 75:926-929. doi: 10.1136/jnnp.2003.026195
10. Eyding J, Krogias C, Schollhammer M, Eyding D, Wilkening W, Meves S, Schroder A, Przuntek H, Postert T (2006) Contrast-enhanced ultrasonic parametric perfusion imaging detects dysfunctional tissue at risk in acute MCA stroke. J Cereb Blood Flow Metab 26:576-582. doi: 10.1038/ sj.jcbfm.9600216
11. Eyding J, Nolte-Martin A, Krogias C, Postert T (2007) Changes of contrast-specific ultrasonic cerebral perfusion patterns in the course of stroke; reliability of region-wise and parametric imaging analysis. Ultrasound Med Biol 33:329-334. doi: 10.1016/j.ultrasmedbio.2006.08.013
12. Fatar M, Stroick M, Griebe M, Alonso A, Kreisel S, Kern R, Hennerici M, Meairs S (2008) Effect of combined ultrasound and microbubbles treatment in an experimental model of cerebral ischemia. Ultrasound Med Biol 34:1414-1420. doi: 10.1016/j.ultrasmedbio.2008.02.008
13. Federlein J, Postert T, Meves S, Weber S, Przuntek H, Buttner T (2000) Ultrasonic evaluation of pathological brain perfusion in acute stroke using second harmonic imaging. J Neurol Neurosurg Psychiatry 69:616-622. doi: 10.1136/jnnp.69.5.616
14. Harrer JU, Mayfrank L, Mull M, Klotzsch C (2003) Second harmonic imaging: A new ultrasound technique to assess human brain tumour perfusion. J Neurol Neurosurg Psychiatry 74:333-338. doi: 10.1136/ jnnp.74.3.333
15. Hawkins BT, Davis TP (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 57:173-185. doi: 10.1124/pr.57.2.4
16. Holscher T, Wilkening W, Draganski B, Meves SH, Eyding J, Voit H, Bogdahn U, Przuntek H, Postert T (2005) Transcranial ultrasound brain perfusion assessment with a contrast agent-specific imaging mode: results of a two-center trial. Stroke 36:2283-2285. doi: 10.1161/ 01.STR.0000179038.63109.b0
17. Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA (2001) Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 220:640-646. doi: 10.1148/radiol.2202001804
18. Hynynen K, McDannold N, Martin H, Jolesz FA, Vykhodtseva N (2003) The threshold for brain damage in rabbits induced by bursts of ultrasound in the presence of an ultrasound contrast agent (Optison). Ultrasound Med Biol 29:473-481. doi: 10.1016/S0301-5629(02)00741-X
19. Hynynen K, McDannold N, Sheikov NA, Jolesz FA, Vykhodtseva N (2005) Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. Neuroimage 24:12-20. doi: 10.1016/j.neuroimage.2004.06.046
20. Kern R, Perren F, Schoeneberger K, Gass A, Hennerici M, Meairs S (2004) Ultrasound microbubble destruction imaging in acute middle cerebral artery stroke. Stroke 35:1665-1670. doi: 10.1161/ 01.STR.0000129332.10721.7e
21. Kern R, Perren F, Kreisel S, Szabo K, Hennerici M, Meairs S (2005) Multi-planar transcranial ultrasound imaging - standards, landmarks and correlation with magnetic resonance imaging. Ultrasound Med Biol 31:311-315. doi: 10.1016/j.ultrasmedbio.2004.12.006
22. Kinoshita M, McDannold N, Jolesz FA, Hynynen K (2006) Targeted delivery of antibodies through the blood-brain barrier by MRI-guided focused ultrasound. Biochem Biophys Res Commun 340:1085-1090. doi: 10.1016/ j.bbrc.2005.12.112
23. Kirk J, Plumb J, Mirakhur M, McQuaid S (2003) Tight junctional abnormality in multiple sclerosis white matter affects all calibres of vessel and is associated with blood-brain barrier leakage and active demyelination. J Pathol 201:319-327. doi: 10.1002/path.1434
24. Lewandowsky M (1900) Zur Lehre von der Cerebrospinalflussigkeit. Z Klin Med 40:480-494
25. McDannold N, Vykhodtseva N, Raymond S, Jolesz FA, Hynynen K (2005) MRI-guided targeted blood-brain barrier disruption with focused ultrasound: Histological findings in rabbits. Ultrasound Med Biol 31:1527-1537. doi: 10.1016/j.ultrasmedbio.2005.07.010
26. McDannold N, Vykhodtseva N, Hynynen K (2006) Targeted disruption of the blood-brain barrier with focused ultrasound: Association with cavitation activity. Phys Med Biol 51:793-807. doi: 10.1088/0031-9155/51/4/003
27. Meairs S, Daffertshofer M, Neff W, Eschenfelder C, Hennerici M (2000) Pulse-inversion contrast harmonic imaging: Ultrasonographic assessment of cerebral perfusion. Lancet 355:550-551. doi: 10.1016/ S0140-6736(99)04361-5
28. Mesiwala AH, Farrell L, Wenzel HJ, Silbergeld DL, Crum LA, Winn HR, Mourad PD (2002) High-intensity focused ultrasound selectively disrupts the blood-brain barrier in vivo. Ultrasound Med Biol 28:389-400. doi: 10.1016/S0301-5629(01)00521-X
29. Meyer-Wiethe K, Cangur H, Seidel GU (2005) Comparison of different mathematical models to analyze diminution kinetics of ultrasound contrast enhancement in a flow phantom. Ultrasound Med Biol 31:93-98. doi: 10.1016/j.ultrasmedbio.2004.05.006
30. Molina CA, Ribo M, Rubiera M, Montaner J, Santamarina E, Delgado-Mederos R, Arenillas JF, Huertas R, Purroy F, Delgado P, Alvarez-Sabin J (2006) Microbubble administration accelerates clot lysis during continuous 2-MHz ultrasound monitoring in stroke patients treated with intravenous tissue plasminogen activator. Stroke 37:425-429. doi: 10.1161/ 01.STR.0000199064.94588.39
31. Ogawa K, Tachibana K, Uchida T, Tai T, Yamashita N, Tsujita N, Miyauchi R (2001) High-resolution scanning electron microscopic evaluation of cell-membrane porosity by ultrasound. Med Electron Microsc 34:249-253. doi: 10.1007/s007950100022
32. Pardridge WM (2005) The blood-brain barrier: Bottleneck in brain drug development. NeuroRx 2:3-14. doi: 10.1602/neurorx.2.1.3
33. Pettenpohl J, Diels A, Kablau M, Kern R, Sick C, Hennerici M, Meairs S (2007) Dynamic microvascular perfusion maps for assessement of brain infarction. Cerebrovasc Dis 23(Suppl 1):1-76
34. Petty MA, Lo EH (2002) Junctional complexes of the blood-brain barrier: permeability changes in neuroinflammation. Prog Neurobiol 68:311-323. doi: 10.1016/S0301-0082(02)00128-4
35. Postert T, Muhs A, Meves S, Federlein J, Przuntek H, Buttner T (1998) Transient response harmonic imaging: An ultrasound technique related to brain perfusion. Stroke 29:1901-1907
36. Postert T, Hoppe P, Federlein J, Helbeck S, Ermert H, Przuntek H, Buttner T, Wilkening W (2000) Contrast agent specific imaging modes for the ultrasonic assessment of parenchymal cerebral echo contrast enhancement. J Cereb Blood Flow Metab 20:1709-1716. doi: 10.1097/ 00004647-200012000-00010
37. Reese T, Karnovsky M (1967) Fine structural localization of a blood-brain barrier to exogenous peroxidase. J Biol Chem 34:207-217
38. Rim SJ, Leong-Poi H, Lindner JR, Couture D, Ellegala D, Mason H, Durieux M, Kassel NF, Kaul S (2001) Quantification of cerebral perfusion with "Real-Time" contrast-enhanced ultrasound. Circulation 104:2582-2587. doi: 10.1161/hc4601.099400
39. Schlachetzki F, Holscher T, Koch HJ, Draganski B, May A, Schuierer G, Bogdahn U (2002) Observation on the integrity of the blood-brain barrier after microbubble destruction by diagnostic transcranial color-coded sonography. J Ultrasound Med 21:419-429
40. Seidel G, Greis C, Sonne J, Kaps M (1999) Harmonic grey scale imaging of the human brain. J Neuroimaging 9:171-174
41. Seidel G, Algermissen C, Christoph A, Claassen L, Vidal-Langwasser M, Katzer T (2000) Harmonic imaging of the human brain. Visualization of brain perfusion with ultrasound. Stroke 31:151-154
42. Seidel G, Meyer-Wiethe K, Berdien G, Hollstein D, Toth D, Aach T (2004) Ultrasound perfusion imaging in acute middle cerebral artery infarction predicts outcome. Stroke 35:1107-1111. doi: 10.1161/ 01.STR.0000124125.19773.40
43. Sheikov N, McDannold N, Vykhodtseva N, Jolesz F, Hynynen K (2004) Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles. Ultrasound Med Biol 30:979-989. doi: 10.1016/j.ultrasmedbio.2004.04.010
44. Sheikov N, McDannold N, Sharma S, Hynynen K (2008) Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium. Ultrasound Med Biol 34:1093-1104. doi: 10.1016/j.ultrasmedbio.2007.12.015
45. Sobesky J, Zaro WO, Lehnhardt FG, Hesselmann V, Thiel A, Dohmen C, Jacobs A, Neveling M, Heiss WD (2004) Which time-to-peak threshold best identifies penumbral flow? A comparison of perfusion-weighted magnetic resonance imaging and positron emission tomography in acute ischemic stroke. Stroke 35:2843-2847. doi: 10.1161/01.STR.0000147043.29399.f6
46. Stroick M, Alonso A, Fatar M, Griebe M, Kreisel S, Kern R, Gaud E, Arditi M, Hennerici M, Meairs S (2006) Effects of simultaneous application of ultrasound and microbubbles on intracerebral hemorrhage in an animal model. Ultrasound Med Biol 32:1377-1382. doi: 10.1016/ j.ultrasmedbio.2006.05.027
47. Taniyama Y, Tachibana K, Hiraoka K, Namba T, Yamasaki K, Hashiya N, Aoki M, Ogihara T, Yasufumi K, Morishita R (2002) Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation 105:1233-1239. doi: 10.1161/hc1002.105228
48. Wardlaw JM, Sandercock PA, Dennis MS, Starr J (2003) Is breakdown of the blood-brain barrier responsible for lacunar stroke, leukoaraiosis, and dementia? Stroke 34:806-812. doi: 10.1161/01.STR.0000058480.77236.B3
49. Wiesmann M, Meyer K, Albers T, Seidel G (2004) Parametric perfusion imaging with contrast-enhanced ultrasound in acute ischemic stroke. Stroke 35:508-513. doi: 10.1161/01.STR.0000114877.58809.3D
50. Xie F, Tsutsui JM, Lof J, Unger EC, Johanning J, Culp WC, Matsunaga T, Porter TR (2005) Effectiveness of lipid microbubbles and ultrasound in declotting thrombosis. Ultrasound Med Biol 31:979-985. doi: 10.1016/ j.ultrasmedbio.2005.03.008