Recent advances in molecular, multimodal and theranostic ultrasound imaging

Advanced Drug Delivery Reviews

Volumn 72, Issue , 2014, Pages 15-27

  Kiessling, Fabian ^a   Fokong, Stanley ^a   Bzyl, Jessica ^a   Lederle, Wiltrud ^a   Palmowski, Moritz ^a   Lammers, Twan ^a,b  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

Angiogenesis; Blood brain barrier; Cardiovascular; Cavitation; Drug delivery; Molecular imaging; Nanomedicine; Sonography; Theranostics; Tumor

Indexed keywords

BUBBLES (IN FLUIDS); CAVITATION; DIAGNOSIS; DRUG DELIVERY; MEDICAL NANOTECHNOLOGY; NUCLEIC ACIDS; THERANOSTICS; TUMORS; ULTRASONIC IMAGING; ULTRASONOGRAPHY;

ANGIOGENESIS; BLOOD-BRAIN BARRIER; CARDIOVASCULAR; CONTRAST AGENT; DIAGNOSTIC AGENTS; NEUROLOGICAL DISEASE; REAL-TIME DIAGNOSIS; ULTRASOUND IMAGING;

MOLECULAR IMAGING;

ECHO CONTRAST MEDIUM; CONTRAST MEDIUM;

CARDIOVASCULAR DISEASE; CLINICAL PRACTICE; CONJUGATION; CONTRAST ENHANCEMENT; DIAGNOSTIC IMAGING; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG PENETRATION; DRUG UPTAKE; EXTRAVASATION; HUMAN; ISOTOPE LABELING; MALIGNANT NEOPLASTIC DISEASE; MICROBUBBLE; MOLECULAR IMAGING; NEUROLOGIC DISEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARTICLE SIZE; PHOTOACOUSTICS; PRIORITY JOURNAL; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; ULTRASOUND; ANIMAL; ECHOGRAPHY; PROCEDURES; ULTRASOUND THERAPY;

ANIMALS; CONTRAST MEDIA; DRUG DELIVERY SYSTEMS; HUMANS; MICROBUBBLES; ULTRASONIC THERAPY; ULTRASONOGRAPHY;

EID: 84901641518     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2013.11.013     Document Type: Review

References (139)

1. Shung K.K. Diagnostic ultrasound: past, present, and future. J. Med. Biol. Eng. 2011, 31:371-374.
2. von Reutern G.M., Goertler M.W., Bornstein N.M., Del Sette M., Evans D.H., Hetzel A., Kaps M., Perren F., Razumovky A., von Reutern M., Shiogai T., Titianova E., Traubner P., Venketasubramanian N., Wong L.K., Yasaka M. Grading carotid stenosis using ultrasonic methods. Stroke 2012, 43:916-921.
3. Baker J.A., Soo M.S. The evolving role of sonography in evaluating solid breast masses. Semin. Ultrasound CT MR 2000, 21:286-296.
4. Cosgrove D.O., Chan K.E. Renal transplants: what ultrasound can and cannot do. Ultrasound Q. 2008, 24:77-87. [quiz 141-142].
5. Coleman A.J., Saunders J.E. A review of the physical properties and biological effects of the high amplitude acoustic field used in extracorporeal lithotripsy. Ultrasonics 1993, 31:75-89.
6. Al-Bataineh O., Jenne J., Huber P. Clinical and future applications of high intensity focused ultrasound in cancer. Cancer Treat. Rev. 2012, 38:346-353.
7. Strobel D., Seitz K., Blank W., Schuler A., Dietrich C.F., von Herbay A., Friedrich-Rust M., Bernatik T. Tumor-specific vascularization pattern of liver metastasis, hepatocellular carcinoma, hemangioma and focal nodular hyperplasia in the differential diagnosis of 1,349 liver lesions in contrast-enhanced ultrasound (CEUS). Ultraschall Med. 2009, 30:376-382.
8. Seitz K., Strobel D., Bernatik T., Blank W., Friedrich-Rust M., Herbay A., Dietrich C.F., Strunk H., Kratzer W., Schuler A. Contrast-enhanced ultrasound (CEUS) for the characterization of focal liver lesions -prospective comparison in clinical practice: CEUS vs. CT (DEGUM multicenter trial). Parts of this manuscript were presented at the Ultrasound Dreilandertreffen 2008, Davos. Ultraschall Med. 2009, 30:383-389.
9. Seitz K., Bernatik T., Strobel D., Blank W., Friedrich-Rust M., Strunk H., Greis C., Kratzer W., Schuler A. Contrast-enhanced ultrasound (CEUS) for the characterization of focal liver lesions in clinical practice (DEGUM Multicenter Trial): CEUS vs. MRI-a prospective comparison in 269 patients. Ultraschall Med. 2010, 31:492-499.
10. Claudon M., Cosgrove D., Albrecht T., Bolondi L., Bosio M., Calliada F., Correas J.M., Darge K., Dietrich C., D'Onofrio M., Evans D.H., 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 H.P., Whittingham T. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) -update 2008. Ultraschall Med. 2008, 29:28-44.
11. Mulvagh S.L., Rakowski H., Vannan M.A., Abdelmoneim S.S., Becher H., Bierig S.M., Burns P.N., Castello R., Coon P.D., Hagen M.E., Jollis J.G., Kimball T.R., Kitzman D.W., Kronzon I., Labovitz A.J., Lang R.M., Mathew J., Moir W.S., Nagueh S.F., Pearlman A.S., Perez J.E., Porter T.R., Rosenbloom J., Strachan G.M., Thanigaraj S., Wei K., Woo A., Yu E.H., Zoghbi W.A. American Society of Echocardiography consensus statement on the clinical applications of ultrasonic contrast agents in echocardiography. J. Am. Soc. Echocardiogr. 2008, 21:1179-1201. [quiz 1281].
12. Wei K. Contrast echocardiography: what have we learned from the new guidelines?. Curr. Cardiol. Rep. 2010, 12:237-242.
13. Allendoerfer J., Tanislav C. Diagnostic and prognostic value of contrast-enhanced ultrasound in acute stroke. Ultraschall Med. 2008, 29(Suppl. 4):S210-S214.
14. Welschehold S., Geisel F., Beyer C., Reuland A., Kerz T. Contrast-enhanced transcranial Doppler ultrasonography in the diagnosis of brain death. J. Neurol. Neurosurg. Psychiatry 2013, 84:939-940.
15. Tamai H., Takiguchi Y., Oka M., Shingaki N., Enomoto S., Shiraki T., Furuta M., Inoue I., Iguchi M., Yanaoka K., Arii K., Shimizu Y., Nakata H., Shinka T., Sanke T., Ichinose M. Contrast-enhanced ultrasonography in the diagnosis of solid renal tumors. J. Ultrasound Med. 2005, 24:1635-1640.
16. Correas J.M., Claudon M., Tranquart F., Helenon A.O. The kidney: imaging with microbubble contrast agents. Ultrasound Q. 2006, 22:53-66.
17. Darge K. Voiding urosonography with ultrasound contrast agents for the diagnosis of vesicoureteric reflux in children. I. Procedure. Pediatr. Radiol. 2008, 38:40-53.
18. Li X.L., Zeng G.M., Shi L., Liang J., Cai Q. Urban ecological land in Changsha City: its quantitative analysis and optimization. Ying Yong Sheng Tai Xue Bao 2010, 21:415-421.
19. Dietrich C.F., Braden B., Hocke M., Ott M., Ignee A. Improved characterisation of solitary solid pancreatic tumours using contrast enhanced transabdominal ultrasound. J. Cancer Res. Clin. Oncol. 2008, 134:635-643.
20. D'Onofrio M., Megibow A.J., Faccioli N., Malago R., Capelli P., Falconi M., Mucelli R.P. Comparison of contrast-enhanced sonography and MRI in displaying anatomic features of cystic pancreatic masses. AJR Am. J. Roentgenol. 2007, 189:1435-1442.
21. Ripolles T., Martinez M.J., Lopez E., Castello I., Delgado F. Contrast-enhanced ultrasound in the staging of acute pancreatitis. Eur. Radiol. 2010, 20:2518-2523.
22. Catalano O., Aiani L., Barozzi L., Bokor D., De Marchi A., Faletti C., Maggioni F., Montanari N., Orlandi P.E., Siani A., Sidhu P.S., Thompson P.K., Valentino M., Ziosi A., Martegani A. CEUS in abdominal trauma: multi-center study. Abdom. Imaging 2009, 34:225-234.
23. Sorelli P.G., Cosgrove D.O., Svensson W.E., Zaman N., Satchithananda K., Barrett N.K., Lim A.K. Can contrast-enhanced sonography distinguish benign from malignant breast masses?. J. Clin. Ultrasound 2010, 38:177-181.
24. Balleyguier C., Opolon P., Mathieu M.C., Athanasiou A., Garbay J.R., Delaloge S., Dromain C. New potential and applications of contrast-enhanced ultrasound of the breast: own investigations and review of the literature. Eur. J. Radiol. 2009, 69:14-23.
25. Lassau N., Chami L., Chebil M., Benatsou B., Bidault S., Girard E., Abboud G., Roche A. Dynamic contrast-enhanced ultrasonography (DCE-US) and anti-angiogenic treatments. Discov. Med. 2011, 11:18-24.
26. Knieling F., Waldner M.J., Goertz R.S., Zopf S., Wildner D., Neurath M.F., Bernatik T., Strobel D. Early response to anti-tumoral treatment in hepatocellular carcinoma-can quantitative contrast-enhanced ultrasound predict outcome?. Ultraschall Med. 2013, 34:38-46.
27. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1995, 1:27-31.
28. Bergers G., Benjamin L.E. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 2003, 3:401-410.
29. Ferrara N. VEGF and the quest for tumour angiogenesis factors. Nat. Rev. Cancer 2002, 2:795-803.
30. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 2004, 25:581-611.
31. Brooks P.C., Clark R.A., Cheresh D.A. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 1994, 264:569-571.
32. Hood J.D., Cheresh D.A. Role of integrins in cell invasion and migration. Nat. Rev. Cancer 2002, 2:91-100.
33. Somanath P.R., Malinin N.L., Byzova T.V. Cooperation between integrin alphavbeta3 and VEGFR2 in angiogenesis. Angiogenesis 2009, 12:177-185.
34. Lopez-Novoa J.M., Bernabeu C. The physiological role of endoglin in the cardiovascular system. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H959-H974.
35. Foygel K., Wang H., Machtaler S., Lutz A.M., Chen R., Pysz M., Lowe A.W., Tian L., Carrigan T., Brentnall T.A., Willmann J.K. Detection of pancreatic ductal adenocarcinoma in mice by ultrasound imaging of thymocyte differentiation antigen 1. Gastroenterology 2013, 145:885-894.
36. Wang L., Li L., Guo Y., Tong H., Fan X., Ding J., Huang H. Construction and in vitro/in vivo targeting of PSMA-targeted nanoscale microbubbles in prostate cancer. Prostate 2013, 73:1147-1158.
37. Wu W., Wang Y., Shen S., Wu J., Guo S., Su L., Hou F., Wang Z., Liao Y., Bin J. In vivo ultrasound molecular imaging of inflammatory thrombosis in arteries with cyclic Arg-Gly-Asp-modified microbubbles targeted to glycoprotein IIb/IIIa. Invest. Radiol. 2013, 48:803-812.
38. Bokor D., Chambers J.B., Rees P.J., Mant T.G., Luzzani F., Spinazzi A. Clinical safety of SonoVue, a new contrast agent for ultrasound imaging, in healthy volunteers and in patients with chronic obstructive pulmonary disease. Invest. Radiol. 2001, 36:104-109.
39. Korpanty G., Grayburn P.A., Shohet R.V., Brekken R.A. Targeting vascular endothelium with avidin microbubbles. Ultrasound Med. Biol. 2005, 31:1279-1283.
40. Cui W., Bei J., Wang S., Zhi G., Zhao Y., Zhou X., Zhang H., Xu Y. Preparation and evaluation of poly(l-lactide-co-glycolide) (PLGA) microbubbles as a contrast agent for myocardial contrast echocardiography. J. Biomed. Mater. Res. B Appl. Biomater. 2005, 73:171-178.
41. Fokong S., Siepmann M., Liu Z., Schmitz G., Kiessling F., Gatjens J. Advanced characterization and refinement of poly N-butyl cyanoacrylate microbubbles for ultrasound imaging. Ultrasound Med. Biol. 2011, 37:1622-1634.
42. Sirsi S., Borden M. Microbubble compositions, properties and biomedical applications. Bubble Sci. Eng. Technol. 2009, 1:3-17.
43. Borden M.A., Caskey C.F., Little E., Gillies R.J., Ferrara K.W. DNA and polylysine adsorption and multilayer construction onto cationic lipid-coated microbubbles. Langmuir 2007, 23:9401-9408.
44. Schutt E.G., Klein D.H., Mattrey R.M., Riess J.G. Injectable microbubbles as contrast agents for diagnostic ultrasound imaging: the key role of perfluorochemicals. Angew. Chem. Int. Ed. Engl. 2003, 42:3218-3235.
45. Postema M., Schmitz G. Ultrasonic bubbles in medicine: influence of the shell. Ultrason. Sonochem. 2007, 14:438-444.
46. Kiessling F., Bzyl J., Fokong S., Siepmann M., Schmitz G., Palmowski M. Targeted ultrasound imaging of cancer: an emerging technology on its way to clinics. Curr. Pharm. Des. 2012, 18:2184-2199.
47. Unnikrishnan S., Klibanov A.L. Microbubbles as ultrasound contrast agents for molecular imaging: preparation and application. AJR Am. J. Roentgenol. 2012, 199:292-299.
48. Klibanov A.L. Microbubble contrast agents: targeted ultrasound imaging and ultrasound-assisted drug-delivery applications. Invest. Radiol. 2006, 41:354-362.
49. Kollmann C. New sonographic techniques for harmonic imaging-underlying physical principles. Eur. J. Radiol. 2007, 64:164-172.
50. Simpson D.H., Chin C.T., Burns P.N. Pulse inversion Doppler: a new method for detecting nonlinear echoes from microbubble contrast agents. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 1999, 46:372-382.
51. Eckersley R.J., Chin C.T., Burns P.N. Optimising phase and amplitude modulation schemes for imaging microbubble contrast agents at low acoustic power. Ultrasound Med. Biol. 2005, 31:213-219.
52. Phillips P.J. Contrast pulse sequences (CPS): imaging nonlinear microbubbles. Ultrasonics 2001, 1739-1745.
53. Wei K., Jayaweera A.R., Firoozan S., Linka A., Skyba D.M., Kaul S. Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation 1998, 97:473-483.
54. Willmann J.K., Paulmurugan R., Chen K., Gheysens O., Rodriguez-Porcel M., Lutz A.M., Chen I.Y., Chen X., Gambhir S.S. US imaging of tumor angiogenesis with microbubbles targeted to vascular endothelial growth factor receptor type 2 in mice. Radiology 2008, 246:508-518.
55. Bzyl J., Palmowski M., Rix A., Arns S., Hyvelin J.M., Pochon S., Ehling J., Schrading S., Kiessling F., Lederle W. The high angiogenic activity in very early breast cancer enables reliable imaging with VEGFR2-targeted microbubbles (BR55). Eur. Radiol. 2013, 23:468-475.
56. Tiemann K., Pohl C., Schlosser T., Goenechea J., Bruce M., Veltmann C., Kuntz S., Bangard M., Becher H. Stimulated acoustic emission: pseudo-Doppler shifts seen during the destruction of nonmoving microbubbles. Ultrasound Med. Biol. 2000, 26:1161-1167.
57. Reinhardt M., Hauff P., Briel A., Uhlendorf V., Linker R.A., Maurer M., Schirner M. Sensitive particle acoustic quantification (SPAQ): a new ultrasound-based approach for the quantification of ultrasound contrast media in high concentrations. Invest. Radiol. 2005, 40:2-7.
58. Reinhardt M., Hauff P., Linker R.A., Briel A., Gold R., Rieckmann P., Becker G., Toyka K.V., Maurer M., Schirner M. Ultrasound derived imaging and quantification of cell adhesion molecules in experimental autoimmune encephalomyelitis (EAE) by Sensitive Particle Acoustic Quantification (SPAQ). Neuroimage 2005, 27:267-278.
59. Palmowski M., Peschke P., Huppert J., Hauff P., Reinhardt M., Maurer M., Karger C.P., Scholz M., Semmler W., Huber P.E., Kiessling F.M. Molecular ultrasound imaging of early vascular response in prostate tumors irradiated with carbon ions. Neoplasia 2009, 11:856-863.
60. Palmowski M., Huppert J., Ladewig G., Hauff P., Reinhardt M., Mueller M.M., Woenne E.C., Jenne J.W., Maurer M., Kauffmann G.W., Semmler W., Kiessling F. Molecular profiling of angiogenesis with targeted ultrasound imaging: early assessment of antiangiogenic therapy effects. Mol. Cancer Ther. 2008, 7:101-109.
61. Fowlkes J., Gardner E., Ivey J., Carson P. The role of acoustic radiation force in contrast enhancement techniques using bubble-based ultrasound contrast agents. J. Acoust. Soc. Am. 1993, 93:2348.
62. Zhao S., Borden M., Bloch S.H., Kruse D., Ferrara K.W., Dayton P.A. Radiation-force assisted targeting facilitates ultrasonic molecular imaging. Mol. Imaging 2004, 3:135-148.
63. Rychak J.J., Klibanov A.L., Ley K.F., Hossack J.A. Enhanced targeting of ultrasound contrast agents using acoustic radiation force. Ultrasound Med. Biol. 2007, 33:1132-1139.
64. Frinking P.J., Tardy I., Theraulaz M., Arditi M., Powers J., Pochon S., Tranquart F. Effects of acoustic radiation force on the binding efficiency of BR55, a VEGFR2-specific ultrasound contrast agent. Ultrasound Med. Biol. 2012, 38:1460-1469.
65. Wijkstra H., Smeenge M., Rosette J.J., de la Pochon S., Tranquart F. Targeted microbubble prostate cancer imaging with BR55. Proceedings of the 17th European Symposium on Ultrasound Imaging 2012.
66. Kaufmann B.A., Sanders J.M., Davis C., Xie A., Aldred P., Sarembock I.J., Lindner J.R. Molecular imaging of inflammation in atherosclerosis with targeted ultrasound detection of vascular cell adhesion molecule-1. Circulation 2007, 116:276-284.
67. Villanueva F.S., Lu E., Bowry S., Kilic S., Tom E., Wang J., Gretton J., Pacella J.J., Wagner W.R. Myocardial ischemic memory imaging with molecular echocardiography. Circulation 2007, 115:345-352.
68. Masseau I., Davis M.J., Bowles D.K. Carotid inflammation is unaltered by exercise in hypercholesterolemic Swine. Med. Sci. Sports Exerc. 2012, 44:2277-2289.
69. Kaufmann B.A., Carr C.L., Belcik J.T., Xie A., Yue Q., Chadderdon S., Caplan E.S., Khangura J., Bullens S., Bunting S., Lindner J.R. Molecular imaging of the initial inflammatory response in atherosclerosis: implications for early detection of disease. Arterioscler. Thromb. Vasc. Biol. 2010, 30:54-59.
70. Schumann P.A., Christiansen J.P., Quigley R.M., McCreery T.P., Sweitzer R.H., Unger E.C., Lindner J.R., Matsunaga T.O. Targeted-microbubble binding selectively to GPIIb IIIa receptors of platelet thrombi. Invest. Radiol. 2002, 37:587-593.
71. Wang X., Hagemeyer C.E., Hohmann J.D., Leitner E., Armstrong P.C., Jia F., Olschewski M., Needles A., Peter K., Ahrens I. Novel single-chain antibody-targeted microbubbles for molecular ultrasound imaging of thrombosis: validation of a unique noninvasive method for rapid and sensitive detection of thrombi and monitoring of success or failure of thrombolysis in mice. Circulation 2012, 125:3117-3126.
72. Bettinger T., Bussat P., Tardy I., Pochon S., Hyvelin J.M., Emmel P., Henrioud S., Biolluz N., Willmann J.K., Schneider M., Tranquart F. Ultrasound molecular imaging contrast agent binding to both E- and P-selectin in different species. Invest. Radiol. 2012, 47:516-523.
73. Kiessling F., Huppert J., Palmowski M. Functional and molecular ultrasound imaging: concepts and contrast agents. Curr. Med. Chem. 2009, 16:627-642.
74. Deshpande N., Pysz M.A., Willmann J.K. Molecular ultrasound assessment of tumor angiogenesis. Angiogenesis 2010, 13:175-188.
75. Sorace A.G., Saini R., Mahoney M., Hoyt K. Molecular ultrasound imaging using a targeted contrast agent for assessing early tumor response to antiangiogenic therapy. J Ultrasound Med. 2012, 31:1543-1550.
76. Deshpande N., Ren Y., Foygel K., Rosenberg J., Willmann J.K. Tumor angiogenic marker expression levels during tumor growth: longitudinal assessment with molecularly targeted microbubbles and US imaging. Radiology 2011, 258:804-811.
77. Korpanty G., Carbon J.G., Grayburn P.A., Fleming J.B., Brekken R.A. Monitoring response to anticancer therapy by targeting microbubbles to tumor vasculature. Clin. Cancer Res. 2007, 13:323-330.
78. Willmann J.K., Lutz A.M., Paulmurugan R., Patel M.R., Chu P., Rosenberg J., Gambhir S.S. Dual-targeted contrast agent for US assessment of tumor angiogenesis in vivo. Radiology 2008, 248:936-944.
79. Pochon S., Tardy I., Bussat P., Bettinger T., Brochot J., von Wronski M., Passantino L., Schneider M. BR55: a lipopeptide-based VEGFR2-targeted ultrasound contrast agent for molecular imaging of angiogenesis. Invest. Radiol. 2010, 45:89-95.
80. Tardy I., Pochon S., Theraulaz M., Emmel P., Passantino L., Tranquart F., Schneider M. Ultrasound molecular imaging of VEGFR2 in a rat prostate tumor model using BR55. Invest. Radiol. 2010, 45:573-578.
81. Pysz M.A., Foygel K., Rosenberg J., Gambhir S.S., Schneider M., Willmann J.K. Antiangiogenic cancer therapy: monitoring with molecular US and a clinically translatable contrast agent (BR55). Radiology 2010, 256:519-527.
82. Bzyl J., Palmowski M., Rix A., Arns S., Hyvelin J.M., Pochon S., Ehling J., Schrading S., Kiessling F., Lederle W. The high angiogenic activity in very early breast cancer enables reliable imaging with VEGFR2-targeted microbubbles (BR55). Eur. Radiol. 2013, 23:468-475.
83. Bachawal S.V., Jensen K.C., Lutz A.M., Gambhir S.S., Tranquart F., Tian L., Willmann J.K. Earlier detection of breast cancer with ultrasound molecular imaging in a transgenic mouse model. Cancer Res. 2013, 73:1689-1698.
84. Deshpande N., Lutz A.M., Ren Y., Foygel K., Tian L., Schneider M., Pai R., Pasricha P.J., Willmann J.K. Quantification and monitoring of inflammation in murine inflammatory bowel disease with targeted contrast-enhanced US. Radiology 2012, 262:172-180.
85. Fokong S., Fragoso A., Rix A., Curaj A., Wu Z., Lederle W., Iranzo O., Gatjens J., Kiessling F., Palmowski M. Ultrasound molecular imaging of E-selectin in tumor vessels using poly n-butyl cyanoacrylate microbubbles covalently coupled to a short targeting peptide. Invest. Radiol. 2013, 48:843-850.
86. Cavalieri F., Zhou M., Tortora M., Lucilla B., Ashokkumar M. Methods of preparation of multifunctional microbubbles and their in vitro/in vivo assessment of stability, functional and structural properties. Curr. Pharm. Des. 2012, 18:2135-2151.
87. Liu Z., Lammers T., Ehling J., Fokong S., Bornemann J., Kiessling F., Gatjens J. Iron oxide nanoparticle-containing microbubble composites as contrast agents for MR and ultrasound dual-modality imaging. Biomaterials 2011, 32:6155-6163.
88. Huynh E., Lovell J.F., Helfield B.L., Jeon M., Kim C., Goertz D.E., Wilson B.C., Zheng G. Porphyrin shell microbubbles with intrinsic ultrasound and photoacoustic properties. J. Am. Chem. Soc. 2012, 134:16464-16467.
89. Seo M., Gorelikov I., Williams R., Matsuura N. Microfluidic assembly of monodisperse, nanoparticle-incorporated perfluorocarbon microbubbles for medical imaging and therapy. Langmuir 2010, 26:13855-13860.
90. Park J.I., Jagadeesan D., Williams R., Oakden W., Chung S., Stanisz G.J., Kumacheva E. Microbubbles loaded with nanoparticles: a route to multiple imaging modalities. ACS Nano 2010, 4:6579-6586.
91. Barrefelt A.A., Brismar T.B., Egri G., Aspelin P., Olsson A., Oddo L., Margheritelli S., Caidahl K., Paradossi G., Dahne L., Axelsson R., Hassan M. Multimodality imaging using SPECT/CT and MRI and ligand functionalized 99mTc-labeled magnetic microbubbles. EJNMMI Res. 2013, 3:12.
92. Yang F., Li Y., Chen Z., Zhang Y., Wu J., Gu N. Superparamagnetic iron oxide nanoparticle-embedded encapsulated microbubbles as dual contrast agents of magnetic resonance and ultrasound imaging. Biomaterials 2009, 30:3882-3890.
93. Vlaskou D., Plank C., Mykhaylyk O. Magnetic and acoustically active microbubbles loaded with nucleic acids for gene delivery. Methods Mol. Biol. 2013, 948:205-241.
94. Fan C.H., Ting C.Y., Lin H.J., Wang C.H., Liu H.L., Yen T.C., Yeh C.K. SPIO-conjugated, doxorubicin-loaded microbubbles for concurrent MRI and focused-ultrasound enhanced brain-tumor drug delivery. Biomaterials 2013, 34:3706-3715.
95. Feshitan J.A., Vlachos F., Sirsi S.R., Konofagou E.E., Borden M.A. Theranostic Gd(III)-lipid microbubbles for MRI-guided focused ultrasound surgery. Biomaterials 2012, 33:247-255.
96. Feshitan J.A., Boss M.A., Borden M.A. Magnetic resonance properties of Gd(III)-bound lipid-coated microbubbles and their cavitation fragments. Langmuir 2012, 28:15336-15343.
97. Wang L.V. Prospects of photoacoustic tomography. Med. Phys. 2008, 35:5758-5767.
98. Xu R.X. Multifunctional microbubbles and nanobubbles for photoacoustic imaging. Contrast Media Mol. Imaging 2011, 6:401-411.
99. Karpiouk A.B., Aglyamov S.R., Mallidi S., Shah J., Scott W.G., Rubin J.M., Emelianov S.Y. Combined ultrasound and photoacoustic imaging to detect and stage deep vein thrombosis: phantom and ex vivo studies. J. Biomed. Opt. 2008, 13:054061.
100. Erpelding T.N., Kim C., Pramanik M., Jankovic L., Maslov K., Guo Z., Margenthaler J.A., Pashley M.D., Wang L.V. Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system. Radiology 2010, 256:102-110.
101. Koczera P., Wu Z., Fokong S., Theek B., Appold L., Jorge S., Möckel D., Liu Z., Curaj A., Storm G., Zandvoort M., Kiessling F., Lammers T. Fluorescently labeled microbubbles for facilitating translational molecular ultrasound studies, Drug Delivery and. Transl. Res. 2012, 2:56-64.
102. Fokong S., Theek B., Wu Z., Koczera P., Appold L., Jorge S., Resch-Genger U., van Zandvoort M., Storm G., Kiessling F., Lammers T. Image-guided, targeted and triggered drug delivery to tumors using polymer-based microbubbles. J. Control. Release 2012, 163:75-81.
103. Eisenbrey J.R., Burstein O.M., Kambhampati R., Forsberg F., Liu J.B., Wheatley M.A. Development and optimization of a doxorubicin loaded poly(lactic acid) contrast agent for ultrasound directed drug delivery. J. Control. Release 2010, 143:38-44.
104. Deckers R., Yudina A., Cardoit L.C., Moonen C.T. A fluorescent chromophore TOTO-3 as a 'smart probe' for the assessment of ultrasound-mediated local drug delivery in vivo. Contrast Media Mol. Imaging 2011, 6:267-274.
105. Yuan B. Sensitivity of fluorophore-quencher labeled microbubbles to externally applied static pressure. Med. Phys. 2009, 36:3455-3469.
106. Tartis M.S., Kruse D.E., Zheng H., Zhang H., Kheirolomoom A., Marik J., Ferrara K.W. Dynamic microPET imaging of ultrasound contrast agents and lipid delivery. J. Control. Release 2008, 131:160-166.
107. Palmowski M., Morgenstern B., Hauff P., Reinhardt M., Huppert J., Maurer M., Woenne E.C., Doerk S., Ladewig G., Jenne J.W., Delorme S., Grenacher L., Hallscheidt P., Kauffmann G.W., Semmler W., Kiessling F. Pharmacodynamics of streptavidin-coated cyanoacrylate microbubbles designed for molecular ultrasound imaging. Invest. Radiol. 2008, 43:162-169.
108. Lazarova N., Causey P.W., Lemon J.A., Czorny S.K., Forbes J.R., Zlitni A., Genady A., Foster F.S., Valliant J.F. The synthesis, magnetic purification and evaluation of 99mTc-labeled microbubbles. Nucl. Med. Biol. 2011, 38:1111-1118.
109. Voogt M.J., Trillaud H., Kim Y.S., Mali W.P., Barkhausen J., Bartels L.W., Deckers R., Frulio N., Rhim H., Lim H.K., Eckey T., Nieminen H.J., Mougenot C., Keserci B., Soini J., Vaara T., Kohler M.O., Sokka S., van den Bosch M.A. Volumetric feedback ablation of uterine fibroids using magnetic resonance-guided high intensity focused ultrasound therapy. Eur. Radiol. 2012, 22:411-417.
110. Quesson B., de Zwart J.A., Moonen C.T. Magnetic resonance temperature imaging for guidance of thermotherapy. J. Magn. Reson. Imaging 2000, 12:525-533.
111. Cline H.E., Hynynen K., Hardy C.J., Watkins R.D., Schenck J.F., Jolesz F.A. MR temperature mapping of focused ultrasound surgery. Magn. Reson. Med. 1994, 31:628-636.
112. Koning G.A., Eggermont A.M., Lindner L.H., ten Hagen T.L. Hyperthermia and thermosensitive liposomes for improved delivery of chemotherapeutic drugs to solid tumors. Pharm. Res. 2010, 27:1750-1754.
113. Grull H., Langereis S. Hyperthermia-triggered drug delivery from temperature-sensitive liposomes using MRI-guided high intensity focused ultrasound. J. Control. Release 2012, 161:317-327.
114. Hijnen N.M., Heijman E., Kohler M.O., Ylihautala M., Ehnholm G.J., Simonetti A.W., Grull H. Tumour hyperthermia and ablation in rats using a clinical MR-HIFU system equipped with a dedicated small animal set-up. Int. J. Hyperthermia 2012, 28:141-155.
115. Molina C.A., Ribo M., Rubiera M., Montaner J., Santamarina E., Delgado-Mederos R., Arenillas J.F., Huertas R., Purroy F., Delgado P., Alvarez-Sabin J. Microbubble administration accelerates clot lysis during continuous 2-MHz ultrasound monitoring in stroke patients treated with intravenous tissue plasminogen activator. Stroke 2006, 37:425-429.
116. Wang J., Pelletier M., Zhang H., Xia H., Zhao Y. High-frequency ultrasound-responsive block copolymer micelle. Langmuir 2009, 25:13201-13205.
117. Zhang H., Xia H., Wang J., Li Y. High intensity focused ultrasound-responsive release behavior of PLA-b-PEG copolymer micelles. J. Control. Release 2009, 139:31-39.
118. Oerlemans C., Deckers R., Storm G., Hennink W.E., Nijsen J.F. Evidence for a new mechanism behind HIFU-triggered release from liposomes. J. Control. Release 2013, 168:327-333.
119. Deckers R., Paradissis A., Oerlemans C., Talelli M., Storm G., Hennink W.E., Nijsen J.F. New insights into the HIFU-triggered release from polymeric micelles. Langmuir 2013, 29:9483-9490.
120. O'Neill B.E., Vo H., Angstadt M., Li K.P., Quinn T., Frenkel V. Pulsed high intensity focused ultrasound mediated nanoparticle delivery: mechanisms and efficacy in murine muscle. Ultrasound Med. Biol. 2009, 35:416-424.
121. Hancock H.A., Smith L.H., Cuesta J., Durrani A.K., Angstadt M., Palmeri M.L., Kimmel E., Frenkel V. Investigations into pulsed high-intensity focused ultrasound-enhanced delivery: preliminary evidence for a novel mechanism. Ultrasound Med. Biol. 2009, 35:1722-1736.
122. Lammers T., Aime S., Hennink W.E., Storm G., Kiessling F. Theranostic nanomedicine. Acc. Chem. Res. 2011, 44:1029-1038.
123. Lammers T., Kiessling F., Hennink W.E., Storm G. Nanotheranostics and image-guided drug delivery: current concepts and future directions. Mol. Pharm. 2010, 7:1899-1912.
124. Martin K.H., Dayton P.A. Current status and prospects for microbubbles in ultrasound theranostics. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2013, 5:329-345.
125. Sirsi S.R., Borden M.A. Advances in ultrasound mediated gene therapy using microbubble contrast agents. Theranostics 2012, 2:1208-1222.
126. Kiessling F., Fokong S., Koczera P., Lederle W., Lammers T. Ultrasound microbubbles for molecular diagnosis, therapy, and theranostics. J. Nucl. Med. 2012, 53:345-348.
127. Cochran M.C., Eisenbrey J., Ouma R.O., Soulen M., Wheatley M.A. Doxorubicin and paclitaxel loaded microbubbles for ultrasound triggered drug delivery. Int. J. Pharm. 2011, 414:161-170.
128. Lentacker I., Geers B., Demeester J., De Smedt S.C., Sanders N.N. Design and evaluation of doxorubicin-containing microbubbles for ultrasound-triggered doxorubicin delivery: cytotoxicity and mechanisms involved. Mol. Ther. 2010, 18:101-108.
129. Klibanov A.L., Shevchenko T.I., Raju B.I., Seip R., Chin C.T. Ultrasound-triggered release of materials entrapped in microbubble-liposome constructs: a tool for targeted drug delivery. J. Control. Release 2010, 148:13-17.
130. Kooiman K., Bohmer M.R., Emmer M., Vos H.J., Chlon C., Shi W.T., Hall C.S., de Winter S.H., Schroen K., Versluis M., de Jong N., van Wamel A. Oil-filled polymer microcapsules for ultrasound-mediated delivery of lipophilic drugs. J. Control. Release 2009, 133:109-118.
131. van Wamel A., Kooiman K., Harteveld M., Emmer M., ten Cate F.J., Versluis M., de Jong N. Vibrating microbubbles poking individual cells: drug transfer into cells via sonoporation. J. Control. Release 2006, 112:149-155.
132. Schlicher R.K., Radhakrishna H., Tolentino T.P., Apkarian R.P., Zarnitsyn V., Prausnitz M.R. Mechanism of intracellular delivery by acoustic cavitation. Ultrasound Med. Biol. 2006, 32:915-924.
133. Yudina A., Lepetit-Coiffe M., Moonen C.T. Evaluation of the temporal window for drug delivery following ultrasound-mediated membrane permeability enhancement. Mol. Imaging Biol. 2011, 13:239-249.
134. Wrenn S.P., Dicker S.M., Small E.F., Dan N.R., Mleczko M., Schmitz G., Lewin P.A. Bursting bubbles and bilayers. Theranostics 2012, 2:1140-1159.
135. Rapoport N., Gao Z., Kennedy A. Multifunctional nanoparticles for combining ultrasonic tumor imaging and targeted chemotherapy. J. Natl. Cancer Inst. 2007, 99:1095-1106.
136. Park J., Zhang Y., Vykhodtseva N., Jolesz F.A., McDannold N.J. The kinetics of blood-brain barrier permeability and targeted doxorubicin delivery into brain induced by focused ultrasound. J. Control. Release 2012, 162:134-142.
137. Marty B., Larrat B., Van Landeghem M., Robic C., Robert P., Port M., Le Bihan D., Pernot M., Tanter M., Lethimonnier F., Meriaux S. Dynamic study of blood-brain barrier closure after its disruption using ultrasound: a quantitative analysis. J. Cereb. Blood Flow Metab. 2012, 32:1948-1958.
138. Hynynen K. Ultrasound for drug and gene delivery to the brain. Adv. Drug Deliv. Rev. 2008, 60:1209-1217.
139. Choi J.J., Selert K., Vlachos F., Wong A., Konofagou E.E. Noninvasive and localized neuronal delivery using short ultrasonic pulses and microbubbles. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:16539-16544.