Assessment of the biodistribution of an [18F]FDG-loaded perfluorocarbon double emulsion using dynamic micro-PET in rats

Contrast Media and Molecular Imaging

Volumn 8, Issue 4, 2013, Pages 366-374

  Fabiilli, Mario L ^a   Piert, Morand R ^a   Koeppe, Robert A ^a   Sherman, Phillip S ^a   Quesada, Carole A ^a   Kripfgans, Oliver D ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Acoustic droplet vaporization; Biodistribution; Emulsion; Micro PET; Perfluorocarbon; Responsive agents; Ultrasound

Indexed keywords

FLUOROCARBON; FLUORODEOXYGLUCOSE F 18;

ANIMAL EXPERIMENT; AREA UNDER THE CURVE; ARTICLE; BRAIN; CONTROLLED STUDY; DIFFUSION; DRUG ACCUMULATION; DRUG DISTRIBUTION; DRUG RETENTION; DRUG STABILITY; DRUG TRANSPORT; ECHOGRAPHY; EMULSION; FEMALE; GLIOSARCOMA; IN VITRO STUDY; LUNG CAPILLARY; NONHUMAN; PLASMA CONCENTRATION-TIME CURVE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RADIOLOGICAL PARAMETERS; RAT; STANDARDIZED UPTAKE VALUE; TIME TO MAXIMUM PLASMA CONCENTRATION;

ANIMALS; CELL LINE, TUMOR; FEMALE; FLUOROCARBONS; FLUORODEOXYGLUCOSE F18; POSITRON-EMISSION TOMOGRAPHY; RATS; RATS, INBRED F344;

EID: 84876843670     PISSN: 15554309     EISSN: 15554317     Source Type: Journal    
DOI: 10.1002/cmmi.1532     Document Type: Article

References (64)

1. Ferrara KW, Pollard R, Borden MA. Ultrasound microbubble contrast agents: fundamentals and application to gene and drug delivery. Annu Rev Biomed Eng 2007; 9: 425-447.
2. Miller DL, Averkiou MA, Brayman AA, Everbach EC, Holland CK, Wible JH, Wu J. Bioeffects considerations for diagnostic ultrasound contrast agents. J Ultrasound Med 2008; 27(4): 611-632.
3. Pillai R, Marinelli ER, Fan H, Nanjappan P, Song B, von Wronski MA, Cherkaoui S, Tardy I, Pochon S, Schneider M, Nunn AD, Swenson RE. A phospholipid-PEG2000 conjugate of a vascular endothelial growth factor receptor 2 (VEGFR2)-targeting heterodimer peptide for contrast-enhanced ultrasound imaging of angiogenesis. Bioconjug Chem 2010; 21(3): 556-562.
4. Bzyl J, Lederle W, Rix A, Grouls C, Tardy I, Pochon S, Siepmann M, Penzkofer T, Schneider M, Kiessling F, Palmowski M. Molecular and functional ultrasound imaging in differently aggressive breast cancer xenografts using two novel ultrasound contrast agents (BR55 and BR38). Eur Radiol 2011; 21(9): 1988-1995.
5. Datta S, Coussios CC, Ammi AY, Mast TD, de Courten-Myers GM, Holland CK. Ultrasound-enhanced thrombolysis using Definity as a cavitation nucleation agent. Ultrasound Med Biol 2008; 34(9): 1421-1433.
6. Watanabe Y, Horie S, Funaki Y, Kikuchi Y, Yamazaki H, Ishii K, Mori S, Vassaux G, Kodama T. Delivery of Na/I symporter gene into skeletal muscle using nanobubbles and ultrasound: visualization of gene expression by PET. J Nucl Med 2010; 51(6): 951-958.
7. Tartis MS, McCallan J, Lum AFH, LaBell R, Stieger SM, Matsunaga TO, Ferrara KW. Therapeutic effects of paclitaxel-containing ultrasound contrast agents. Ultrasound Med Biol 2006; 32(11): 1771-1780.
8. Cerroni B, Chiessi E, Margheritelli S, Oddo L, Paradossi G. Polymer shelled microparticles for a targeted doxorubicin delivery in cancer therapy. Biomacromolecules 2011; 12(3): 593-601.
9. Yu TH, Fan XL, Xiong SH, Hu K, Wang ZB. Microbubbles assist goat liver ablation by high intensity focused ultrasound. Eur Radiol 2006; 16(7): 1557-1563.
10. Diaz-Lopez R, Tsapis N, Fattal E. Liquid perfluorocarbons as contrast agents for ultrasonography and 19F-MRI. Pharm Res 2010; 27(1): 1-16.
11. Fabiilli ML, Haworth KJ, Sebastian IE, Kripfgans OD, Carson PL, Fowlkes JB. Delivery of chlorambucil using an acoustically-triggered perfluoropentane emulsion. Ultrasound Med Biol 2010; 36(8): 1364-1375.
12. Hwang TL, Lin YJ, Chi CH, Huang TH, Fang JY. Development and evaluation of perfluorocarbon nanobubbles for apomorphine delivery. J Pharmacol Sci 2009; 98(10): 3735-3747.
13. Rapoport NY, Kennedy AM, Shea JE, Scaife CL, Nam K-H. Controlled and targeted tumor chemotherapy by ultrasound-activated nanoemulsions/microbubbles. J Control Release 2009; 138(2): 268-276.
14. Wang CH, Kang ST, Lee YH, Luo YL, Huang YF, Yeh CK. Aptamer-conjugated and drug-loaded acoustic droplets for ultrasound theranosis. Biomaterials 2012; 33(6): 1939-1947.
15. Zhang M, Fabiilli ML, Haworth KJ, Padilla F, Swanson SD, Kripfgans OD, Carson PL, Fowlkes JB. Acoustic droplet vaporization for enhancement of thermal ablation by high intensity focused ultrasound. Acad Radiol 2011; 18(9): 1123-1132.
16. Zhang P, Porter T. An in vitro study of a phase-shift nanoemulsion: a potential nucleation agent for bubble-enhanced hifu tumor ablation. Ultrasound Med Biol 2010; 36(11): 1856-1866.
17. de Jong N, ten Cate FJ, Vletter WB, Roelandt JRTC. Quantification of transpulmonary echocontrast effects. Ultrasound Med Biol 1993; 19(4): 279-288.
18. Leakakos T, Schutt EG, Calvin JC, Smith D, Bradley JD, Strnat CA, del Balzo U, Hazard DY, Otto S, Fields TK, Keipert PE, Klein DH, Flaim SF. Pulmonary gas trapping differences among animal species in response to intravenous infusion of perfluorocarbon emulsions. Artif Cell Blood Sub 1994; 22(4): 1199-1204.
19. Schutt E, Barber P, Fields T, Flaim S, Horodniak J, Keipert P, Kinner R, Kornburst L, Leakakos T, Pelura T, Weers J, Houmes R, Lachmann B. Proposed mechanism of pulmonary gas trapping (PGT) following intravenous perfluorocarbon emulsion administration. Artif Cell Blood Sub 1994; 22(4): 1205-1214.
20. Rapoport N, Nam KH, Gupta R, Gao ZG, Mohan P, Payne A, Todd N, Liu X, Kim T, Shea J, Scaife C, Parker DL, Jeong EK, Kennedy AM. Ultrasound-mediated tumor imaging and nanotherapy using drug loaded, block copolymer stabilized perfluorocarbon nanoemulsions. J Control Release 2011; 153(1): 4-15.
21. Willmann JK, Cheng Z, Davis C, Lutz AM, Schipper MK, Nielsen CH, Gambhir SS. Targeted microbubbles for imaging tumor angiogenesis: assessment of whole-body biodistribution with dynamic micro-PET in mice. Radiology 2008; 249(1): 212-219.
22. Perkins AC, Frier M, Hindle AJ, Blackshaw PE, Bailey SE, Hebden JM, Middleton SM, Wastie ML. Human biodistribution of an ultrasound contrast agent (Quantison(TM)) by radiolabelling and gamma scintigraphy. Br J Radiol 1997; 70(834): 603-611.
23. Ferrara KW, Borden MA, Zhang H. Lipid-shelled vehicles: engineering for ultrasound molecular imaging and drug delivery. Acc Chem Res 2009; 42(7): 881-892.
24. Tartis MS, Kruse DE, Zheng HR, Zhang H, Kheirolomoom A, Marik J, Ferrara KW. Dynamic microPET imaging of ultrasound contrast agents and lipid delivery. J Control Release 2008; 131(3): 160-166.
25. Kok MB, de Vries A, Abdurrachim D, Prompers JJ, Grull H, Nicolay K, Strijkers GJ. Quantitative H-1 MRI, F-19 MRI, and F-19 MRS of cell-internalized perfluorocarbon paramagnetic nanoparticles. Contrast Media Mol I 2011; 6(1): 19-27.
26. Mohan P, Rapoport N. Doxorubicin as a molecular nanotheranostic agent: effect of doxorubicin encapsulation in micelles or nanoemulsions on the ultrasound-mediated intracellular delivery and nuclear trafficking. Mol Pharm 2010; 7(6): 1959-1973.
27. Gorelikov I, Martin AL, Seo M, Matsuura N. Silica-coated quantum dots for optical evaluation of perfluorocarbon droplet interactions with cells. Langmuir 2011; 27(24): 15024-15033.
28. Anderson CR, Hu XW, Zhang H, Tlaxca J, Decleves AE, Houghtaling R, Sharma K, Lawrence M, Ferrara KW, Rychak JJ. Ultrasound molecular imaging of tumor angiogenesis with an integrin targeted microbubble contrast agent. Invest Radiol 2011; 46(4): 215-224.
29. Piroth MD, Pinkawa M, Holy R, Klotz J, Nussen S, Stoffels G, Coenen HH, Kaiser HJ, Langen KJ, Eble MJ. Prognostic value of early [(18)F]fluoroethyltyrosine positron emission tomography after radiochemotherapy in glioblastoma multiforme. Int J Radiat Oncol 2011; 80(1): 176-184.
30. Basu S Personalized versus evidence-based medicine with PET-based imaging. Nat Rev Clin Oncol 2010; 7(11): 665-668.
31. Fabiilli ML, Lee JA, Kripfgans OD, Carson PL, Fowlkes JB. Delivery of water-soluble drugs using acoustically triggered perfluorocarbon double emulsions. Pharm Res 2010; 27(12): 2753-2765.
32. Rajian JR, Fabiilli ML, Fowlkes JB, Carson PL, Wang X. Drug delivery monitoring by photoacoustic tomography with an ICG encapsulated double emulsion. Opt Express 2011;19(15):14335-14347.
33. Couture O, Faivre M, Pannacci N, Babataheri A, Servois V, Tabeling P, Tanter M. Ultrasound internal tattooing. Med Phys 2011; 38(2): 1116-1123.
34. Apfel RE, Apfel Enterprises Inc., assignee. Activatable infusable dispersions containing drops of a superheated liquid for methods of therapy and diagnosis. United States Patent, November 1998.
35. Kripfgans OD, Fowlkes JB, Miller DL, Eldevik OP, Carson PL. Acoustic droplet vaporization for therapeutic and diagnostic applications. Ultrasound Med Biol 2000; 26(7): 1177-1189.
36. Sheeran PS, Luois S, Dayton PA, Matsunaga TO. Formulation and acoustic studies of a new phase-shift agent for diagnostic and therapeutic ultrasound. Langmuir 2011; 27(17): 10412-10420.
37. Martz TD, Sheeran PS, Bardin D, Lee AP, Dayton PA. Precision manufacture of phase-change perfluorocarbon droplets using microfluidics. Ultrasound Med Biol 2011; 37(11): 1952-1957.
38. Fabiilli ML, Haworth KJ, Fakhri NH, Kripfgans OD, Carson PL, Fowlkes JB. The role of inertial cavitation in acoustic droplet vaporization. IEEE Trans Ultrason Ferroelectr Freq Control 2009; 56(5): 1006-1017.
39. Fang JY, Hung CF, Hua SC, Hwang TL. Acoustically active pefluorocarbon nanoemulsions as drug delivery carriers for camptothecin: drug release and cytoxicity against cancer cells. Ultrasonics 2009; 49(1): 39-46.
40. Rapoport N, Gao Z, Kennedy A. Multifunctional nanoparticles for combining ultrasonic tumor imaging and targeted chemotherapy. J Natl Cancer Inst 2007; 99(14): 1095-1106.
41. Kripfgans OD, Fowlkes JB, Woydt M, Eldevik OP, Carson PL. In vivo droplet vaporization for occlusion therapy and phase aberration correction. IEEE Trans Ultrason Ferroelectr Freq Control 2002; 49(2): 726-738.
42. Kripfgans OD, Orifici CM, Carson PL, Ives KA, Eldevik OP, Fowlkes JB. Acoustic droplet vaporization for temporal and spatial control of tissue occlusion: a kidney study. IEEE Trans Ultrason Ferroelectr Freq Control 2005; 52(7): 1101-1110.
43. Zhang M, Fabiilli ML, Haworth KJ, Fowlkes JB, Kripfgans OD, Roberts WW, Ives KA, Carson PL. Initial investigation of acoustic droplet vaporization for occlusion in canine kidney. Ultrasound Med Biol 2010; 36(10): 1691-1703.
44. Haworth KJ, Fowlkes JB, Carson PL, Kripfgans OD. Towards aberration correction of transcranial ultrasound using acoustic droplet vaporization. Ultrasound Med Biol 2008; 34(3): 435-445.
45. Bentley PK, Johnson OL, Washington C, Lowe KC. Uptake of concentrated perfluorocarbon emulsions into rat lymphoid-tissues. J Pharm Pharmacol 1993; 45(3): 182-185.
46. Satterfield R, Tarter VM, Schumacher DJ, Tran P, Mattrey RF. Comparison of different perfluorocarbons as ultrasound contrast agents. Invest Radiol 1993; 28(4): 325-331.
47. Riess JG. Oxygen carriers ('blood substitutes') - raison d'etre, chemistry, and some physiology. Chem Rev 2001; 101(9): 2797-2919.
48. Couture O, Urban A, Bretagne A, Martinez L, Tanter M, Tabeling P. In vivo targeted delivery of large payloads with an ultrasound clinical scanner. Med Phys 2012; 39(8): 5229-5237.
49. Lanza GM, Wallace KD, Scott MJ, Cacheris WP, Abendschein DR, Christy DH, Sharkley AM, Miller JG, Gaffney PJ, Wickline SA. A novel site-targeted ultrasonic contrast agent with broad biomedical application. Circulation 1996; 94(12): 3334-3340.
50. Ganta S, Paxton JW, Baguley BC, Garg S. Pharmacokinetics and pharmacodynamics of chlorambucil delivered in parenteral emulsion. Int J Pharm 2008; 360(1-2): 115-121.
51. Apfel RE. Superheated drop detector. Nucl Instrum Meth 1979; 162(1-3): 603-608.
52. d'Errico F. Radiation dosimetry and spectrometry with superheated emulsions. Nucl Instrum Meth Phys Res B 2001; 184: 229-254.
53. Ficheux MF, Bonakdar L, Leal-Calderon F, Bibette J. Some stability criteria for double emulsions. Langmuir 1998; 14(10): 2702-2706.
54. West CML, Jones T, Price P. The potential of positron-emission tomography to study anticancer-drug resistance. Nat Rev Cancer 2004; 4(6): 457-469.
55. Toyama H, Ichise M, Liow JS, Vines DC, Seneca NM, Modell KJ, Seidel J, Green MV, Innis RB. Evaluation of anesthesia effects on [F-18]FDG uptake in mouse brain and heart using small animal PET. Nucl Med Biol 2004; 31(2): 251-256.
56. Fueger BJ, Czernin J, Hildebrandt I, Tran C, Halpern BS, Stout D, Phelps ME, Weber WA. Impact of animal handling on the results of F-18-FDG PET studies in mice. J Nucl Med 2006; 47(6): 999-1006.
57. Canaud B, Aljama P, Tielemans C, Gasparovic V, Gutierrez A, Locatelli F. Pathochemical toxicity of perfluorocarbon-5070, a liquid test performance fluid previously used in dialyzer manufacturing, confirmed in animal experiment. J Am Soc Nephrol 2005; 16(6): 1819-1823.
58. Kutscher HL, Chao P, Deshmukh M, Singh Y, Hu P, Joseph LB, Reimer DC, Stein S, Laskin DL, Sinko PJ. Threshold size for optimal passive pulmonary targeting and retention of rigid microparticles in rats. J Control Release 2010; 143(1): 31-37.
59. Schwinn DA, Mcintyre RW, Reves JG. Isoflurane-induced vasodilation - role of the alpha-adrenergic nervous-system. Anesth Analg 1990; 71(5): 451-459.
60. Owens DE, Peppas NA. Opsonization, biodistribution, and pharmaokinetics of polymeric nanoparticles. Int J Pharm 2006; 307(1): 93-102.
61. Giraudeau C, Djemai B, Ghaly MA, Boumezbeur F, Meriaux S, Robert P, Port M, Robic C, Le Bihan D, Lethimonnier F, Valette J. High sensitivity 19F MRI of a perfluorooctyl bromide emulsion: application to a dynamic biodistribution study and oxygen tension mapping in the mouse liver and spleen. NMR Biomed 2012; 25(4): 654-660.
62. Troster SD, Muller U, Kreuter J. Modification of the body distribution of poly(methyl methacrylate) nanoparticles in rats by coating with surfactants. Int J Pharm 1990; 61(1-2): 85-100.
63. Vittaz M, Bazile D, Spenlehauer G, Verrecchia T, Veillard M, Puisieux F, Labarre D. Effect of PEO surface density on long-circulating PLA-PEO nanoparticles which are very low complement activators. Biomaterials 1996; 17(16): 1575-1581.
64. Knoess C, Siegel S, Smith A, Newport D, Richerzhagen N, Winkeler A, Jacobs A, Goble RN, Graf R, Wienhard K, Heiss WD. Performance evaluation of the microPET R4 PET scanner for rodents. Eur J Nucl Med Mol Imag 2003; 30(5): 737-747.