Ultrasonic enhancement of drug penetration in solid tumors

Frontiers in Oncology

Volumn 3 AUG, Issue , 2013, Pages

  Lai, Chun Yen ^a   Fite, Brett Z ^a   Ferrara, Katherine W ^a  

^a University of California   (United States)

Author keywords

Enhanced drug delivery; Sonoporation; Tumor penetration; Ultrasound; Vascular permeability

Indexed keywords

DOXORUBICIN; LIPOSOME; NANOPARTICLE;

ARTICLE; DISEASE ASSOCIATION; DRUG PENETRATION; DRUG RELEASE; EPITHELIAL MESENCHYMAL TRANSITION; HIGH INTENSITY FOCUSED ULTRASOUND; HUMAN; HYPERTHERMIA; MICROBUBBLE; NUCLEAR MAGNETIC RESONANCE IMAGING; PERFUSION; PHASE TRANSITION; POSITRON EMISSION TOMOGRAPHY; RADIOFREQUENCY ABLATION; SIGNAL NOISE RATIO; SOLID TUMOR; TUMOR ABLATION; TUMOR BLOOD FLOW; TUMOR VASCULARIZATION; ULTRASOUND;

EID: 84888767550     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00204     Document Type: Article

References (124)

1. Wall PD, Fry WJ, Stephens R, Tucker D, Lettvin JY. Changes produced in the central nervous system by ultrasound. Science (1951) 114:686-7. doi:10.1126/science.114.2974.686
2. Fry WJ, Dunn F. Ultrasonic irradiation of the central nervous system at high sound levels. J Acoust Soc Am (1956) 28:129-31. doi:10.1121/1.1908200
3. Fry FJ, Ades HW, Fry WJ. Production of reversible changes in the central nervous system by ultrasound. Science (1958) 127:83-4. doi:10.1126/science.127.3289.83
4. Lynn JG, Zwemer RL, Chick AJ, Miller AE. A new method for the generation and use of focused ultrasound in experimental biology. J Gen Physiol (1942) 26:179-93. doi:10.1085/jgp.26.2.179
5. Lynn J, Zwemer RL, Chick AJ. The biological application of focused ultrasound waves. Science (1942) 96:119-20. doi:10.1126/science.96.2483.119
6. Fry WJ, Wulff VJ, Tucker D, Fry FJ. Physical factors involved in ultrasonically induced changes in living systems: Identification of non-temperature effects. J Acoust Soc Am (1950) 22:867-76. doi:10.1121/1.1906707
7. Watson K, Lai CY, Qin S, Kruse DE, Lin YC, Seo JW, et al. Ultrasound increases nanoparticle delivery by reducing intratumoral pressure and increasing transport in epithelial and epithelial-mesenchymal transition tumors. Cancer Res (2012) 72:1485-93. doi:10.1158/0008-5472.CAN-11-3232
8. Wang S, Shin IS, Hancock H, Jang B-S, Kim H-S, Lee SM, et al. Pulsed high intensity focused ultrasound increases penetration and therapeutic efficacy of monoclonal antibodies in murine xenograft tumors. J Control Release (2012) 162:218-24. doi:10.1016/j.jconrel.2012.06.025
9. Frenkel V. Ultrasound mediated delivery of drugs and genes to solid tumors. Adv Drug Deliv Rev (2008) 60:1193-208. doi:10.1016/j.addr.2008.03.007
10. Dewhirst MW, Vujaskovic Z, Jones E, Thrall D. Re-setting the biologic rationale for thermal therapy. Int J Hyperthermia (2005) 21:779-90. doi:10.1080/02656730500271668
11. Jones EL, Oleson JR, Prosnitz LR, Samulski TV, Vujaskovic Z, Yu DH, et al. Randomized trial of hyperthermia and radiation for superficial tumors. J Clin Oncol (2005) 23:3079-85. doi:10.1200/JCO.2005.05.520
12. Gaber MH, Wu NZ, Hong K, Huang SK, Dewhirst MW, Papahadjopoulos D. Thermosensitive liposomes: extravasation and release of contents in tumor microvascular networks. Int J Radiat Oncol Biol Phys (1996) 36:1177-87. doi:10.1016/S0360-3016(96)00389-6
13. Yuh EL, Shulman SG, Mehta SA, Xie J, Chen L, Frenkel V, et al. Delivery of systemic chemotherapeutic agent to tumors by using focused ultrasound: study in a murine model. Radiology (2005) 234(2):431-7. doi:10.1148/radiol.2342030889
14. Ahmed M, Monsky WE, Girnun G, Lukyanov A, D'Ippolito G, Kruskal JB, et al. Radiofrequency thermal ablation sharply increases intratumoral liposomal doxorubicin accumulation and tumor coagulation. Cancer Res (2003) 63:6327-33.
15. Goldberg SN, Ahmed M. Minimally invasive image-guided therapies for hepatocellular carcinoma. J Clin Gastroenterol (2002) 35:S115-29. doi:10.1097/00004836-200211002-00008
16. Wood BJ, Poon RT, Locklin JK, Dreher MR, Ng KK, Eugeni M, et al. Phase I study of heat-deployed liposomal doxorubicin during radiofrequency ablation for hepatic malignancies. J Vasc Interv Radiol (2012) 23:248-55. doi:10.1016/j.jvir.2011.10.018
17. Viglianti BL, Abraham SA, Michelich CR, Yarmolenko PS, MacFall JR, Bally MB, et al. In vivo monitoring of tissue pharmacokinetics of liposome/drug using MRI: illustration of targeted delivery. Magn Reson Med (2004) 51:1153-62. doi:10.1002/mrm.20074
18. Ponce AM, Viglianti BL, Yu DH, Yarmolenko PS, Michelich CR, Woo J, et al. Magnetic resonance imaging of temperature-sensitive liposome release: drug dose painting and antitumor effects. J Natl Cancer Inst (2007) 99:53-63. doi:10.1093/jnci/djk005
19. Kong G, Anyarambhatla G, Petros WP, Braun RD, Colvin OM, Needham D, et al. Efficacy of liposomes and hyperthermia in a human tumor xenograft model: importance of triggered drug release. Cancer Res (2000) 60:6950-7.
20. Dromi S, Frenkel V, Luk A, Traughber B, Angstadt M, Bur M, et al. Pulsed-high intensity focused ultrasound and low temperature sensitive liposomes for enhanced targeted drug delivery and antitumor effect. Clin Cancer Res (2007) 13:2722-7. doi:10.1158/1078-0432.CCR-06-2443
21. Loo C, Lowery A, Halas N, West J, Drezek R. Immunotargeted nanoshells for integrated cancer imaging and therapy. Nano Lett (2005) 5:709-11. doi:10.1021/nl050127s
22. Derfus AM, von Maltzahn G, Harris TJ, Duza T, Vecchio KS, Ruoslahti E, et al. Remotely triggered release from magnetic nanoparticles. Adv Mater (2007) 19:3932-6. doi:10.1002/adma.200700091
23. Gannon CJ, Patra CR, Bhattacharya R, Mukherjee P, Curley SA. Intracellular gold nanoparticles enhance non-invasive radiofrequency thermal destruction of human gastrointestinal cancer cells. J Nanobiotechnol (2008) 6:2. doi:10.1186/1477-3155-6-2
24. Yatvin MB, Weinstein JN, Dennis WH, Blumenthal R. Design of liposomes for enhanced local release of drugs by hyperthermia. Science (1978) 202:1290-3. doi:10.1126/science.364652
25. Paoli EE, Kruse DE, Seo JW, Zhang H, Kheirolomoom A, Watson KD, et al. An optical and microPET assessment of thermally-sensitive liposome biodistribution in the Met-1 tumor model: Importance of formulation. J Control Release (2010) 143:13-22. doi:10.1016/j.jconrel.2009.12.010
26. Needham D, Anyarambhatla G, Kong G, Dewhirst MW. A new temperature-sensitive liposome for use with mild hyperthermia: characterization and testing in a human tumor xenograft model. Cancer Res (2000) 60:1197-201.
27. Mills JK, Needham D. Lysolipid incorporation in dipalmitoylphosphatidylcholine bilayer membranes enhances the ion permeability and drug release rates at the membrane phase transition. Biochim Biophys Acta (2005) 1716:77-96. doi:10.1016/j.bbamem.2005.08.007
28. Tagami T, Ernsting MJ, Li S-D. Optimization of a novel and improved thermosensitive liposome formulated with DPPC and a Brij surfactant using a robust in vitro system. J Control Release (2011) 154:290-7. doi:10.1016/j.jconrel.2011.05.020
29. Lindner LH, Eichhorn ME, Eibl H, Teichert N, Schmitt-Sody M, Issels RD, et al. Novel temperature-sensitive liposomes with prolonged circulation time. Clin Cancer Res (2004) 10:2168-78. doi:10.1158/1078-0432.CCR-03-0035
30. Kheirolomoom A, Mahakian LM, Lai C-Y, Lindfors HA, Seo JW, Paoli EE, et al. Copper-doxorubicin as a nanoparticle cargo retains efficacy with minimal toxicity. Mol Pharm (2010) 7:1948-58. doi:10.1021/mp100245u
31. Partanen A, Yarmolenko PS, Viitala A, Appanaboyina S, Haemmerich D, Ranjan A, et al. Mild hyperthermia with magnetic resonance-guided high-intensity focused ultrasound for applications in drug delivery. Int J Hyperthermia (2012) 28:320-36. doi:10.3109/02656736.2012.680173
32. Staruch RM, Ganguly M, Tannock IF, Hynynen K, Chopra R. Enhanced drug delivery in rabbit VX2 tumours using thermosensitive liposomes and MRI-controlled focused ultrasound hyperthermia. Int J Hyperthermia (2012) 28:776-87. doi:10.3109/02656736.2012.736670
33. Lum AFH, Borden MA, Dayton PA, Kruse DE, Simon SI, Ferrara KW. Ultrasound radiation force enables targeted deposition of model drug carriers loaded on microbubbles. J Control Release (2006) 111:128-34. doi:10.1016/j.jconrel.2005.11.006
34. Kheirolomoom A, Dayton PA, Lum AFH, Little E, Paoli EE, Zheng H, et al. Acoustically-active microbubbles conjugated to liposomes: characterization of a proposed drug delivery vehicle. J Control Release (2007) 118:275-84. doi:10.1016/j.jconrel.2006.12.015
35. Kwan JJ, Kaya M, Borden MA, Dayton PA. Theranostic oxygen delivery using ultrasound and microbubbles. Theranostics (2012) 2:1174-84. doi:10.7150/thno.4410
36. Rapoport N. Phase-shift, stimuli-responsive perfluorocarbon nanodroplets for drug delivery to cancer. Wiley Interdiscip Rev Nanomed Nanobiotechnol (2012) 4:492-510. doi:10.1002/wnan.1176
37. Chomas JE, Dayton PA, May D, Allen J, Klibanov A, Ferrara K. Optical observation of contrast agent destruction. Appl Phys Lett (2000) 77:1056-8. doi:10.1063/1.1287519
38. Chomas JE, Dayton P, May D, Ferrara K. Threshold of fragmentation for ultrasonic contrast agents. J Biomed Opt (2001) 6:141-50. doi:10.1117/1.1352752
39. Chomas JE, Dayton P, Allen J, Morgan K, Ferrara KW. Mechanisms of contrast agent destruction. IEEE Trans Ultrason Ferroelectr Freq Control (2001) 48:232-48. doi:10.1109/58.896136
40. Qin S, Caskey CF, Ferrara KW. Ultrasound contrast microbubbles in imaging and therapy: physical principles and engineering. Phys Med Biol (2009) 54:R27-57. doi:10.1088/0031-9155/54/6/R01
41. Caskey CF, Stieger SM, Qin S, Dayton PA, Ferrara KW. Direct observations of ultrasound microbubble contrast agent interaction with the microvessel wall. J Acoust Soc Am (2007) 122:1191-200. doi:10.1121/1.2747204
42. Caskey CF, Qin S, Dayton PA, Ferrara KW. Microbubble tunneling in gel phantoms. J Acoust Soc Am (2009) 125:EL183-9. doi:10.1121/1.3097679
43. Kilroy JP, Klibanov AL, Wamhoff BR, Hossack JA. Intravascular ultrasound catheter to enhance microbubble-based drug delivery via acoustic radiation force. IEEE Trans Ultrason Ferroelectr Freq Control (2012) 59:2156-66. doi:10.1109/TUFFC.2012.2442
44. Miller DL, Song J. Lithotripter shock waves with cavitation nucleation agents produce tumor growth reduction and gene transfer in vivo. Ultrasound Med Biol (2002) 28:1343-8. doi:10.1016/S0301-5629(02)00572-0
45. Miller DL, Song J. Tumor growth reduction and DNA transfer by cavitation-enhanced high-intensity focused ultrasound in vivo. Ultrasound Med Biol (2003) 29:887-93. doi:10.1016/S0301-5629(03)00031-0
46. Hauff P, Seemann S, Reszka R, Schultze-Mosgau M, Reinhardt M, Buzasi T, et al. Evaluation of gas-filled microparticles and sonoporation as gene delivery system: feasibility study in rodent tumor models. Radiology (2005) 236:572-8. doi:10.1148/radiol.2362040870
47. Howard CM, Forsberg F, Minimo C, Liu JB, Merton DA, Claudio PP. Ultrasound guided site specific gene delivery system using adenoviral vectors and commercial ultrasound contrast agents. J Cell Physiol (2006) 209:413-21. doi:10.1002/jcp.20736
48. Sonoda S, Tachibana K, Uchino E, Yamashita T, Sakoda K, Sonoda KH, et al. Inhibition of melanoma by ultrasound-microbubble-aided drug delivery suggests membrane permeabilization. Cancer Biol Ther (2007) 6:1276-83.
49. Burke CW, Klibanov AL, Sheehan JP, Price RJ. Inhibition of glioma growth by microbubble activation in a subcutaneous model using low duty cycle ultrasound without significant heating. J Neurosurg (2011) 114:1654-61. doi:10.3171/2010.11.JNS101201
50. 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) 20:20. doi:10.1016/j.ultrasmedbio.2007.11.009
51. Choi JJ, Feshitan JA, Baseri B, Shougang W, Yao-Sheng T, Borden MA, et al. Microbubble-size dependence of focused ultrasound-induced blood-brain barrier opening in mice in vivo. IEEE Trans Biomed Eng (2010) 57:145-54. doi:10.1109/TBME.2009.2034533
52. Stieger SM, Caskey CF, Adamson RH, Qin S, Curry FR, Wisner ER, et al. Enhancement of vascular permeability with low-frequency contrast-enhanced ultrasound in the chorioallantoic membrane model. Radiology (2007) 243:112-21. doi:10.1148/radiol.2431060167
53. Delalande A, Kotopoulis S, Postema M, Midoux P, Pichon C. Sonoporation: mechanistic insights and ongoing challenges for gene transfer. Gene (2013) 525(2):191-9. doi:10.1016/j.gene.2013.03.095
54. Sirsi SR, Borden MA. Advances in ultrasound mediated gene therapy using microbubble contrast agents. Theranostics (2012) 2:1208-22. doi:10.7150/thno.4306
55. Dayton PA, Zhao S, Bloch SH, Schumann P, Penrose K, Matsunaga TO, et al. Application of ultrasound to selectively localize nanodroplets for targeted imaging and therapy. Mol Imaging (2006) 5:160-74.
56. Dayton PA, Morgan KE, Klibanov ALS, Brandenburger G, Nightingale KR, Ferrara KW. A preliminary evaluation of the effects of primary and secondary radiation forces on acoustic contrast agents. IEEE Trans Ultrason Ferroelectr Freq Control (1997) 44:1264-77. doi:10.1109/58.656630
57. Dayton P, Klibanov A, Brandenburger G, Ferrara K. Acoustic radiation force in vivo: a mechanism to assist targeting of microbubbles. Ultrasound Med Biol (1999) 25:1195-201. doi:10.1016/S0301-5629(99)00062-9
58. O'Reilly MA, Hynynen K. Ultrasound enhanced drug delivery to the brain and central nervous system. Int J Hyperthermia (2012) 28:386-96. doi:10.3109/02656736.2012.666709
59. Hynynen K, McDannold N, Martin H, Jolesz FA, Vykhodtseva N. The threshold for brain damage in rabbits induced by bursts of ultrasound in the presence of an ultrasound contrast agent (optison). Ultrasound Med Biol (2003) 29:473-81. doi:10.1016/S0301-5629(02)00741-X
60. Baseri B, Choi JJ, Deffieux T, Samiotaki G, Tung Y-S, Olumolade O, et al. Activation of signaling pathways following localized delivery of systemically administered neurotrophic factors across the blood-brain barrier using focused ultrasound and microbubbles. Phys Med Biol (2012) 57:N65-81. doi:10.1088/0031-9155/57/7/N65
61. Choi JJ, Feshitan JA, Shougang W, Yao-Sheng T, Baseri B, Borden MA, et al. The dependence of the ultrasound-induced blood-brain barrier opening characteristics on microbubble size in vivo. AIP Conf Proc (2009) 1113:58-62. doi:10.1063/1.3131471
62. Choi JJ, Small SA, Konofagou EE. Optimization of blood-brain barrier opening in mice using focused ultrasound. IEEE Ultrasonics Symposium (IEEE Cat. No.06CH37777); 2006 Oct 3-6; Vancouver, Canada (2006). p. 540-3.
63. Konofagou EE, Choi J, Baseri B, Lee A. Characterization and optimization of trans-blood-brain barrier diffusion in vivo. AIP Conf Proc (2009) 1113:418-22. doi:10.1063/1.3131462
64. Konofagou EE, Choi J, Lee A, Baseri B. Molecular imaging through the blood-brain barrier: safety assessment and parameter dependence. Proc IEEE Int Symp Biomed Imaging; 2009 Jun 28 to Jul 1; Boston, MA (2009). p. 771-4. doi:10.1109/ISBI.2009.5193163
65. Konofagou EE, Tung Y-S, Choi J, Deffieux T, Baseri B, Vlachos F. Ultrasound-induced blood-brain barrier opening. Curr Pharm Biotechnol (2012) 13:1332-45. doi:10.2174/138920112800624364
66. Tung YS, Marquet F, Teichert T, Ferrera V, Konofagou EE. Feasibility of noninvasive cavitation-guided blood-brain barrier opening using focused ultrasound and microbubbles in nonhuman primates. Appl Phys Lett (2011) 98:163704-1-163704-3. doi:10.1063/1.3580763
67. Fite BZ, Liu Y, Kruse DE, Caskey CF, Walton JH, Lai CY, et al. Magnetic resonance thermometry at 7T for real-time monitoring and correction of ultrasound induced mild hyperthermia. PLoS ONE (2012) 7:e35509. doi:10.1371/journal.pone.0035509
68. Lai C, Kruse DE, Caskey CF, Stephens DN, Sutcliffe PL, Ferrara KW. Noninvasive thermometry assisted by a dual-function ultrasound transducer for mild hyperthermia. IEEE Trans Ultrason Ferroelectr Freq Control (2010) 57:2671-84. doi:10.1109/TUFFC.2010.1741
69. Roemer RB. Engineering aspects of hyperthermia therapy. Annu Rev Biomed Eng (1999) 1:347-76. doi:10.1146/annurev.bioeng.1.1.347
70. Rygh CB, Qin SP, Seo JW, Mahakian LM, Zhang H, Adamson R, et al. Longitudinal investigation of permeability and distribution of macromolecules in mouse malignant transformation using PET. Clin Cancer Res (2011) 17:550-9. doi:10.1158/1078-0432.CCR-10-2049
71. Qin S, Seo JW, Zhang H, Qi J, Curry F-RE, Ferrara KW. An imaging-driven model for liposomal stability and circulation. Mol Pharm (2009) 7:12-21. doi:10.1021/mp900122j
72. Wong AW, Ormsby E, Zhang H, Seo JW, Mahakian LM, Caskey CF, et al. A comparison of image contrast with (64)Cu-labeled long circulating liposomes and (18)F-FDG in a murine model of mammary carcinoma. Am J Nucl Med Mol Imaging (2013) 3:32-43.
73. Zheng J, Liu J, Dunne M, Jaffray D, Allen C. In vivo performance of a liposomal vascular contrast agent for CT and MR-based image guidance applications. Pharm Res (2007) 24:1193-201. doi:10.1007/s11095-006-9220-1
74. Huang H, Dunne M, Lo J, Jaffray DA, Allen C. Comparison of computed tomography-and optical image-based assessment of liposome distribution. Mol Imaging (2013) 12:148-60.
75. Kim CK, Park BK, Lee HM, Kim SS, Kim E. MRI techniques for prediction of local tumor progression after high-intensity focused ultrasonic ablation of prostate cancer. AJR Am J Roentgenol (2008) 190:1180-6. doi:10.2214/AJR.07.2924
76. Kim CK, Park BK, Kim B. Diffusion-weighted MRI at 3 T for the evaluation of prostate cancer. AJR Am J Roentgenol (2010) 194:1461-9. doi:10.2214/AJR.09.3654
77. Hynynen K, Damianou C, Darkazanli A, Unger E, Schenck JF. The feasibility of using MRI to monitor and guide noninvasive ultrasound surgery. Ultrasound Med Biol (1993) 19:91-2. doi:10.1016/0301-5629(93)90022-G
78. Funaki K, Fukunishi H, Funaki T, Sawada K, Kaji Y, Maruo T. Magnetic resonance-guided focused ultrasound surgery for uterine fibroids: relationship between the therapeutic effects and signal intensity of preexisting T2-weighted magnetic resonance images. Am J Obstet Gynecol (2007) 196:e1-6. doi:10.1016/j.ajog.2006.08.030
79. McDannold NJ, Hynynen K, Wolf D, Wolf G, Jolesz F. MRI evaluation of thermal ablation of tumors with focused ultrasound. J Magn Reson Imaging (1998) 8:91-100. doi:10.1002/jmri.1880080119
80. Punwani S, Emberton M, Walkden M, Sohaib A, Freeman A, Ahmed H, et al. Prostatic cancer surveillance following whole-gland high-intensity focused ultrasound: comparison of MRI and prostate-specific antigen for detection of residual or recurrent disease. Br J Radiol (2012) 85:720-8. doi:10.1259/bjr/61380797
81. Tempany CM, Stewart EA, McDannold N, Quade BJ, Jolesz FA, Hynynen K. MR imaging-guided focused ultrasound surgery of uterine leiomyomas: a feasibility study. Radiology (2003) 226:897-905. doi:10.1148/radiol.2271020395
82. Chen L, Bouley D, Yuh E, D'Arceuil H, Butts K. Study of focused ultrasound tissue damage using MRI and histology. J Magn Reson Imaging (1999) 10:146-53. doi:10.1002/(SICI)1522-2586(199908)10:2<146::AID-JMRI6>3.3.CO;2-3
83. Jacobs MA, Ouwerkerk R, Kamel I, Bottomley PA, Bluemke DA, Kim HS. Proton, diffusion-weighted imaging, and sodium (23Na) MRI of uterine leiomyomata after MR-guided high-intensity focused ultrasound: a preliminary study. J Magn Reson Imaging (2009) 29:649-56. doi:10.1002/jmri.21677
84. Cirillo S, Petracchini M, D'Urso L, Dellamonica P, Illing R, Regge D, et al. Endorectal magnetic resonance imaging and magnetic resonance spectroscopy to monitor the prostate for residual disease or local cancer recurrence after transrectal high-intensity focused ultrasound. BJU Int (2008) 102:452-8. doi:10.1111/j.1464-410X.2008.07633.x
85. Wu T, Felmlee JP, Greenleaf JF, Riederer SJ, Ehman RL. Assessment of thermal tissue ablation with MR elastography. Magn Reson Med (2001) 45:80-7. doi:10.1002/1522-2594(200101)45:1<80::AID-MRM1012>3.0.CO;2-Y
86. Kirkham AP, Emberton M, Hoh IM, Illing RO, Freeman AA, Allen C. MR imaging of prostate after treatment with high-intensity focused ultrasound. Radiology (2008) 246:833-44. doi:10.1148/radiol.2463062080
87. Rouviere O, Lyonnet D, Raudrant A, Colin-Pangaud C, Chapelon JY, Bouvier R, et al. MRI appearance of prostate following transrectal HIFU ablation of localized cancer. Eur Urol (2001) 40:265-74. doi:10.1159/000049786
88. Ben Cheikh A, Girouin N, Ryon-Taponnier P, Mege-Lechevallier F, Gelet A, Chapelon JY, et al. MR detection of local prostate cancer recurrence after transrectal high-intensity focused US treatment: preliminary results. J Radiol (2008) 89:571-7. doi:10.1016/S0221-0363(08)71483-5
89. Delli Castelli D, Dastru W, Terreno E, Cittadino E, Mainini F, Torres E, et al. In vivo MRI multicontrast kinetic analysis of the uptake and intracellular trafficking of paramagnetically labeled liposomes. J Control Release (2010) 144:271-9. doi:10.1016/j.jconrel.2010.03.005
90. Howseman AM, Bowtell RW. Functional magnetic resonance imaging: imaging techniques and contrast mechanisms. Philos Trans R Soc Lond B Biol Sci (1999) 354:1179-94. doi:10.1098/rstb.1999.0473
91. Gore JC, Manning HC, Quarles CC, Waddell KW, Yankeelov TE. Magnetic resonance in the era of molecular imaging of cancer. Magn Reson Imaging (2011) 29:587-600. doi:10.1016/j.mri.2011.02.003
92. Parker DL. Applications of NMR imaging in hyperthermia-an evaluation of the potential for localized tissue heating and noninvasive temperature monitoring. IEEE Trans Biomed Eng (1984) 31:161-7. doi:10.1109/TBME.1984.325382
93. Rieke V, Butts Pauly K. MR thermometry. J Magn Reson Imaging (2008) 27:376-90. doi:10.1002/jmri.21265
94. Parker DL, Smith V, Sheldon P, Crooks LE, Fussell L. Temperature distribution measurements in two-dimensional NMR imaging. Med Phys (1983) 10:321-5. doi:10.1118/1.595307
95. Le Bihan D, Delannoy J, Levin RL. Temperature mapping with MR imaging of molecular diffusion: application to hyperthermia. Radiology (1989) 171:853-7.
96. Young IR, Hand JW, Oatridge A, Prior MV, Forse GR. Further observations on the measurement of tissue T1 to monitor temperature in vivo by MRI. Magn Reson Med (1994) 31:342-5. doi:10.1002/mrm.1910310317
97. Graham SJ, Stanisz GJ, Kecojevic A, Bronskill MJ, Henkelman RM. Analysis of changes in MR properties of tissues after heat treatment. Magn Reson Med (1999) 42:1061-71. doi:10.1002/(SICI)1522-2594(199912)42:6<1061::AID-MRM10>3.0.CO;2-T
98. Chen J, Daniel BL, Pauly KB. Investigation of proton density for measuring tissue temperature. J Magn Reson Imaging (2006) 23:430-7. doi:10.1002/jmri.20516
99. Ishihara Y, Calderon A, Watanabe H, Okamoto K, Suzuki Y, Kuroda K, et al. Precise and fast temperature mapping using water proton chemical-shift. Magn Reson Med (1995) 34:814-23. doi:10.1002/mrm.1910340606
100. Galiana G, Branca RT, Jenista ER, Warren WS. Accurate temperature imaging based on intermolecular coherences in magnetic resonance. Science (2008) 322:421-4. doi:10.1126/science.1163242
101. Quesson B, de Zwart JA, Moonen CTW. Magnetic resonance temperature imaging for guidance of thermotherapy. J Magn Reson Imaging (2000) 12:525-33. doi:10.1002/1522-2586(200010)12:4<525::AID-JMRI3>3.0.CO;2-V
102. Peters RD, Hinks RS, Henkelman RM. Ex vivo tissue-type independence in proton-resonance frequency shift MR thermometry. Magn Reson Med (1998) 40:454-9. doi:10.1002/mrm.1910400316
103. Weidensteiner C, Kerioui N, Quesson B, de Senneville BD, Trillaud H, Moonen CT. Stability of real-time MR temperature mapping in healthy and diseased human liver. J Magn Reson Imaging (2004) 19:438-46. doi:10.1002/jmri.20019
104. Bankson JA, Stafford RJ, Hazle JD. Partially parallel imaging with phase-sensitive data: increased temporal resolution for magnetic resonance temperature imaging. Magn Reson Med (2005) 53:658-65. doi:10.1002/mrm.20378
105. Guo JY, Kholmovski EG, Zhang L, Jeong EK, Parker DL. k-Space inherited parallel acquisition (KIPA): application on dynamic magnetic resonance imaging thermometry. Magn Reson Imaging (2006) 24:903-15. doi:10.1016/j.mri.2006.03.001
106. Kohler MO, Mougenot C, Quesson B, Enholm J, Le Bail B, Laurent C, et al. Volumetric HIFU ablation under 3D guidance of rapid MRI thermometry. Med Phys (2009) 36:3521-35. doi:10.1118/1.3152112
107. Enholm JK, Kohler MO, Quesson B, Mougenot C, Moonen CTW, Sokka SD. Improved volumetric MR-HIFU ablation by robust binary feedback control. IEEE Trans Biomed Eng (2010) 57:103-13. doi:10.1109/TBME.2009.2034636
108. Ergun AS. Analytical and numerical calculations of optimum design frequency for focused ultrasound therapy and acoustic radiation force. Ultrasonics (2011) 51:786-94. doi:10.1016/j.ultras.2011.03.006
109. Wu F, Wang Z-B, Cao Y-D, Zhou Q, Zhang Y, Xu Z-L, et al. Expression of tumor antigens and heat-shock protein 70 in breast cancer cells after high-intensity focused ultrasound ablation. Ann Surg Oncol (2007) 14:1237-42. doi:10.1245/s10434-006-9275-6
110. Wu F, Zhou L, Chen WR. Host antitumour immune responses to HIFU ablation. Int J Hyperthermia (2007) 23:165-71. doi:10.1080/02656730701206638
111. Zhou Q, Zhu X-Q, Zhang J, Xu Z-L, Lu P, Wu F. Changes in circulating immunosuppressive cytokine levels of cancer patients after high intensity focused ultrasound treatment. Ultrasound Med Biol (2008) 34:81-7. doi:10.1016/j.ultrasmedbio.2007.07.013
112. Lu P, Zhu X-Q, Xu Z-L, Zhou Q, Zhang J, Wu F. Increased infiltration of activated tumor-infiltrating lymphocytes after high intensity focused ultrasound ablation of human breast cancer. Surgery (2009) 145:286-93. doi:10.1016/j.surg.2008.10.010
113. Xu Z-L, Zhu X-Q, Lu P, Zhou Q, Zhang J, Wu F. Activation of tumor-infiltrating antigen presenting cells by high intensity focused ultrasound ablation of human breast cancer. Ultrasound Med Biol (2009) 35:50-7. doi:10.1016/j.ultrasmedbio.2008.08.005
114. Zhang Y, Deng J, Feng J, Wu F. Enhancement of antitumor vaccine in ablated hepatocellular carcinoma by high-intensity focused ultrasound. World J Gastroenterol (2010) 16:3584-91. doi:10.3748/wjg.v16.i28.3584
115. Deng J, Zhang Y, Feng J, Wu F. Dendritic cells loaded with ultrasound-ablated tumor induce in vivo specific antitumor responses. Ultrasound Med Biol (2010) 36:441-8. doi:10.1016/j.ultrasmedbio.2009.12.004
116. Higgins JP, Bernstein MB, Hodge JW. Enhancing immune responses to tumor-associated antigens. Cancer Biol Ther (2009) 8:1440-9. doi:10.4161/cbt.8.15.9133
117. Liu F, Hu Z, Qiu L, Hui C, Li C, Zhong P, et al. Boosting high-intensity focused ultrasound-induced anti-tumor immunity using a sparse-scan strategy that can more effectively promote dendritic cell maturation. J Transl Med (2010) 8:7. doi:10.1186/1479-5876-8-7
118. Dalfior D, Delahunt B, Brunelli M, Parisi A, Ficarra V, Novara G, et al. Utility of racemase and other immunomarkers in the detection of adenocarcinoma in prostatic tissue damaged by high intensity focused ultrasound therapy. Pathology (2010) 42:1-5. doi:10.3109/00313020903434447
119. Zhong-Lin X, Xue-Qiang Z, Pei L, Qiang Z, Jun Z, Feng W. Activation of tumor-infiltrating antigen presenting cells by high intensity focused ultrasound ablation of human breast cancer. Ultrasound Med Biol (2009) 35(1):50-7. doi:10.1016/j.ultrasmedbio.2008.08.005
120. Zhang H, Liu L, Sharma R, Alfieri A, Saha S, Garg M, et al. High intensity focused ultrasound (HIFU)-enhanced autologous in situ vaccination for prostate cancer. Int J Radiat Oncol Biol Phys (2008) 72:S165-6. doi:10.1016/j.ijrobp.2008.06.516
121. Hu Z, Yang XY, Liu Y, Sankin GN, Pua EC, Morse MA, et al. Investigation of HIFU-induced anti-tumor immunity in a murine tumor model. J Transl Med (2007) 5:34. doi:10.1186/1479-5876-5-34
122. Zerbini A, Pilli M, Fagnoni F, Pelosi G, Pizzi MG, Schivazappa S, et al. Increased immunostimulatory activity conferred to antigen-presenting cells by exposure to antigen extract from hepatocellular carcinoma after radiofrequency thermal ablation. J Immunother (2008) 31:271-82. doi:10.1097/CJI.0b013e318160ff1c
123. ter Haar G, Rivens I, Chen L, Riddler S. High intensity focused ultrasound for the treatment of rat tumours. Phys Med Biol (1991) 36:1495-501. doi:10.1088/0031-9155/36/11/009
124. Chen L, ter Haar G, Hill CR, Eccles SA, Box G. Treatment of implanted liver tumors with focused ultrasound. Ultrasound Med Biol (1998) 24:1475-88. doi:10.1016/S0301-5629(98)00134-3