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Image-guided drug delivery with magnetic resonance guided high intensity focused ultrasound and temperature sensitive liposomes in a rabbit Vx2 tumor model
Open accessAbstract
Clinical-grade doxorubicin encapsulated low temperature sensitive liposomes (LTSLs) were combined with a clinical magnetic resonance-guided high intensity focused ultrasound (MR-HIFU) platform to investigate in vivo image-guided drug delivery. Plasma pharmacokinetics were determined in 3 rabbits. Fifteen rabbits with Vx2 tumors within superficial thigh muscle were randomly assigned into three treatment groups: 1) free doxorubicin, 2) LTSL and 3) LTSL + MR-HIFU. For the LTSL + MR-HIFU group, mild hyperthermia (40-41 °C) was applied to the tumors using an MR-HIFU system. Image-guided non-invasive hyperthermia was applied for a total of 30 min, completed within 1h after LTSL infusion. High-pressure liquid chromatography (HPLC) analysis of the harvested tumor and organ/tissue homogenates was performed to determine doxorubicin concentration. Fluorescence microscopy was performed to determine doxorubicin spatial distribution in the tumors. Sonication of Vx2 tumors resulted in accurate (mean = 40.5 ± 0.1 °C) and spatially homogenous (SD = 1.0 °C) temperature control in the target region. LTSL + MR-HIFU resulted in significantly higher tumor doxorubicin concentrations (7.6- and 3.4-fold greater compared to free doxorubicin and LTSL respectively, p<0.05, Newman-Keuls). This improved tumor concentration was achieved despite heating <25% of the tumor volume. Free doxorubicin and LTSL treatments appeared to deliver more drug in the tumor periphery as compared to the tumor core. In contrast, LTSL + MR-HIFU treatment suggested an improved distribution with doxorubicin found in both the tumor periphery and core. Doxorubicin bio-distribution in non-tumor organs/tissues was fairly similar between treatment groups. This technique has potential for clinical translation as an image-guided method to deliver drug to a solid tumor.
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“Some auxiliary means, such as topical hyperthermia, radiotherapy and high intensity focused ultrasound, etc., can also be used to enhance this effect [158–160].”
From Non-viral delivery systems for CRISPR/Cas9-based genome editing: challenges and opportunities (2018) · cites this paper as [160]
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Frazier, N., & Ghandehari, H. (2015) · Biotechnology and Bioengineering · doi:10.1002/bit.25653 · Cited by 67
“This phenomenon is likely due to the hyperthermia effects reducing the interstitial pressure while improving tumor perfusion but may also be attributed to vibrational forces from ultrasound creating better penetration (Ranjan et al., 2012).”
Backgroundde Smet, M., Hijnen, N. M., Langereis, S., Elevelt, A., Heijman, E., Dubois, L. J., Lambin, P., & Grüll, H. (2013) · Investigative Radiology · doi:10.1097/rli.0b013e3182806940 · Cited by 63
“Similar results were obtained by Ranjan et al, 26 showing an increased doxorubicin uptake in the tumor periphery as well as in the tumor core, suggesting an improved intratumoral distribution of the drug.”
ResultUltrasound-mediated drug delivery using liposomes modified with a thermosensitive polymer
Ninomiya, K., Kawabata, S., Tashita, H., & Shimizu, N. (2013) · Ultrasonics Sonochemistry · doi:10.1016/j.ultsonch.2013.07.014 · Cited by 64
MRI-Guided Focused Ultrasound as a New Method of Drug Delivery
Thanou, M., & Gedroyc, W. (2013) · Journal of Drug Delivery · doi:10.1155/2013/616197 · Cited by 55
Evidence for a new mechanism behind HIFU-triggered release from liposomes
Oerlemans, C., Deckers, R., Storm, G., Hennink, W. E., & Nijsen, J. F. W. (2013) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.03.019 · Cited by 62
“A recently developed and customized technology for triggered drug release from different DDS is high-intensity focused ultrasound (HIFU) [25–29].”
BackgroundGorbet, M.-J., & Ranjan, A. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107456 · Cited by 64
Nanobiotechnology-based delivery strategies: New frontiers in brain tumor targeted therapies
Mangraviti, A., Gullotti, D. M., Tyler, B., & Brem, H. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.03.031 · Cited by 60
Shen, W., Anastasiadis, P., Nguyen, B., Yarnell, D., Yarowsky, P., Frenkel, V., & Fishman, P. S. (2017) · Cell Transplantation · doi:10.1177/0963689717715824 · Cited by 59
“A T2-weighted scan in the region of the treatment was performed prior to the exposures for treatment planning and targeting, similar to the clinical MRgFUS systems.(26) For each treatment, exposures were carried out at a single location, where the geometric center of the focal zone was targeted at the striatum.”
MethodNanomaterial-Based Drug Delivery System Targeting Lymph Nodes
Cheng, Z., Que, H., Chen, L., Sun, Q., & Wei, X. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14071372 · Cited by 60
Bing, C., Staruch, R., Tillander, M., Köhler, M. O., Mougenot, C., Ylihautala, M., Laetsch, T. W., & Chopra, R. (2016) · International Journal of Hyperthermia · doi:10.1080/02656736.2016.1179799 · Cited by 57
VanOsdol, J., Ektate, K., Ramasamy, S., Maples, D., Collins, W., Malayer, J. R., & Ranjan, A. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.12.033 · Cited by 57
“Tissue homogenization and sample preparation for HPLC were carried out using previously published methods [7,22].”
BackgroundMethodSaravanakumar, K., Hu, X., MubarakAli, D., & Wang, M. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666190709221141 · Cited by 54
Partanen, A., Tillander, M., Yarmolenko, P., Wood, B. J., Dreher, M. R., & Köhler, M. O. (2012) · Medical Physics · doi:10.1118/1.4769116 · Cited by 53
López‐Noriega, A., Ruiz‐Hernández, E., Quinlan, E., Storm, G., Hennink, W. E., & O’Brien, F. J. (2014) · Journal of Controlled Release · doi:10.1016/j.jconrel.2014.05.043 · Cited by 53
Versatile Nanosystem-Based Cancer Theranostics: Design Inspiration and Predetermined Routing
Opoku‐Damoah, Y., Wang, R., Zhou, J., & Ding, Y. (2016) · Theranostics · doi:10.7150/thno.14860 · Cited by 53
Targeted Drug Delivery Systems: Strategies and Challenges
Pattni, B. S., & Torchilin, V. P. (2014) · Advances in delivery science and technology · doi:10.1007/978-3-319-11355-5_1 · Cited by 53
Gourevich, D., Dogadkin, O., Volovick, A., Wang, L., Gnaïm, J., Cochran, S., & Melzer, A. (2013) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.05.038 · Cited by 49
Meng, L., Deng, Z., Niu, L., Li, F., Yan, F., Wu, J., Cai, F., & Zheng, H. (2015) · Theranostics · doi:10.7150/thno.12295 · Cited by 49
“It therefore has the potential to be a noninvasive modality for clinical applications [12-17].”
BackgroundDC BeadM1™: towards an optimal transcatheter hepatic tumour therapy
Lewis, A. L., Dreher, M. R., OʼByrne, V., Grey, D., Caine, M., Dunn, A., Tang, Y., Hall, B. C., Fowers, K. D., Johnson, C. G., et al. (2015) · Journal of Materials Science Materials in Medicine · doi:10.1007/s10856-015-5629-6 · Cited by 48
Bayer, A. M., Alam, S., Mattern‐Schain, S. I., & Best, M. D. (2014) · Chemistry - A European Journal · doi:10.1002/chem.201304094 · Cited by 47
Hyperthermia as Adjunct to Intravesical Chemotherapy for Bladder Cancer
Owusu, R. A., Abern, M. R., & Inman, B. A. (2013) · BioMed Research International · doi:10.1155/2013/262313 · Cited by 48
Bing, C., Patel, P. A., Staruch, R., Shaikh, S., Nofiele, J. T., Staruch, M. W., Szczepanski, D., Williams, N. S., Laetsch, T. W., & Chopra, R. (2018) · International Journal of Hyperthermia · doi:10.1080/02656736.2018.1550815 · Cited by 46
Singh, M. P., Sethuraman, S. N., Ritchey, J. W., Fiering, S., Guha, C., Malayer, J. R., & Ranjan, A. (2019) · International Journal of Hyperthermia · doi:10.1080/02656736.2019.1663280 · Cited by 47
Metadata
- Authors
- Ranjan, A., Jacobs, G. C., Woods, D. L., Negussie, A. H., Partanen, A., Yarmolenko, P. S., Gacchina, C. E., Sharma, K. V., Frenkel, V., Wood, B. J., & Dreher, M. R.
- Affiliations
- National Institutes of Health (US)
- Catholic University of America (US)
- Corresponding author
- Dreher, Matthew R.
- Venue
- Journal of Controlled Release
- Publisher
- Elsevier BV
- Published
- 2012-03
- Volume
- 158
- Issue
- 3
- Pages
- 487-494
- ISSN
- 0168-3659 (ISSN-L)
- PMC
- PMC3319290
- OpenAlex
- W1982194007
- Cited by
- 267
- References
- 44
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 11 · 2023: 14 · 2022: 12 · 2021: 17 · 2020: 12 · 2019: 15 · 2018: 18 · 2017: 20 · 2016: 38 · 2015: 28 · 2014: 30 · 2013: 30 · 2012: 13
- FWCI
- 13.80
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Controlled Release (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Center for Interventional Oncology in the Intramural Research Program of the National Institutes of Health
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › Ultrasound and Hyperthermia Applications
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Physical Sciences › Engineering › Biomedical Engineering › Nanoplatforms for cancer theranostics
- Keywords
- image-guided drug delivery, MR-guided focused ultrasound, thermosensitive liposomes, doxorubicin, cancer hyperthermia, VX2 tumor model, plasma pharmacokinetics, drug biodistribution
- MeSH terms
- Animals, Doxorubicin, Female, Liposomes, Neoplasms, Magnetic Resonance Spectroscopy, Rabbits, Temperature, Tissue Distribution, Ultrasonography, Drug Delivery Systems, High-Intensity Focused Ultrasound Ablation
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