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SPIO-conjugated, doxorubicin-loaded microbubbles for concurrent MRI and focused-ultrasound enhanced brain-tumor drug delivery
Abstract
The blood-brain barrier (BBB) can be temporarily and locally opened by focused ultrasound (FUS) in the presence of circulating microbubbles (MBs). Currently, contrast-enhanced magnetic resonance imaging (CE-MRI) is used to monitor contrast agent leakage to verify BBB-opening and infer drug deposition. However, despite being administered concurrently, MBs, therapeutic agent, and contrast agent have distinct pharmacodynamic behaviors, thus complicating the quantification and optimization of BBB-opening and drug delivery. Here we propose multifunctional MBs loaded with therapeutic agent (doxorubicin; DOX) and conjugated with superparamagnetic iron oxide (SPIO) nanoparticles. These DOX-SPIO-MBs were designed to concurrently open the BBB and perform drug delivery upon FUS exposure, act as dual MRI and ultrasound contrast agent, and allow magnetic targeting (MT) to achieve enhanced drug delivery. We performed burst-tone FUS after injection of DOX-SPIO-MBs, followed by MT with an external magnet attached to the scalp in a rat glioma model. Animals were monitored by T2-weighted MRI and susceptibility weighted imaging and the concentration of SPIO particles was determined by spin-spin relaxivity. We found that DOX-SPIO-MBs were stable and provided significant superparamagnetic/acoustic properties for imaging. BBB-opening and drug delivery were achieved concurrently during the FUS exposure. In addition, MT increased local SPIO deposition in tumor regions by 22.4%. Our findings suggest that DOX-SPIO-MBs with FUS could be an excellent theranostic tool for future image-guided drug delivery to brain tumors.
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“SPION-labeling in combination with MRI (and recently also MPI) has been the method of choice for cell tracking [193, 255].”
From Iron oxide nanoparticles: Diagnostic, therapeutic and theranostic applications (2019) · cites this paper as [255]
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Xu, S., Yang, F., Zhou, X., Zhuang, Y., Liu, B., Mu, Y., Wang, X., Shen, H. Y., Zhi, G., & Wu, D. (2015) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.5b06594 · Cited by 51
Nanotechnologies for the study of the central nervous system
Ajetunmobi, A., Prina‐Mello, A., Volkov, Y., Corvin, A. P., & Tropea, D. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.09.004 · Cited by 47
“They concluded that their platform could improve the clinical therapeutic efficacy of chemotherapeutic agents by imageguided drug delivery for brain tumour treatment (Fan et al., 2013).”
BackgroundOlumolade, O., Wang, S., Samiotaki, G., & Konofagou, E. E. (2016) · Ultrasound in Medicine & Biology · doi:10.1016/j.ultrasmedbio.2016.05.004 · Cited by 48
Metalloporphyrins in Medicine: From History to Recent Trends
Faustova, M. R., Nikolskaya, E. D., Sokol, M. B., Chirkina, M., Petrov, R., & Yabbarov, N. G. (2020) · ACS Applied Bio Materials · doi:10.1021/acsabm.0c00941 · Cited by 47
Zhu, P., Simon, I., Kokalari, I., Kohane, D. S., & Rwei, A. Y. (2024) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2024.115275 · Cited by 45
Magnetic iron oxide nanogels for combined hyperthermia and drug delivery for cancer treatment
Patri, S. K., Thanh, N. T. K., & Kamaly, N. (2024) · Nanoscale · doi:10.1039/d4nr02058h · Cited by 49
Efficient Enhancement of Blood-Brain Barrier Permeability Using Acoustic Cluster Therapy (ACT)
Åslund, A., Snipstad, S., Healey, A., Kvåle, S., TORP, S. H., Sontum, P. C., Davies, C. D. L., & van Wamel, A. J. E. T. (2016) · Theranostics · doi:10.7150/thno.16577 · Cited by 43
Shakeri‐Zadeh, A., Khoei, S., Khoee, S., Sharifi, A. M., & Shiran, M. B. (2014) · Journal of Medical Ultrasonics · doi:10.1007/s10396-014-0558-4 · Cited by 43
Song, W., Luo, Y., Zhao, Y., Liu, X., Zhao, J., Luo, J., Zhang, Q., Ran, H., Wang, Z., & Guo, D. (2017) · Nanomedicine · doi:10.2217/nnm-2017-0027 · Cited by 43
Guigou, C., Lalande, A., Millot, N., Belharet, K., & Grayeli, A. B. (2021) · Brain Sciences · doi:10.3390/brainsci11030358 · Cited by 45
“The use of an EMF made it possible to draw SPIONS through the BBB [42,43,47,49, 57,60,61,73,76,78,81,83,94,113,119,120,128,133,134].”
MethodAbdalkader, R., Kawakami, S., Unga, J., Suzuki, R., Maruyama, K., Yamashita, F., & Hashida, M. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.03.014 · Cited by 42
“Many studies have reported on the different methods by which doxorubicin or paclitaxel was successfully prepared and tested for tumor therapy in combination with US irradiation [10,24,25].”
BackgroundThe detection of β-amyloid plaques in an Alzheimer's disease rat model with DDNP-SPIO
Zhang, D., Fa, H., Zhou, J., Li, S., Diao, X.-W., & Yin, W. H. (2014) · Clinical Radiology · doi:10.1016/j.crad.2014.09.019 · Cited by 43
Optimized shapes of magnetic arrays for drug targeting applications
Barnsley, L. C., Carugo, D., & Stride, E. (2016) · Journal of Physics D Applied Physics · doi:10.1088/0022-3727/49/22/225501 · Cited by 40
“A design volume was set up to optim ize a Halbach array of orthogonally magnetized segments to target and retain magnetic microparticles in the vessel network around the brain at a depth of 50 mm, which has a range of possible applications (for example, magnetic microbubbles can be used for localized opening of the bl…”
BackgroundMethodMagnetic Particle Imaging in Neurosurgery
Meola, A., Rao, J., Chaudhary, N., Song, G., Zheng, X., & Chang, S. D. (2019) · World Neurosurgery · doi:10.1016/j.wneu.2019.01.180 · Cited by 40
Metadata
- Authors
- Fan, C.-H., Ting, C.-Y., Lin, H.-J., Wang, C.-H., Liu, H.-L., Yen, T.-C., & Yeh, C.-K.
- Affiliations
- National Tsing Hua University (TW)
- Chang Gung University (TW)
- Corresponding author
- Liu, Hao-Li
- Yeh, Chih-Kuang
- Venue
- Biomaterials
- Publisher
- Elsevier BV
- Published
- 2013-05
- Volume
- 34
- Issue
- 14
- Pages
- 3706-3715
- ISSN
- 0142-9612 (ISSN-L)
- OpenAlex
- W2067444098
- Cited by
- 225
- References
- 36
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 7 · 2023: 9 · 2022: 13 · 2021: 17 · 2020: 11 · 2019: 25 · 2018: 18 · 2017: 24 · 2016: 24 · 2015: 26 · 2014: 26 · 2013: 9
- FWCI
- 15.64
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biomaterials (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Council of Taiwan (100-2218-E-182-001, 101-2627-M-007-001, 101-2221-E-007-035-MY3)
- National Tsing Hua University (102N2050E1)
- Taiwan National Health Research Institutes (NM-101-PP-04)
- Materials Analysis Technology Inc. Corporation
- 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
- superparamagnetic iron oxide nanoparticles, microbubbles, doxorubicin, focused ultrasound, blood-brain barrier opening, brain tumor drug delivery, magnetic targeting, theranostics, image-guided drug delivery, glioma, MRI contrast agents, ultrasound contrast agents, susceptibility-weighted imaging
- MeSH terms
- Animals, Brain Neoplasms, Doxorubicin, Ferric Compounds, Magnetic Resonance Imaging, Male, Drug Delivery Systems, Rats, Sprague-Dawley, Microbubbles, Cell Line, Tumor, Rats
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