The DOI matches its Crossref record; 54 of the 54 references it cites were found in a registry or an index.
Duality of Iron Oxide Nanoparticles in Cancer Therapy: Amplification of Heating Efficiency by Magnetic Hyperthermia and Photothermal Bimodal Treatment
Abstract
The pursuit of innovative, multifunctional, more efficient, and safer treatments is a major challenge in preclinical nanoparticle-mediated thermotherapeutic research. Here, we report that iron oxide nanoparticles have the dual capacity to act as both magnetic and photothermal agents. We further explore every key aspect of this magnetophotothermal approach, choosing iron oxide nanocubes for their high efficiency for the magnetic hyperthermia modality itself. In aqueous suspension, the nanocubes' exposure to both: an alternating magnetic field and near-infrared laser irradiation (808 nm), defined as the DUAL-mode, amplifies the heating effect 2- to 5-fold by comparison with magnetic stimulation alone, yielding unprecedented heating powers (specific loss powers) up to 5000 W/g. In cancer cells, the laser excitation restores the optimal efficiency of magnetic hyperthermia, otherwise inhibited by intracellular confinement, resulting in a remarkable heating efficiency in the DUAL-mode (up to 15-fold amplification), with respect to the magnetophotothermal mode. As a consequence, the dual action yielded complete apoptosis-mediated cell death. In solid tumors in vivo, single-mode treatments (magnetic or laser hyperthermia) reduced tumor growth, while DUAL-mode treatment resulted in complete tumor regression, mediated by heat-induced tumoral cell apoptosis and massive denaturation of the collagen fibers, and a long-lasting thermal efficiency over repeated treatments.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Cancer Cell Imaging and Photothermal Therapy in the Near-Infrared Region by Using Gold Nanorods
Huang, X., El-Sayed, I. H., Qian, W., & El-Sayed, M. A. (2006) · Journal of the American Chemical Society · doi:10.1021/ja057254a · Cited by 5,436
Preparation and Growth Mechanism of Gold Nanorods (NRs) Using Seed-Mediated Growth Method
Nikoobakht, B., & El-Sayed, M. A. (2003) · Chemistry of Materials · doi:10.1021/cm020732l · Cited by 5,069
Jain, P. K., Huang, X., El-Sayed, I. H., & El-Sayed, M. A. (2008) · Accounts of Chemical Research · doi:10.1021/ar7002804 · Cited by 4,215
Graphene in Mice: Ultrahigh In Vivo Tumor Uptake and Efficient Photothermal Therapy
Yang, K., Zhang, S., Zhang, G., Sun, X., Lee, S.-T., & Liu, Z. (2010) · Nano Letters · doi:10.1021/nl100996u · Cited by 2,407
Reddy, L. H., Arias, J. L., Nicolas, J., & Couvreur, P. (2012) · Chemical Reviews · doi:10.1021/cr300068p · Cited by 2,010
Immunotargeted Nanoshells for Integrated Cancer Imaging and Therapy
Loo, C., Lowery, A., Halas, N., West, J., & Drezek, R. (2005) · Nano Letters · doi:10.1021/nl050127s · Cited by 1,792
Jordan, A., Scholz, R., Wust, P., Fähling, H., & Felix, R. (1999) · Journal of Magnetism and Magnetic Materials · doi:10.1016/s0304-8853(99)00088-8 · Cited by 1,494
In vivo biodistribution and highly efficient tumour targeting of carbon nanotubes in mice
Liu, Z., Cai, W., He, L., Nakayama, N., Chen, K., Sun, X., Chen, X., & Dai, H. (2007) · Nature Nanotechnology · doi:10.1038/nnano.2006.170 · Cited by 1,436
Maier-Hauff, K., Ulrich, F., Nestler, D., Niehoff, H., Wust, P., Thiesen, B., Orawa, H., Budach, V., & Jordan, A. (2011) · Journal of Neuro-Oncology · doi:10.1007/s11060-010-0389-0 · Cited by 1,429
Gold nanocages covered by smart polymers for controlled release with near-infrared light
Yavuz, M. S., Cheng, Y., Chen, J., Cobley, C. M., Zhang, Q., Rycenga, M., Xie, J., Kim, C., Song, K. H., Schwartz, A. G., et al. (2009) · Nature Materials · doi:10.1038/nmat2564 · Cited by 1,405
Exchange-coupled magnetic nanoparticles for efficient heat induction
Lee, J.-H., Jang, J.-T., Choi, J.-S., Moon, S. H., Noh, S.-H., Kim, J.-W., Kim, J.-G., Kim, I.-S., Park, K. I., & Cheon, J. (2011) · Nature Nanotechnology · doi:10.1038/nnano.2011.95 · Cited by 1,364
In vivo Biodistribution and Highly Efficient Tumour Targeting of Carbon Nanotubes in Mice
Liu, Z., Cai, W., He, L., Nakayama, N., Chen, K., Sun, X., Chen, X., & Dai, H. (2020) · Nano-Enabled Medical Applications · doi:10.1201/9780429399039-14 · Cited by 1,213
Magnetic particle hyperthermia—biophysical limitations of a visionary tumour therapy
Hergt, R., & Dutz, S. (2007) · Journal of Magnetism and Magnetic Materials · doi:10.1016/j.jmmm.2006.10.1156 · Cited by 922
Theranostic Nanoshells: From Probe Design to Imaging and Treatment of Cancer
Bardhan, R., Lal, S., Joshi, A., & Halas, N. J. (2011) · Accounts of Chemical Research · doi:10.1021/ar200023x · Cited by 917
Donaldson, K., Murphy, F. A., Duffin, R., & Poland, C. A. (2010) · Particle and Fibre Toxicology · doi:10.1186/1743-8977-7-5 · Cited by 916
A New Era for Cancer Treatment: Gold‐Nanoparticle‐Mediated Thermal Therapies
Kennedy, L. C., Bickford, L. R., Lewinski, N. A., Coughlin, A. J., Hu, Y., Day, E. S., West, J. L., & Drezek, R. A. (2011) · Small · doi:10.1002/smll.201000134 · Cited by 885
Targeting Strategies for Multifunctional Nanoparticles in Cancer Imaging and Therapy
Yu, M. K., Park, J., & Jon, S. (2012) · Theranostics · doi:10.7150/thno.3463 · Cited by 883
In Vivo Near-Infrared Mediated Tumor Destruction by Photothermal Effect of Carbon Nanotubes
Moon, H. K., Lee, S. H., & Choi, H. C. (2009) · ACS Nano · doi:10.1021/nn900904h · Cited by 797
Guardia, P., Di Corato, R., Lartigue, L., Wilhelm, C., Espinosa, A., Garcia-Hernandez, M., Gazeau, F., Manna, L., & Pellegrino, T. (2012) · ACS Nano · doi:10.1021/nn2048137 · Cited by 752
Self-citationZhou, M., Zhang, R., Huang, M., Lu, W., Song, S., Melancon, M. P., Tian, M., Liang, D., & Li, C. (2010) · Journal of the American Chemical Society · doi:10.1021/ja106855m · Cited by 718
Martinez-Boubeta, C., Simeonidis, K., Makridis, A., Angelakeris, M., Iglesias, O., Guardia, P., Cabot, A., Yedra, L., Estradé, S., Peiró, F., et al. (2013) · Scientific Reports · doi:10.1038/srep01652 · Cited by 539
Johannsen, M., Gneveckow, U., Thiesen, B., Taymoorian, K., Cho, C. H., Waldöfner, N., Scholz, R., Jordan, A., Loening, S. A., & Wust, P. (2007) · European Urology · doi:10.1016/j.eururo.2006.11.023 · Cited by 532
Soenen, S. J., Parak, W. J., Rejman, J., & Manshian, B. (2015) · Chemical Reviews · doi:10.1021/cr400714j · Cited by 515
A Review of Clinical Translation of Inorganic Nanoparticles
Anselmo, A. C., & Mitragotri, S. (2015) · The AAPS Journal · doi:10.1208/s12248-015-9780-2 · Cited by 509
American National Standard for the Safe Use of Lasers.
(1975) · Annals of Internal Medicine · doi:10.7326/0003-4819-82-1-132_2 · Cited by 498
Magnetic nanoparticle hyperthermia for prostate cancer
Johannsen, M., Thiesen, B., Wust, P., & Jordan, A. (2010) · International Journal of Hyperthermia · doi:10.3109/02656731003745740 · Cited by 469
Chu, M., Shao, Y., Peng, J., Dai, X., Li, H., Wu, Q., & Shi, D. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.01.086 · Cited by 451
Lartigue, L., Hugounenq, P., Alloyeau, D., Clarke, S. P., Lévy, M., Bacri, J.-C., Bazzi, R., Brougham, D. F., Wilhelm, C., & Gazeau, F. (2012) · ACS Nano · doi:10.1021/nn304477s · Cited by 421
Self-citationA smart and versatile theranostic nanomedicine platform based on nanoporphyrin
Li, Y., Lin, T.-Y., Luo, Y., Liu, Q., Xiao, W., Guo, W., Lac, D., Zhang, H., Feng, C., Wachsmann-Hogiu, S., et al. (2014) · Nature Communications · doi:10.1038/ncomms5712 · Cited by 414
Magnetic hyperthermia efficiency in the cellular environment for different nanoparticle designs
Di Corato, R., Espinosa, A., Lartigue, L., Tharaud, M., Chat, S., Pellegrino, T., Ménager, C., Gazeau, F., & Wilhelm, C. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.04.036 · Cited by 412
Self-citationMagnetite Fe3O4Nanocrystals: Spectroscopic Observation of Aqueous Oxidation Kinetics
Tang, J., Myers, M., Bosnick, K. A., & Brus, L. E. (2003) · The Journal of Physical Chemistry B · doi:10.1021/jp027048e · Cited by 389
Martinez-Boubeta, C., Simeonidis, K., Makridis, A., Angelakeris, M., Iglesias, Ò., Guardia, P., Cabot, A., Yedra, L., Estradé, S., Peiró, F., et al. (2013) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) · Cited by 381
Long term in vivo biotransformation of iron oxide nanoparticles
Levy, M., Luciani, N., Alloyeau, D., Elgrabli, D., Deveaux, V., Pechoux, C., Chat, S., Wang, G., Vats, N., Gendron, F., et al. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.02.031 · Cited by 361
Self-citationSize and structure effect on optical transitions of iron oxide nanocrystals
He, Y. P., Miao, Y. M., Li, C. R., Wang, S. Q., Cao, L., Xie, S. S., Yang, G. Z., Zou, B. S., & Burda, C. (2005) · Physical Review B · doi:10.1103/physrevb.71.125411 · Cited by 345
He, R., Wang, Y.-C., Wang, X., Wang, Z., Liu, G., Zhou, W., Wen, L., Li, Q., Wang, X., Chen, X., et al. (2014) · Nature Communications · doi:10.1038/ncomms5327 · Cited by 344
Di Corato, R., Béalle, G., Kolosnjaj-Tabi, J., Espinosa, A., Clément, O., Silva, A. K. A., Ménager, C., & Wilhelm, C. (2015) · ACS Nano · doi:10.1021/nn506949t · Cited by 339
Self-citationBoca, S. C., Potara, M., Gabudean, A.-M., Juhem, A., Baldeck, P. L., & Astilean, S. (2011) · Cancer Letters · doi:10.1016/j.canlet.2011.06.022 · Cited by 325
Magnetic nanoparticle clusters for photothermal therapy with near-infrared irradiation
Shen, S., Wang, S., Zheng, R., Zhu, X., Jiang, X., Fu, D., & Yang, W. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2014.10.064 · Cited by 315
Zhou, Z., Sun, Y., Shen, J., Wei, J., Yu, C., Kong, B., Liu, W., Yang, H., Yang, S., & Wang, W. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.04.063 · Cited by 305
Biodegradation of Iron Oxide Nanocubes: High-Resolution In Situ Monitoring
Lartigue, L., Alloyeau, D., Kolosnjaj-Tabi, J., Javed, Y., Guardia, P., Riedinger, A., Péchoux, C., Pellegrino, T., Wilhelm, C., & Gazeau, F. (2013) · ACS Nano · doi:10.1021/nn305719y · Cited by 274
Self-citationHeat-Generating Iron Oxide Nanocubes: Subtle “Destructurators” of the Tumoral Microenvironment
Kolosnjaj-Tabi, J., Di Corato, R., Lartigue, L., Marangon, I., Guardia, P., Silva, A. K. A., Luciani, N., Clément, O., Flaud, P., Singh, J. V., et al. (2014) · ACS Nano · doi:10.1021/nn405356r · Cited by 232
Self-citationShen, S., Kong, F., Guo, X., Wu, L., Shen, H., Xie, M., Wang, X., Jin, Y., & Ge, Y. (2013) · Nanoscale · doi:10.1039/c3nr01447a · Cited by 173
Guardia, P., Riedinger, A., Nitti, S., Pugliese, G., Marras, S., Genovese, A., Materia, M. E., Lefevre, C., Manna, L., & Pellegrino, T. (2014) · Journal of Materials Chemistry B · doi:10.1039/c4tb00061g · Cited by 168
Self-citationIn Situ Measurement of Magnetization Relaxation of Internalized Nanoparticles in Live Cells
Soukup, D., Moise, S., Céspedes, E., Dobson, J., & Telling, N. D. (2015) · ACS Nano · doi:10.1021/nn503888j · Cited by 158
Photothermal cancer therapy via femtosecond-laser-excited FePt nanoparticles
Chen, C., Kuo, L.-R., Lee, S., Yeu-Kuang, H., Chou, S., Chen, C., Chang, F., Lin, K., Tsai, D.-H., & Chen, Y.-Y. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.10.044 · Cited by 141
Pasparakis, G., Manouras, T., Vamvakaki, M., & Argitis, P. (2014) · Nature Communications · doi:10.1038/ncomms4623 · Cited by 138
Chen, H., Burnett, J., Zhang, F., Zhang, J., Paholak, H. J., & Sun, D. (2013) · Journal of Materials Chemistry B · doi:10.1039/c3tb21338b · Cited by 133
Can magneto-plasmonic nanohybrids efficiently combine photothermia with magnetic hyperthermia?
Espinosa, A., Bugnet, M., Radtke, G., Neveu, S., Botton, G. A., Wilhelm, C., & Abou‐Hassan, A. (2015) · Nanoscale · doi:10.1039/c5nr06168g · Cited by 130
Self-citationWang, Y.-H., Chen, S., Liao, A., et al. (2014) · Scientific Reports · doi:10.1038/srep05685 · Cited by 67
Abdulla‐Al‐Mamun, M., Kusumoto, Y., Zannat, T., Horie, Y., & Manaka, H. (2013) · RSC Advances · doi:10.1039/c3ra21479f · Cited by 58
Photothermal Microscopy of the Core of Dextran-Coated Iron Oxide Nanoparticles During Cell Uptake
Bogart, L. K., Taylor, A., Cesbron, Y., et al. (2012) · ACS Nano · doi:10.1021/nn300868z · Cited by 57
Quarta, A., Bernareggi, D., Benigni, F., Luison, E., Nano, G., Nitti, S., Cesta, M. C., Ciccio, L. D., Canevari, S., Pellegrino, T., et al. (2014) · Nanoscale · doi:10.1039/c4nr04426f · Cited by 33
Self-citationDouble thermal transitions of type I collagen in acidic solution
Liu, Y., Liu, L., Chen, M., & Zhang, Q. (2012) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2012.715042 · Cited by 25
Sivakumar, B., Girija, A. R., Nagaoka, Y., Fukuda, T., Iwai, S., Venugopal, K., Kato, K., Maekawa, T., & Nair, S. D. (2015) · RSC Advances · doi:10.1039/c5ra00168d · Cited by 15
Cited by
Inorganic nanomaterials with rapid clearance for biomedical applications
Wang, X., Zhong, X., Li, J., Liu, Z., & Cheng, L. (2021) · Chemical Society Reviews · doi:10.1039/d0cs00461h · Cited by 509
Recent Advances in Cell Membrane–Camouflaged Nanoparticles for Cancer Phototherapy
Zhen, X., Cheng, P., & Pu, K. (2019) · Small · doi:10.1002/smll.201804105 · Cited by 483
Versatile Types of Organic/Inorganic Nanohybrids: From Strategic Design to Biomedical Applications
Zhao, N., Yan, L., Zhao, X., Chen, X., Li, A., Zheng, D., Zhou, X., Dai, X., & Xu, F.-J. (2019) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00401 · Cited by 429
Inorganic nanoparticles: A potential cancer therapy for human welfare
Pugazhendhi, A., Edison, T. N. J. I., Karuppusamy, I., & Kathirvel, B. (2018) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2018.01.034 · Cited by 325
Recent advances and future prospects of iron oxide nanoparticles in biomedicine and diagnostics
Vallabani, N. V. S., & Singh, S. (2018) · 3 Biotech · doi:10.1007/s13205-018-1286-z · Cited by 322
Metadata
- Authors
- Espinosa, A., Di Corato, R., Kolosnjaj-Tabi, J., Flaud, P., Pellegrino, T., & Wilhelm, C.
- Venue
- ACS Nano
- Publisher
- American Chemical Society (ACS)
- Published
- 2016-01-20
- Volume
- 10
- Issue
- 2
- Pages
- 2436-2446
- ISSN
- 1936-0851 (ISSN-L)
- 1936-086X
- OpenAlex
- W2291888828
- Cited by
- 788
- References
- 54
- FWCI
- 43.62
- Type
- journal article
- Language
- en
- Open access
- closed
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.
