Recent Advances in Multimodal Molecular Imaging of Cancer Mediated by Hybrid Magnetic Nanoparticles
Abstract
:1. Introduction
2. Magnetic Nanoparticles as Molecular Imaging Agents in Magnetic Resonance Imaging
2.1. Characteristics of Magnetic Nanoparticles Impacting T1 and T2 MRI Signals
2.2. T1–T2 Dual-Mode MRI Contrast Agents
2.3. Applications of MRI Nanomaterials in Cancer Diagnosis
2.3.1. MRI Nanomaterials as T2 Contrast Agents in Cancer Imaging
2.3.2. MRI Nanomaterials as T1 Contrast Agents in Cancer Imaging
2.3.3. MRI Nanomaterials as T1–T2 Contrast Agents in Cancer Imaging
3. Hybrid Magnetic Nanoparticles as MRI–Optical Dual-Mode Imaging Agents for Cancer Diagnosis
4. Hybrid Magnetic Nanoparticles for MRI Radiation-Based Dual-Mode Imaging for Cancer Diagnosis
4.1. MRI–PET/SPECT Dual Imaging
4.1.1. MRI–PET Dual Imaging in Cancer Diagnosis
4.1.2. MRI–SPECT Dual Imaging for Cancer Diagnosis
4.2. MRI–CT Dual Imaging in Cancer Diagnosis
5. Magnetic Nanoparticle-Based Non-Traditional Multimodal Imaging for Cancer Diagnosis
5.1. Magnetic Particle Imaging (MPI)
5.2. MNP-Assisted Multimodal Ultrasound Imaging
5.2.1. Magneto-Motive Ultrasound Imaging (MMUI)
5.2.2. Magneto Photoacoustic Imaging (MPA)
6. General Remarks and Future Perspectives
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- World Health Organization. All Cancers Fact Sheet. 2018. Available online: https://www.who.int/news-room/fact-sheets/detail/cancer (accessed on 4 February 2021).
- Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kumari, P.; Ghosh, B.; Biswas, S. Nanocarriers for cancer-targeted drug delivery. J. Drug Target. 2016, 24, 179–191. [Google Scholar] [CrossRef] [PubMed]
- Alavi, M.; Hamidi, M. Passive and active targeting in cancer therapy by liposomes and lipid nanoparticles. Drug Metab. Pers. Ther. 2019, 34. [Google Scholar] [CrossRef] [PubMed]
- Raza, F.; Zafar, H.; You, X.; Khan, A.; Wu, J.; Ge, L. Cancer nanomedicine: Focus on recent developments and self-assembled peptide nanocarriers. J. Mater. Chem. B 2019, 7, 7639–7655. [Google Scholar] [CrossRef]
- Zafar, H.; Raza, F.; Ma, S.; Wei, Y.; Zhang, J.; Shen, Q. Recent progress on nanomedicine-induced ferroptosis for cancer therapy. Biomater. Sci. 2021, 9, 5092–5115. [Google Scholar] [CrossRef]
- Massoud, T.F.; Gambhir, S.S. Molecular imaging in living subjects: Seeing fundamental biological processes in a new light. Genes Dev. 2003, 17, 545–580. [Google Scholar] [CrossRef] [Green Version]
- James, M.L.; Gambhir, S.S. A molecular imaging primer: Modalities, imaging agents, and applications. Physiol. Rev. 2012, 92, 897–965. [Google Scholar] [CrossRef] [Green Version]
- Anderson, C.J.; Lewis, J.S. Current status and future challenges for molecular imaging. Philos. Trans. A Math. Phys. Eng. Sci. 2017, 375, 20170023. [Google Scholar] [CrossRef]
- Key, J.; Leary, J.F. Nanoparticles for multimodal in vivo imaging in nanomedicine. Int. J. Nanomed. 2014, 9, 711–726. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.; Lee, N.; Hyeon, T. Recent development of nanoparticles for molecular imaging. Philos. Trans. A Math. Phys. Eng. Sci. 2017, 375, 20170022. [Google Scholar] [CrossRef]
- Martínez-Rodríguez, I.; Banzo, I. Advances in PET: The success of multimodal molecular imaging. Med. Clínica 2017, 148, 354–356. [Google Scholar] [CrossRef]
- Wu, M.; Shu, J. Multimodal Molecular Imaging: Current Status and Future Directions. Contrast Media Mol. Imaging 2018, 2018, 1382183. [Google Scholar] [CrossRef] [Green Version]
- Zlitni, A.; Gambhir, S.S. Molecular imaging agents for ultrasound. Curr. Opin. Chem. Biol. 2018, 45, 113–120. [Google Scholar] [CrossRef] [Green Version]
- Luengo Morato, Y.; Marciello, M.; Lozano Chamizo, L.; Ovejero Paredes, K.; Filice, M. 14-Hybrid magnetic nanoparticles for multimodal molecular imaging of cancer. In Magnetic Nanoparticle-Based Hybrid Materials; Ehrmann, A., Nguyen, T.A., Ahmadi, M., Farmani, A., Nguyen-Tri, P., Eds.; Woodhead Publishing: Sawston, UK, 2021; pp. 343–386. [Google Scholar] [CrossRef]
- Heo, S.H.; Kim, J.W.; Shin, S.S.; Jeong, Y.Y.; Kang, H.K. Multimodal imaging evaluation in staging of rectal cancer. World J. Gastroenterol. 2014, 20, 4244–4255. [Google Scholar] [CrossRef]
- Wang, Y.; Kang, S.; Doerksen, J.D.; Glaser, A.K.; Liu, J.T. Surgical Guidance via Multiplexed Molecular Imaging of Fresh Tissues Labeled with SERS-Coded Nanoparticles. IEEE J. Sel. Top. Quantum Electron. 2016, 22, 154–164. [Google Scholar] [CrossRef] [Green Version]
- Shin, T.-H.; Choi, Y.; Kim, S.; Cheon, J. Recent advances in magnetic nanoparticle-based multi-modal imaging. Chem. Soc. Rev. 2015, 44, 4501–4516. [Google Scholar] [CrossRef]
- Liu, M.; Anderson, R.C.; Lan, X.; Conti, P.S.; Chen, K. Recent advances in the development of nanoparticles for multimodality imaging and therapy of cancer. Med. Res. Rev. 2020, 40, 909–930. [Google Scholar] [CrossRef]
- Ovejero Paredes, K.; Díaz-García, D.; García-Almodóvar, V.; Lozano Chamizo, L.; Marciello, M.; Díaz-Sánchez, M.; Prashar, S.; Gómez-Ruiz, S.; Filice, M. Multifunctional Silica-Based Nanoparticles with Controlled Release of Organotin Metallodrug for Targeted Theranosis of Breast Cancer. Cancers 2020, 12, 187. [Google Scholar] [CrossRef] [Green Version]
- Filice, M.; Ruiz-Cabello, J. Nucleic Acid Nanotheranostics: Biomedical Applications; Elsevier: Amsterdam, The Netherlands, 2019. [Google Scholar]
- Marciello, M.; Pellico, J.; Fernandez-Barahona, I.; Herranz, F.; Ruiz-Cabello, J.; Filice, M. Recent advances in the preparation and application of multifunctional iron oxide and liposome-based nanosystems for multimodal diagnosis and therapy. Interface Focus 2016, 6, 20160055. [Google Scholar] [CrossRef]
- Kim, D.; Kim, J.; Park, Y.I.; Lee, N.; Hyeon, T. Recent Development of Inorganic Nanoparticles for Biomedical Imaging. ACS Cent. Sci. 2018, 4, 324–336. [Google Scholar] [CrossRef] [Green Version]
- Siddique, S.; Chow, J.C.L. Application of Nanomaterials in Biomedical Imaging and Cancer Therapy. Nanomaterials 2020, 10, 1700. [Google Scholar] [CrossRef]
- Marciello, M.; Luengo, Y.; Morales, M.P. Iron Oxide Nanoparticles for Cancer Diagnosis and Therapy. In Nanoarchitectonics for Smart Delivery and Drug Targeting; William Andrew: Norwich, NY, USA, 2016; pp. 667–694. [Google Scholar] [CrossRef]
- Lee, N.; Yoo, D.; Ling, D.; Cho, M.H.; Hyeon, T.; Cheon, J. Iron Oxide Based Nanoparticles for Multimodal Imaging and Magnetoresponsive Therapy. Chem. Rev. 2015, 115, 10637–10689. [Google Scholar] [CrossRef]
- Burke, B.P.; Cawthorne, C.; Archibald, S.J. Multimodal nanoparticle imaging agents: Design and applications. Philos Trans. A Math. Phys. Eng. Sci 2017, 375, 20170261. [Google Scholar] [CrossRef]
- McDougald, W.A.; Collins, R.; Green, M.; Tavares, A.A.S. High Dose MicroCT Does Not Contribute Toward Improved MicroPET/CT Image Quantitative Accuracy and Can Limit Longitudinal Scanning of Small Animals. Front. Phys. 2017, 5, 50. [Google Scholar] [CrossRef]
- Kalyane, D.; Raval, N.; Maheshwari, R.; Tambe, V.; Kalia, K.; Tekade, R.K. Employment of enhanced permeability and retention effect (EPR): Nanoparticle-based precision tools for targeting of therapeutic and diagnostic agent in cancer. Mater. Sci. Eng. C Mater. Biol. Appl. 2019, 98, 1252–1276. [Google Scholar] [CrossRef]
- Perez-Herrero, E.; Fernandez-Medarde, A. Advanced targeted therapies in cancer: Drug nanocarriers, the future of chemotherapy. Eur. J. Pharm. Biopharm. 2015, 93, 52–79. [Google Scholar] [CrossRef] [Green Version]
- Attia, M.F.; Anton, N.; Wallyn, J.; Omran, Z.; Vandamme, T.F. An overview of active and passive targeting strategies to improve the nanocarriers efficiency to tumour sites. J. Pharm. Pharmacol. 2019, 71, 1185–1198. [Google Scholar] [CrossRef] [Green Version]
- Siemann, D.W. The unique characteristics of tumor vasculature and preclinical evidence for its selective disruption by Tumor-Vascular Disrupting Agents. Cancer Treat. Rev. 2011, 37, 63–74. [Google Scholar] [CrossRef] [Green Version]
- Park, J.; Choi, Y.; Chang, H.; Um, W.; Ryu, J.H.; Kwon, I.C. Alliance with EPR Effect: Combined Strategies to Improve the EPR Effect in the Tumor Microenvironment. Theranostics 2019, 9, 8073–8090. [Google Scholar] [CrossRef]
- Branca, M.; Marciello, M.; Ciuculescu-Pradines, D.; Respaud, M.; del Puerto Morales, M.; Serra, R.; Casanove, M.-J.; Amiens, C. Towards MRI T2 contrast agents of increased efficiency. J. Magn. Magn. Mater. 2015, 377, 348–353. [Google Scholar] [CrossRef]
- Zahraei, M.; Marciello, M.; Lazaro-Carrillo, A.; Villanueva, A.; Herranz, F.; Talelli, M.; Costo, R.; Monshi, A.; Shahbazi-Gahrouei, D.; Amirnasr, M.; et al. Versatile theranostics agents designed by coating ferrite nanoparticles with biocompatible polymers. Nanotechnology 2016, 27, 255702. [Google Scholar] [CrossRef] [PubMed]
- Fatima, H.; Kim, K.-S. Iron-based magnetic nanoparticles for magnetic resonance imaging. Adv. Powder Technol. 2018, 29, 2678–2685. [Google Scholar] [CrossRef]
- Bakhtiary, Z.; Saei, A.A.; Hajipour, M.J.; Raoufi, M.; Vermesh, O.; Mahmoudi, M. Targeted superparamagnetic iron oxide nanoparticles for early detection of cancer: Possibilities and challenges. Nanomed. Nanotechnol. Biol. Med. 2016, 12, 287–307. [Google Scholar] [CrossRef] [PubMed]
- Mehrabian, H.; Detsky, J.; Soliman, H.; Sahgal, A.; Stanisz, G.J. Advanced Magnetic Resonance Imaging Techniques in Management of Brain Metastases. Front. Oncol. 2019, 9, 440. [Google Scholar] [CrossRef] [PubMed]
- Stabile, A.; Giganti, F.; Rosenkrantz, A.B.; Taneja, S.S.; Villeirs, G.; Gill, I.S.; Allen, C.; Emberton, M.; Moore, C.M.; Kasivisvanathan, V. Multiparametric MRI for prostate cancer diagnosis: Current status and future directions. Nat. Rev. Urol. 2020, 17, 41–61. [Google Scholar] [CrossRef]
- Lee, N.; Hyeon, T. Magnetic Nanoparticles for Magnetic Resonance Imaging Contrast Agents. In Magnetic Nanoparticles in Biosensing and Medicine; Ionescu, A., Llandro, J., Darton, N.J., Eds.; Cambridge University Press: Cambridge, UK, 2019; pp. 228–250. [Google Scholar] [CrossRef]
- Zhang, W.; Liu, L.; Chen, H.; Hu, K.; Delahunty, I.; Gao, S.; Xie, J. Surface impact on nanoparticle-based magnetic resonance imaging contrast agents. Theranostics 2018, 8, 2521–2548. [Google Scholar] [CrossRef]
- Bao, Y.; Sherwood, J.A.; Sun, Z. Magnetic iron oxide nanoparticles as T1 contrast agents for magnetic resonance imaging. J. Mater. Chem. C 2018, 6, 1280–1290. [Google Scholar] [CrossRef]
- Wei, H.; Bruns, O.T.; Kaul, M.G.; Hansen, E.C.; Barch, M.; Wiśniowska, A.; Chen, O.; Chen, Y.; Li, N.; Okada, S.; et al. Exceedingly small iron oxide nanoparticles as positive MRI contrast agents. Proc. Natl. Acad. Sci. USA 2017, 114, 2325–2330. [Google Scholar] [CrossRef] [Green Version]
- Avasthi, A.; Caro, C.; Pozo-Torres, E.; Leal, M.P.; García-Martín, M.L. Magnetic Nanoparticles as MRI Contrast Agents. Top. Curr. Chem. 2020, 378, 40. [Google Scholar] [CrossRef]
- Zhou, Z.; Yang, L.; Gao, J.; Chen, X. Structure–Relaxivity Relationships of Magnetic Nanoparticles for Magnetic Resonance Imaging. Adv. Mater. 2019, 31, 1804567. [Google Scholar] [CrossRef]
- Lu, Y.; Xu, Y.J.; Zhang, G.B.; Ling, D.; Wang, M.Q.; Zhou, Y.; Wu, Y.D.; Wu, T.; Hackett, M.J.; Kim, B.H.; et al. Iron oxide nanoclusters for T 1 magnetic resonance imaging of non-human primates article. Nat. Biomed. Eng. 2017, 1, 637–643. [Google Scholar] [CrossRef]
- Macher, T.; Totenhagen, J.; Sherwood, J.; Qin, Y.; Gurler, D.; Bolding, M.S.; Bao, Y. Ultrathin Iron Oxide Nanowhiskers as Positive Contrast Agents for Magnetic Resonance Imaging. Adv. Funct. Mater. 2015, 25, 490–494. [Google Scholar] [CrossRef]
- Javed, Y.; Akhtar, K.; Anwar, H.; Jamil, Y. MRI based on iron oxide nanoparticles contrast agents: Effect of oxidation state and architecture. J. Nanoparticle Res. 2017, 19, 366. [Google Scholar] [CrossRef]
- Estelrich, J.; Sánchez-Martín, M.J.; Busquets, M.A. Nanoparticles in magnetic resonance imaging: From simple to dual contrast agents. Int. J. Nanomed. 2015, 10, 1727–1741. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Z.; Bai, R.; Munasinghe, J.; Shen, Z.; Nie, L.; Chen, X. T1–T2 Dual-Modal Magnetic Resonance Imaging: From Molecular Basis to Contrast Agents. ACS Nano 2017, 11, 5227–5232. [Google Scholar] [CrossRef]
- Miao, Y.; Chen, P.; Yan, M.; Xiao, J.; Hong, B.; Zhou, K.; Zhang, G.; Qian, J.; Wu, Z. Highly sensitive T1-T2dual-mode MRI probe based on ultra-small gadolinium oxide-decorated iron oxide nanocrystals. Biomed. Mater. 2021, 16, 044104. [Google Scholar] [CrossRef]
- Gao, L.; Yu, J.; Liu, Y.; Zhou, J.; Sun, L.; Wang, J.; Zhu, J.; Peng, H.; Lu, W.; Yu, L.; et al. Tumor-penetrating Peptide Conjugated and Doxorubicin Loaded T1-T2 Dual Mode MRI Contrast Agents Nanoparticles for Tumor Theranostics. Theranostics 2018, 8, 92–108. [Google Scholar] [CrossRef]
- Li, F.; Zhi, D.; Luo, Y.; Zhang, J.; Nan, X.; Zhang, Y.; Zhou, W.; Qiu, B.; Wen, L.; Liang, G. Core/shell Fe3O4/Gd2O3 nanocubes as T1-T2 dual modal MRI contrast agents. Nanoscale 2016, 8, 12826–12833. [Google Scholar] [CrossRef]
- Yang, L.; Zhou, Z.; Liu, H.; Wu, C.; Zhang, H.; Huang, G.; Ai, H.; Gao, J. Europium-engineered iron oxide nanocubes with high T1 and T2 contrast abilities for MRI in living subjects. Nanoscale 2015, 7, 6843–6850. [Google Scholar] [CrossRef] [Green Version]
- Dadfar, S.M.; Roemhild, K.; Drude, N.I.; von Stillfried, S.; Knuchel, R.; Kiessling, F.; Lammers, T. Iron oxide nanoparticles: Diagnostic, therapeutic and theranostic applications. Adv. Drug Deliv. Rev. 2019, 138, 302–325. [Google Scholar] [CrossRef]
- Paredes, K.O.; Ruiz-Cabello, J.; Alarcón, D.I.; Filice, M. Chapter 14-The State of the Art of Investigational and Approved Nanomedicine Products for Nucleic Acid Delivery. In Nucleic Acid Nanotheranostics; Filice, M., Ruiz-Cabello, J., Eds.; Elsevier: Amsterdam, The Netherlands, 2019; pp. 421–456. [Google Scholar] [CrossRef]
- Shevtsov, M.A.; Nikolaev, B.P.; Yakovleva, L.Y.; Dobrodumov, A.V.; Zhakhov, A.V.; Mikhrina, A.L.; Pitkin, E.; Parr, M.A.; Rolich, V.I.; Simbircev, A.S.; et al. Recombinant Interleukin-1 Receptor Antagonist Conjugated to Superparamagnetic Iron Oxide Nanoparticles for Theranostic Targeting of Experimental Glioblastoma. Neoplasia 2015, 17, 32–42. [Google Scholar] [CrossRef] [Green Version]
- Ozdemir, A.; Ekiz, M.S.; Dilli, A.; Guler, M.O.; Tekinay, A.B. Amphiphilic peptide coated superparamagnetic iron oxide nanoparticles for in vivo MR tumor imaging. RSC Adv. 2016, 6, 45135–45146. [Google Scholar] [CrossRef]
- Sanjai, C.; Kothan, S.; Gonil, P.; Saesoo, S.; Sajomsang, W. Super-paramagnetic loaded nanoparticles based on biological macromolecules for in vivo targeted MR imaging. Int. J. Biol. Macromol. 2016, 86, 233–241. [Google Scholar] [CrossRef]
- Chee, H.L.; Gan, C.R.R.; Ng, M.; Low, L.; Fernig, D.G.; Bhakoo, K.K.; Paramelle, D. Biocompatible Peptide-Coated Ultrasmall Superparamagnetic Iron Oxide Nanoparticles for In Vivo Contrast-Enhanced Magnetic Resonance Imaging. ACS Nano 2018, 12, 6480–6491. [Google Scholar] [CrossRef] [PubMed]
- Lazaro-Carrillo, A.; Filice, M.; Guillén, M.J.; Amaro, R.; Viñambres, M.; Tabero, A.; Paredes, K.O.; Villanueva, A.; Calvo, P.; del Puerto Morales, M.; et al. Tailor-made PEG coated iron oxide nanoparticles as contrast agents for long lasting magnetic resonance molecular imaging of solid cancers. Mater. Sci. Eng. C 2020, 107, 110262. [Google Scholar] [CrossRef] [PubMed]
- Yang, D.; Yang, G.; Yang, P.; Lv, R.; Gai, S.; Li, C.; He, F.; Lin, J. Assembly of Au Plasmonic Photothermal Agent and Iron Oxide Nanoparticles on Ultrathin Black Phosphorus for Targeted Photothermal and Photodynamic Cancer Therapy. Adv. Funct. Mater. 2017, 27, 1700371. [Google Scholar] [CrossRef]
- Cao, Y.; Mao, Z.; He, Y.; Kuang, Y.; Liu, M.; Zhou, Y.; Zhang, Y.; Pei, R. Extremely Small Iron Oxide Nanoparticle-Encapsulated Nanogels as a Glutathione-Responsive T1 Contrast Agent for Tumor-Targeted Magnetic Resonance Imaging. ACS Appl. Mater. Interfaces 2020, 12, 26973–26981. [Google Scholar] [CrossRef] [PubMed]
- Xu, X.; Zhou, X.; Xiao, B.; Xu, H.; Hu, D.; Qian, Y.; Hu, H.; Zhou, Z.; Liu, X.; Gao, J.; et al. Glutathione-Responsive Magnetic Nanoparticles for Highly Sensitive Diagnosis of Liver Metastases. Nano Lett. 2021, 21, 2199–2206. [Google Scholar] [CrossRef]
- Chen, Y.; Ai, K.; Liu, J.; Ren, X.; Jiang, C.; Lu, L. Polydopamine-based coordination nanocomplex for T1/T2 dual mode magnetic resonance imaging-guided chemo-photothermal synergistic therapy. Biomaterials 2016, 77, 198–206. [Google Scholar] [CrossRef]
- Shu, G.; Chen, M.; Song, J.; Xu, X.; Lu, C.; Du, Y.; Xu, M.; Zhao, Z.; Zhu, M.; Fan, K.; et al. Sialic acid-engineered mesoporous polydopamine nanoparticles loaded with SPIO and Fe(3+) as a novel theranostic agent for T1/T2 dual-mode MRI-guided combined chemo-photothermal treatment of hepatic cancer. Bioact. Mater. 2021, 6, 1423–1435. [Google Scholar] [CrossRef]
- Yang, M.; Gao, L.; Liu, K.; Luo, C.; Wang, Y.; Yu, L.; Peng, H.; Zhang, W. Characterization of Fe3O4/SiO2/Gd2O(CO3)2 core/shell/shell nanoparticles as T1 and T2 dual mode MRI contrast agent. Talanta 2015, 131, 661–665. [Google Scholar] [CrossRef]
- Choi, J.-S.; Lee, J.-H.; Shin, T.-H.; Song, H.-T.; Kim, E.Y.; Cheon, J. Self-Confirming “AND” Logic Nanoparticles for Fault-Free MRI. J. Am. Chem. Soc. 2010, 132, 11015–11017. [Google Scholar] [CrossRef] [Green Version]
- Shin, T.-H.; Choi, J.-S.; Yun, S.; Kim, I.-S.; Song, H.-T.; Kim, Y.; Park, K.I.; Cheon, J. T1 and T2 Dual-Mode MRI Contrast Agent for Enhancing Accuracy by Engineered Nanomaterials. ACS Nano 2014, 8, 3393–3401. [Google Scholar] [CrossRef]
- Li, J.; Li, X.; Gong, S.; Zhang, C.; Qian, C.; Qiao, H.; Sun, M. Dual-Mode Avocado-like All-Iron Nanoplatform for Enhanced T1/T2 MRI-Guided Cancer Theranostic Therapy. Nano Lett. 2020, 20, 4842–4849. [Google Scholar] [CrossRef]
- Liu, D.; Li, J.; Wang, C.; An, L.; Lin, J.; Tian, Q.; Yang, S. Ultrasmall Fe@Fe3O4 nanoparticles as T1-T2 dual-mode MRI contrast agents for targeted tumor imaging. Nanomedicine 2021, 32, 102335. [Google Scholar] [CrossRef]
- Wang, J.; Jia, Y.; Wang, Q.; Liang, Z.; Han, G.; Wang, Z.; Lee, J.; Zhao, M.; Li, F.; Bai, R.; et al. An Ultrahigh-Field-Tailored T1 -T2 Dual-Mode MRI Contrast Agent for High-Performance Vascular Imaging. Adv. Mater. 2021, 33, e2004917. [Google Scholar] [CrossRef]
- Erami, R.S.; Ovejero, K.; Meghdadi, S.; Filice, M.; Amirnasr, M.; Rodríguez-Diéguez, A.; De La Orden, M.U.; Gómez-Ruiz, S. Applications of Nanomaterials Based on Magnetite and Mesoporous Silica on the Selective Detection of Zinc Ion in Live Cell Imaging. Nanomaterials 2018, 8, 434. [Google Scholar] [CrossRef] [Green Version]
- Cho, M.; Contreras, E.Q.; Lee, S.S.; Jones, C.J.; Jang, W.; Colvin, V.L. Characterization and Optimization of the Fluorescence of Nanoscale Iron Oxide/Quantum Dot Complexes. J. Phys. Chem. C 2014, 118, 14606–14616. [Google Scholar] [CrossRef]
- Pahari, S.K.; Olszakier, S.; Kahn, I.; Amirav, L. Magneto-Fluorescent Yolk–Shell Nanoparticles. Chem. Mater. 2018, 30, 775–780. [Google Scholar] [CrossRef]
- Lartigue, L.; Coupeau, M.; Lesault, M. Luminophore and Magnetic Multicore Nanoassemblies for Dual-Mode MRI and Fluorescence Imaging. Nanomaterials 2019, 10, 28. [Google Scholar] [CrossRef] [Green Version]
- Wen, Y.; Xu, M.; Liu, X.; Jin, X.; Kang, J.; Xu, D.; Sang, H.; Gao, P.; Chen, X.; Zhao, L. Magnetofluorescent nanohybrid comprising polyglycerol grafted carbon dots and iron oxides: Colloidal synthesis and applications in cellular imaging and magnetically enhanced drug delivery. Colloids Surf. B Biointerfaces 2019, 173, 842–850. [Google Scholar] [CrossRef]
- Lee, J.H.; Jun, Y.W.; Yeon, S.I.; Shin, J.S.; Cheon, J. Dual-mode nanoparticle probes for high-performance magnetic resonance and fluorescence imaging of neuroblastoma. Angew. Chem. Int. Ed. Engl. 2006, 45, 8160–8162. [Google Scholar] [CrossRef]
- Fei-Peng, Z.; Guo-Tao, C.; Shou-Ju, W.; Ying, L.; Yu-Xia, T.; Ying, T.; Jian-Dong, W.; Chun-Yan, W.; Xin, W.; Jing, S.; et al. Dual-Modality Imaging Probes with High Magnetic Relaxivity and Near-Infrared Fluorescence Based Highly Aminated Mesoporous Silica Nanoparticles. J. Nanomater. 2016, 2016, 6502127. [Google Scholar] [CrossRef] [Green Version]
- Chen, O.; Riedemann, L.; Etoc, F.; Herrmann, H.; Coppey, M.; Barch, M.; Farrar, C.T.; Zhao, J.; Bruns, O.T.; Wei, H.; et al. Magneto-fluorescent core-shell supernanoparticles. Nat. Commun. 2014, 5, 5093. [Google Scholar] [CrossRef] [Green Version]
- He, X.; Shen, X.; Li, D.; Liu, Y.; Jia, K.; Liu, X. Dual-Mode Fluorescence and Magnetic Resonance Imaging Nanoprobe Based on Aromatic Amphiphilic Copolymer Encapsulated CdSe@CdS and Fe3O4. ACS Appl. Bio. Mater. 2018, 1, 520–528. [Google Scholar] [CrossRef]
- Bixner, O.; Gal, N.; Zaba, C.; Scheberl, A.; Reimhult, E. Fluorescent Magnetopolymersomes: A Theranostic Platform to Track Intracellular Delivery. Materials 2017, 10, 1303. [Google Scholar] [CrossRef] [Green Version]
- Demillo, V.G.; Zhu, X. Zwitterionic amphiphile coated magnetofluorescent nanoparticles-synthesis, characterization and tumor cell targeting. J. Mater. Chem. B 2015, 3, 8328–8336. [Google Scholar] [CrossRef] [Green Version]
- Ling, D.; Park, W.; Park, S.-j.; Lu, Y.; Kim, K.S.; Hackett, M.J.; Kim, B.H.; Yim, H.; Jeon, Y.S.; Na, K.; et al. Multifunctional Tumor pH-Sensitive Self-Assembled Nanoparticles for Bimodal Imaging and Treatment of Resistant Heterogeneous Tumors. J. Am. Chem. Soc. 2014, 136, 5647–5655. [Google Scholar] [CrossRef]
- Garcia Ribeiro, R.S.; Belderbos, S.; Danhier, P.; Gallo, J.; Manshian, B.B.; Gallez, B.; Banobre, M.; de Cuyper, M.; Soenen, S.J.; Gsell, W.; et al. Targeting tumor cells and neovascularization using RGD-functionalized magnetoliposomes. Int. J. Nanomed. 2019, 14, 5911–5924. [Google Scholar] [CrossRef] [Green Version]
- Das, M.; Solanki, A.; Apeksha, J.; Devkar, R.; Seshadri, S.; Thakore, S. β-cyclodextrin based dual-responsive multifunctional nanotheranostics for cancer cell targeting and dual drug delivery. Carbohydr. Polym. 2018, 206, 694–705. [Google Scholar] [CrossRef]
- Feld, A.; Merkl, J.P.; Kloust, H.; Flessau, S.; Schmidtke, C.; Wolter, C.; Ostermann, J.; Kampferbeck, M.; Eggers, R.; Mews, A.; et al. A universal approach to ultrasmall magneto-fluorescent nanohybrids. Angew. Chem. Int. Ed. Engl. 2015, 54, 12468–12471. [Google Scholar] [CrossRef] [PubMed]
- Pinkerton, N.M.; Gindy, M.E.; Calero-Ddel, C.V.; Wolfson, T.; Pagels, R.F.; Adler, D.; Gao, D.; Li, S.; Wang, R.; Zevon, M.; et al. Single-Step Assembly of Multimodal Imaging Nanocarriers: MRI and Long-Wavelength Fluorescence Imaging. Adv. Healthc. Mater. 2015, 4, 1376–1385. [Google Scholar] [CrossRef] [PubMed]
- Vijayan, V.M.; Beeran, A.E.; Shenoy, S.J.; Muthu, J.; Thomas, V. New Magneto-Fluorescent Hybrid Polymer Nanogel for Theranostic Applications. ACS Appl. Bio. Mater. 2019, 2, 757–768. [Google Scholar] [CrossRef]
- Wang, G.; Zhang, X.; Liu, Y.; Hu, Z.; Mei, X.; Uvdal, K. Magneto-fluorescent nanoparticles with high-intensity NIR emission, T1- and T2-weighted MR for multimodal specific tumor imaging. J. Mater. Chem. B 2015, 3, 3072–3080. [Google Scholar] [CrossRef] [PubMed]
- Faucon, A.; Benhelli-Mokrani, H.; Fleury, F.; Dubreil, L.; Hulin, P.; Nedellec, S.; Doussineau, T.; Antoine, R.; Orlando, T.; Lascialfari, A.; et al. Tuning the architectural integrity of high-performance magneto-fluorescent core-shell nanoassemblies in cancer cells. J. Colloid Interface Sci. 2016, 479, 139–149. [Google Scholar] [CrossRef] [PubMed]
- Faucon, A.; Maldiney, T.; Clément, O.; Hulin, P.; Nedellec, S.; Robard, M.; Gautier, N.; De Meulenaere, E.; Clays, K.; Orlando, T.; et al. Highly cohesive dual nanoassemblies for complementary multiscale bioimaging. J. Mater. Chem. B 2014, 2, 7747–7755. [Google Scholar] [CrossRef] [Green Version]
- Linot, C.; Poly, J.; Boucard, J.; Pouliquen, D.; Nedellec, S.; Hulin, P.; Marec, N.; Arosio, P.; Lascialfari, A.; Guerrini, A.; et al. PEGylated Anionic Magnetofluorescent Nanoassemblies: Impact of Their Interface Structure on Magnetic Resonance Imaging Contrast and Cellular Uptake. ACS Appl. Mater. Interfaces 2017, 9, 14242–14257. [Google Scholar] [CrossRef]
- Chen, Q.; Shang, W.; Zeng, C.; Wang, K.; Liang, X.; Chi, C.; Liang, X.; Yang, J.; Fang, C.; Tian, J. Theranostic imaging of liver cancer using targeted optical/MRI dual-modal probes. Oncotarget 2017, 8, 32741. [Google Scholar] [CrossRef] [Green Version]
- Namikawa, T.; Sato, T.; Hanazaki, K. Recent advances in near-infrared fluorescence-guided imaging surgery using indocyanine green. Surg. Today 2015, 45, 1467–1474. [Google Scholar] [CrossRef]
- Lin, X.; Zhu, R.; Hong, Z.; Zhang, X.; Chen, S.; Song, J.; Yang, H. GSH-Responsive Radiosensitizers with Deep Penetration Ability for Multimodal Imaging-Guided Synergistic Radio-Chemodynamic Cancer Therapy. Adv. Funct. Mater. 2021, 31, 2101278. [Google Scholar] [CrossRef]
- Sanchez, A.; Ovejero Paredes, K.; Ruiz-Cabello, J.; Martinez-Ruiz, P.; Pingarron, J.M.; Villalonga, R.; Filice, M. Hybrid Decorated Core@Shell Janus Nanoparticles as a Flexible Platform for Targeted Multimodal Molecular Bioimaging of Cancer. ACS Appl. Mater. Interfaces 2018, 10, 31032–31043. [Google Scholar] [CrossRef]
- Mannheim, J.G.; Schmid, A.M.; Schwenck, J.; Katiyar, P.; Herfert, K.; Pichler, B.J.; Disselhorst, J.A. PET/MRI Hybrid Systems. Semin. Nucl. Med. 2018, 48, 332–347. [Google Scholar] [CrossRef]
- Forte, E.; Fiorenza, D.; Torino, E.; Costagliola di Polidoro, A.; Cavaliere, C.; Netti, P.A.; Salvatore, M.; Aiello, M. Radiolabeled PET/MRI Nanoparticles for Tumor Imaging. J. Clin. Med. 2019, 9, 89. [Google Scholar] [CrossRef] [Green Version]
- Calle, D.; Ballesteros, P.; Cerdan, S. Advanced Contrast Agents for Multimodal Biomedical Imaging Based on Nanotechnology. Methods Mol. Biol. 2018, 1718, 441–457. [Google Scholar] [CrossRef]
- Thomas, R.; Park, I.-K.; Jeong, Y. Magnetic Iron Oxide Nanoparticles for Multimodal Imaging and Therapy of Cancer. Int. J. Mol. Sci. 2013, 14, 15910–15930. [Google Scholar] [CrossRef] [Green Version]
- Goldenberg, J.M.; Cardenas-Rodriguez, J.; Pagel, M.D. Preliminary Results that Assess Metformin Treatment in a Preclinical Model of Pancreatic Cancer Using Simultaneous [(18)F]FDG PET and acidoCEST MRI. Mol. Imaging Biol. 2018, 20, 575–583. [Google Scholar] [CrossRef]
- Lee, H.Y.; Li, Z.; Chen, K.; Hsu, A.R.; Xu, C.; Xie, J.; Sun, S.; Chen, X. PET/MRI Dual-Modality Tumor Imaging Using Arginine-Glycine-Aspartic (RGD)-Conjugated Radiolabeled Iron Oxide Nanoparticles. J. Nucl. Med. 2008, 49, 1371–1379. [Google Scholar] [CrossRef] [Green Version]
- Eiber, M.; Nekolla, S.G.; Maurer, T.; Weirich, G.; Wester, H.J.; Schwaiger, M. (68)Ga-PSMA PET/MR with multimodality image analysis for primary prostate cancer. Abdom Imaging 2015, 40, 1769–1771. [Google Scholar] [CrossRef] [Green Version]
- Pinker, K.; Bogner, W.; Baltzer, P.; Karanikas, G.; Magometschnigg, H.; Brader, P.; Gruber, S.; Bickel, H.; Dubsky, P.; Bago-Horvath, Z.; et al. Improved differentiation of benign and malignant breast tumors with multiparametric 18fluorodeoxyglucose positron emission tomography magnetic resonance imaging: A feasibility study. Clin. Cancer Res. 2014, 20, 3540–3549. [Google Scholar] [CrossRef] [Green Version]
- Rice, S.L.; Friedman, K.P. Clinical PET-MR Imaging in Breast Cancer and Lung Cancer. PET Clin. 2016, 11, 387–402. [Google Scholar] [CrossRef] [Green Version]
- Melsaether, A.; Moy, L. Breast PET/MR Imaging. Radiol. Clin. North. Am. 2017, 55, 579–589. [Google Scholar] [CrossRef]
- Madru, R.; Kjellman, P.; Olsson, F.; Wingardh, K.; Ingvar, C.; Stahlberg, F.; Olsrud, J.; Latt, J.; Fredriksson, S.; Knutsson, L.; et al. 99mTc-labeled superparamagnetic iron oxide nanoparticles for multimodality SPECT/MRI of sentinel lymph nodes. J. Nucl. Med. 2012, 53, 459–463. [Google Scholar] [CrossRef] [Green Version]
- Torres Martin de Rosales, R.; Tavare, R.; Glaria, A.; Varma, G.; Protti, A.; Blower, P.J. ((9)(9)m)Tc-bisphosphonate-iron oxide nanoparticle conjugates for dual-modality biomedical imaging. Bioconjug Chem. 2011, 22, 455–465. [Google Scholar] [CrossRef]
- Sun, H.; Zhang, B.; Jiang, X.; Liu, H.; Deng, S.; Li, Z.; Shi, H. Radiolabeled ultra-small Fe3O4 nanoprobes for tumor-targeted multimodal imaging. Nanomedicine 2019, 14, 5–17. [Google Scholar] [CrossRef]
- Liu, Y.; Li, Y.; Li, X.-M.; He, T. Kinetics of (3-Aminopropyl)triethoxylsilane (APTES) Silanization of Superparamagnetic Iron Oxide Nanoparticles. Langmuir 2013, 29, 15275–15282. [Google Scholar] [CrossRef]
- Veintemillas-Verdaguer, S.; Luengo, Y.; Serna, C.J.; Andrés-Vergés, M.; Varela, M.; Calero, M.; Lazaro-Carrillo, A.; Villanueva, A.; Sisniega, A.; Montesinos, P.; et al. Bismuth labeling for the CT assessment of local administration of magnetic nanoparticles. Nanotechnology 2015, 26, 135101. [Google Scholar] [CrossRef] [PubMed]
- Bakenecker, A.C.; Ahlborg, M.; Debbeler, C.; Kaethner, C.; Buzug, T.M.; Lüdtke-Buzug, K. Magnetic particle imaging in vascular medicine. Innov. Surg. Sci. 2018, 3, 179–192. [Google Scholar] [CrossRef]
- Knopp, T.; Gdaniec, N.; Möddel, M. Magnetic particle imaging: From proof of principle to preclinical applications. Phys. Med. Biol. 2017, 62, R124–R178. [Google Scholar] [CrossRef]
- Talebloo, N.; Gudi, M.; Robertson, N.; Wang, P. Magnetic Particle Imaging: Current Applications in Biomedical Research. J. Magn. Reson. Imaging 2020, 51, 1659–1668. [Google Scholar] [CrossRef]
- Meola, A.; Rao, J.; Chaudhary, N.; Song, G.; Zheng, X.; Chang, S.D. Magnetic Particle Imaging in Neurosurgery. World Neurosurg. 2019, 125, 261–270. [Google Scholar] [CrossRef]
- Yu, E.Y.; Bishop, M.; Zheng, B.; Ferguson, R.M.; Khandhar, A.P.; Kemp, S.J.; Krishnan, K.M.; Goodwill, P.W.; Conolly, S.M. Magnetic Particle Imaging: A Novel in Vivo Imaging Platform for Cancer Detection. Nano Lett. 2017, 17, 1648–1654. [Google Scholar] [CrossRef] [PubMed]
- Arami, H.; Teeman, E.; Troksa, A.; Bradshaw, H.; Saatchi, K.; Tomitaka, A.; Gambhir, S.S.; Häfeli, U.O.; Liggitt, D.; Krishnan, K.M. Tomographic magnetic particle imaging of cancer targeted nanoparticles. Nanoscale 2017, 9, 18723–18730. [Google Scholar] [CrossRef] [PubMed]
- Wu, K.; Su, D.; Liu, J.; Saha, R.; Wang, J.-P. Magnetic nanoparticles in nanomedicine: A review of recent advances. Nanotechnology 2019, 30, 502003. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Horvat, S.; Vogel, P.; Kampf, T.; Brandl, A.; Alshamsan, A.; Alhadlaq, H.A.; Ahamed, M.; Albrecht, K.; Behr, V.C.; Beilhack, A.; et al. Crosslinked Coating Improves the Signal-to-Noise Ratio of Iron Oxide Nanoparticles in Magnetic Particle Imaging (MPI). ChemNanoMat 2020, 6, 755–758. [Google Scholar] [CrossRef]
- Antonelli, A.; Szwargulski, P.; Scarpa, E.-S.; Thieben, F.; Cordula, G.; Ambrosi, G.; Guidi, L.; Ludewig, P.; Knopp, T.; Magnani, M. Development of long circulating magnetic particle imaging tracers: Use of novel magnetic nanoparticles and entrapment into human erythrocytes. Nanomedicine 2020, 15, 739–753. [Google Scholar] [CrossRef]
- Pablico-Lansigan, M.H.; Situ, S.F.; Samia, A.C.S. Magnetic particle imaging: Advancements and perspectives for real-time in vivo monitoring and image-guided therapy. Nanoscale 2013, 5, 4040–4055. [Google Scholar] [CrossRef]
- Ferguson, R.M.; Khandhar, A.P.; Krishnan, K.M. Tracer design for magnetic particle imaging (invited). J. Appl. Phys. 2012, 111, 07B318. [Google Scholar] [CrossRef] [Green Version]
- Zhao, Z.; Garraud, N.; Arnold, D.P.; Rinaldi, C. Effects of particle diameter and magnetocrystalline anisotropy on magnetic relaxation and magnetic particle imaging performance of magnetic nanoparticles. Phys. Med. Biol. 2020, 65, 025014. [Google Scholar] [CrossRef]
- Ziemian, S.; Löwa, N.; Kosch, O.; Bajj, D.; Wiekhorst, F.; Schütz, G. Optimization of Iron Oxide Tracer Synthesis for Magnetic Particle Imaging. Nanomaterials 2018, 8, 180. [Google Scholar] [CrossRef] [Green Version]
- Dadfar, S.M.; Camozzi, D.; Darguzyte, M.; Roemhild, K.; Varvarà, P.; Metselaar, J.; Banala, S.; Straub, M.; Güvener, N.; Engelmann, U.; et al. Size-isolation of superparamagnetic iron oxide nanoparticles improves MRI, MPI and hyperthermia performance. J. Nanobiotechnol. 2020, 18, 22. [Google Scholar] [CrossRef]
- Rost, N.C.V.; Sen, K.; Savliwala, S.; Singh, I.; Liu, S.; Unni, M.; Raniero, L.; Rinaldi, C. Magnetic particle imaging performance of liposomes encapsulating iron oxide nanoparticles. J. Magn. Magn. Mater. 2020, 504, 166675. [Google Scholar] [CrossRef]
- Rojas, J.M.; Gavilán, H.; del Dedo, V.; Lorente-Sorolla, E.; Sanz-Ortega, L.; da Silva, G.B.; Costo, R.; Perez-Yagüe, S.; Talelli, M.; Marciello, M.; et al. Time-course assessment of the aggregation and metabolization of magnetic nanoparticles. Acta Biomater. 2017, 58, 181–195. [Google Scholar] [CrossRef]
- Silva, G.B.d.; Marciello, M.; Morales, M.d.P.; Serna, C.J.; Vargas, M.D.; Ronconi, C.M.; Costo, R. Studies of the Colloidal Properties of Superparamagnetic Iron Oxide Nanoparticles Functionalized with Platinum Complexes in Aqueous and PBS Buffer Media. J. Braz. Chem. Soc. 2017, 28, 731–739. [Google Scholar] [CrossRef]
- Salehnia, Z.; Shahbazi-Gahrouei, D.; Akbarzadeh, A.; Baradaran, B.; Farajnia, S.; Naghibi, M. Synthesis and characterisation of iron oxide nanoparticles conjugated with epidermal growth factor receptor (EGFR) monoclonal antibody as MRI contrast agent for cancer detection. IET Nanobiotechnol. 2019, 13, 400–406. [Google Scholar] [CrossRef]
- Arias, L.S.; Pessan, J.P.; Vieira, A.P.M.; Lima, T.M.T.d.; Delbem, A.C.B.; Monteiro, D.R. Iron Oxide Nanoparticles for Biomedical Applications: A Perspective on Synthesis, Drugs, Antimicrobial Activity, and Toxicity. Antibiotics 2018, 7, 46. [Google Scholar] [CrossRef] [Green Version]
- Xue, W.; Liu, Y.; Zhang, N.; Yao, Y.; Ma, P.; Wen, H.; Huang, S.; Luo, Y.; Fan, H. Effects of core size and PEG coating layer of iron oxide nanoparticles on the distribution and metabolism in mice. Int. J. Nanomed. 2018, 13, 5719–5731. [Google Scholar] [CrossRef] [Green Version]
- Ruiz, A.; Alpízar, A.; Beola, L.; Rubio, C.; Gavilán, H.; Marciello, M.; Rodríguez-Ramiro, I.; Ciordia, S.; Morris, C.J.; Morales, M.d.P. Understanding the Influence of a Bifunctional Polyethylene Glycol Derivative in Protein Corona Formation around Iron Oxide Nanoparticles. Materials 2019, 12, 2218. [Google Scholar] [CrossRef] [Green Version]
- Sharma, A.; Cornejo, C.; Mihalic, J.; Geyh, A.; Bordelon, D.E.; Korangath, P.; Westphal, F.; Gruettner, C.; Ivkov, R. Physical characterization and in vivo organ distribution of coated iron oxide nanoparticles. Sci. Rep. 2018, 8, 4916. [Google Scholar] [CrossRef] [Green Version]
- Israel, L.L.; Galstyan, A.; Holler, E.; Ljubimova, J.Y. Magnetic iron oxide nanoparticles for imaging, targeting and treatment of primary and metastatic tumors of the brain. J. Control. Release 2020, 320, 45–62. [Google Scholar] [CrossRef]
- Schütz, G. The Potential of Magnetic Particle Imaging in the Competitive Environment of Cardiac Diagnostics. In Proceedings of the Magnetic Particle Imaging, Berlin/Heidelberg, Germany, 22 April 2012; pp. 129–134. [Google Scholar]
- Graeser, M.; Thieben, F.; Szwargulski, P.; Werner, F.; Gdaniec, N.; Boberg, M.; Griese, F.; Möddel, M.; Ludewig, P.; van de Ven, D.; et al. Human-sized magnetic particle imaging for brain applications. Nat. Commun. 2019, 10, 1936. [Google Scholar] [CrossRef]
- Sedlacik, J.; Frölich, A.; Spallek, J.; Forkert, N.D.; Faizy, T.D.; Werner, F.; Knopp, T.; Krause, D.; Fiehler, J.; Buhk, J.-H. Magnetic Particle Imaging for High Temporal Resolution Assessment of Aneurysm Hemodynamics. PLoS ONE 2016, 11, e0160097. [Google Scholar] [CrossRef]
- Cooley, C.Z.; Mandeville, J.B.; Mason, E.E.; Mandeville, E.T.; Wald, L.L. Rodent Cerebral Blood Volume (CBV) changes during hypercapnia observed using Magnetic Particle Imaging (MPI) detection. Neuroimage 2018, 178, 713–720. [Google Scholar] [CrossRef]
- Zhou, X.Y.; Jeffris, K.E.; Yu, E.Y.; Zheng, B.; Goodwill, P.W.; Nahid, P.; Conolly, S.M. First in vivo magnetic particle imaging of lung perfusion in rats. Phys. Med. Biol. 2017, 62, 3510–3522. [Google Scholar] [CrossRef] [Green Version]
- Bulte, J.W.M.; Walczak, P.; Janowski, M.; Krishnan, K.M.; Arami, H.; Halkola, A.; Gleich, B.; Rahmer, J. Quantitative “Hot Spot” Imaging of Transplanted Stem Cells using Superparamagnetic Tracers and Magnetic Particle Imaging (MPI). Tomography 2015, 1, 91–97. [Google Scholar] [CrossRef] [PubMed]
- Zheng, B.; Vazin, T.; Goodwill, P.W.; Conway, A.; Verma, A.; Saritas, E.U.; Schaffer, D.; Conolly, S.M. Magnetic Particle Imaging tracks the long-term fate of in vivo neural cell implants with high image contrast. Sci. Rep. 2015, 5, 14055. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Ma, X.; Liao, H.; Liang, Z.; Li, F.; Tian, J.; Ling, D. Artificially Engineered Cubic Iron Oxide Nanoparticle as a High-Performance Magnetic Particle Imaging Tracer for Stem Cell Tracking. ACS Nano 2020, 14, 2053–2062. [Google Scholar] [CrossRef] [PubMed]
- Herz, S.; Vogel, P.; Dietrich, P.; Kampf, T.; Rückert, M.A.; Kickuth, R.; Behr, V.C.; Bley, T.A. Magnetic Particle Imaging Guided Real-Time Percutaneous Transluminal Angioplasty in a Phantom Model. Cardiovasc. Interv. Radiol. 2018, 41, 1100–1105. [Google Scholar] [CrossRef]
- Rahmer, J.; Wirtz, D.; Bontus, C.; Borgert, J.; Gleich, B. Interactive Magnetic Catheter Steering With 3-D Real-Time Feedback Using Multi-Color Magnetic Particle Imaging. IEEE Trans. Med. Imaging 2017, 36, 1449–1456. [Google Scholar] [CrossRef]
- Mason, E.E.; Mattingly, E.; Herb, K.; Śliwiak, M.; Franconi, S.; Cooley, C.Z.; Slanetz, P.J.; Wald, L.L. Concept for using magnetic particle imaging for intraoperative margin analysis in breast-conserving surgery. Sci. Rep. 2021, 11, 13456. [Google Scholar] [CrossRef]
- Makela, A.V.; Gaudet, J.M.; Schott, M.A.; Sehl, O.C.; Contag, C.H.; Foster, P.J. Magnetic Particle Imaging of Macrophages Associated with Cancer: Filling the Voids Left by Iron-Based Magnetic Resonance Imaging. Mol. Imaging Biol. 2020, 22, 958–968. [Google Scholar] [CrossRef]
- Parkins, K.M.; Melo, K.P.; Ronald, J.A.; Foster, P.J. Visualizing tumour self-homing with magnetic particle imaging. bioRxiv 2021, 13, 6016–6023. [Google Scholar] [CrossRef]
- Bulte, J.W.M. Superparamagnetic iron oxides as MPI tracers: A primer and review of early applications. Adv. Drug Deliv. Rev. 2019, 138, 293–301. [Google Scholar] [CrossRef]
- Hadadian, Y.; Sampaio, D.R.T.; Ramos, A.P.; Carneiro, A.A.O.; Mozaffari, M.; Cabrelli, L.C.; Pavan, T.Z. Synthesis and characterization of zinc substituted magnetite nanoparticles and their application to magneto-motive ultrasound imaging. J. Magn. Magn. Mater. 2018, 465, 33–43. [Google Scholar] [CrossRef]
- Sjöstrand, S.; Evertsson, M.; Thring, C.; Bacou, M.; Farrington, S.; Moug, S.; Moran, C.; Jansson, T.; Mulvana, H. Contrast-enhanced magnetomotive ultrasound imaging (CE-MMUS) for colorectal cancer staging: Assessment of sensitivity and resolution to detect alterations in tissue stiffness. In Proceedings of the 2019 IEEE International Ultrasonics Symposium (IUS), Glasgow, Scotland, UK, 6–9 October 2019; pp. 1077–1080. [Google Scholar]
- Evertsson, M.; Kjellman, P.; Cinthio, M.; Andersson, R.; Tran, T.A.; Grafström, G.; Toftevall, H.; Fredriksson, S.; Ingvar, C.; Strand, S.E.; et al. Combined Magnetomotive ultrasound, PET/CT, and MR imaging of (68)Ga-labelled superparamagnetic iron oxide nanoparticles in rat sentinel lymph nodes in vivo. Sci. Rep. 2017, 7, 4824. [Google Scholar] [CrossRef]
- Sjöstrand, S.; Evertsson, M.; Jansson, T. Magnetomotive Ultrasound Imaging Systems: Basic Principles and First Applications. Ultrasound Med. Biol. 2020, 46, 2636–2650. [Google Scholar] [CrossRef]
- Mehrmohammadi, M.; Shin, T.-H.; Qu, M.; Kruizinga, P.; Truby, R.L.; Lee, J.-H.; Cheon, J.; Emelianov, S.Y. In vivo pulsed magneto-motive ultrasound imaging using high-performance magnetoactive contrast nanoagents. Nanoscale 2013, 5, 11179–11186. [Google Scholar] [CrossRef] [Green Version]
- Qu, M.; Mehrmohammadi, M.; Emelianov, S. Detection of Nanoparticle Endocytosis Using Magneto-Photoacoustic Imaging. Small 2011, 7, 2858–2862. [Google Scholar] [CrossRef]
- Qu, M.; Mehrmohammadi, M.; Truby, R.; Graf, I.; Homan, K.; Emelianov, S. Contrast-enhanced magneto-photo-acoustic imaging in vivo using dual-contrast nanoparticles. Photoacoustics 2014, 2, 55–62. [Google Scholar] [CrossRef] [Green Version]
- Jin, Y.; Jia, C.; Huang, S.-W.; O’Donnell, M.; Gao, X. Multifunctional nanoparticles as coupled contrast agents. Nat. Commun. 2010, 1, 41. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Arnal, B.; Wei, C.-W.; Shang, J.; Nguyen, T.-M.; O’Donnell, M.; Gao, X. Magneto-Optical Nanoparticles for Cyclic Magnetomotive Photoacoustic Imaging. ACS Nano 2015, 9, 1964–1976. [Google Scholar] [CrossRef] [Green Version]
- Arnal, B.; Yoon, S.J.; Li, J.; Gao, X.; O’Donnell, M. Magneto-optical nanoparticles for cyclic magnetomotive photoacoustic imaging. Phys. C Supercond. Its Appl. 2018, 548, 90–92. [Google Scholar] [CrossRef] [Green Version]
- Konstantinou, G.; Chil, R.; Desco, M.; Vaquero, J.J. Subsurface Laser Engraving Techniques for Scintillator Crystals: Methods, Applications, and Advantages. IEEE Trans. Radiat. Plasma Med. Sci. 2017, 1, 377–384. [Google Scholar] [CrossRef]
- Mela, C.; Papay, F.; Liu, Y. Novel Multimodal, Multiscale Imaging System with Augmented Reality. Diagnostics 2021, 11, 441. [Google Scholar] [CrossRef] [PubMed]
- Herskovits, E.H. Artificial intelligence in molecular imaging. Ann. Transl. Med. 2021, 9, 824. [Google Scholar] [CrossRef] [PubMed]
Imaging Modality | Information | Advantages | Disadvantages |
---|---|---|---|
MRI | Anatomical | High spatial resolution, no tissue penetration limit | Low sensitivity, long imaging time |
Optical imaging | Molecular | High sensitivity, fast acquisition, low cost | Poor spatial resolution, small penetration depth |
CT | Anatomical | High spatial resolution, strong penetration depth, fast acquisition | Radiation risk |
PET | Molecular | High sensitivity, strong penetration depth | Poor spatial resolution, radiation risk |
SPECT | Molecular | High sensitivity, strong penetration depth | Poor spatial resolution, radiation risk |
US | Anatomical | High sensitivity, low cost, fast acquisition | Poor spatial resolution |
MRI–optical imaging | Anatomical/molecular | High sensitivity, high spatial resolution, no tissue penetration limit | High cost |
MRI–CT | Anatomical | High spatial resolution, no tissue penetration limit | Radiation risk, high cost, low sensitivity |
MRI–PET/SPECT | Anatomical/molecular | High spatial resolution, high sensitivity, no tissue penetration limit | Radiation risk, high cost |
MRI–US | Anatomical | High spatial resolution, no tissue penetration limit, high sensitivity | High cost |
Association | |||
---|---|---|---|
Nanoparticles | Optical Agent | Application | Reference |
Iron oxide | Quantum dot | Cervical cancer | [77] |
Iron oxide | Quantum dot | Cervical cancer and neural cells | [75] |
Iron oxide | Carbon dots | Cervical cancer | [76] |
Silica with iron oxide nanoparticles | Rhodamine dye | Neuroblastoma | [78] |
Encapsulation | |||
Nanoparticles | Optical Agent | Application | Reference |
Silica with iron oxide nanoparticles | Rhodamine dye | Neuroblastoma | [78] |
Mesoporous silica nanoparticles (MSNs) with Gd-DTPA | Heptamethine dye (IR-808) | Glioblastoma | [79] |
Silica with iron oxide nanoparticles | Quantum dots | Mammary carcinoma | [80] |
Dispersion | |||
Nanoparticles | Optical Agent | Application | Reference |
Copolyarylene ether nitriles with iron oxide nanoparticles | Quantum dots | Mammary carcinoma | [81] |
Ethylene oxide polymer vesicles and iron oxide nanoparticles | (7-Diethylamino coumarin)-3-carboxyic acid (DEAC-CA) | Cervical cancer | [82] |
Polymeric micelles and MnFe2O4 magnetic nanoparticles | Quantum dots | Glioblastoma | [83] |
Polymeric matrix with iron oxide nanoparticles | Chlorin e6 dye (Ce6) | Colon cancer | [84] |
Liposome with iron oxide nanoparticles | Texas Red dye | Ovarian cancer | [85] |
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Luengo Morato, Y.; Ovejero Paredes, K.; Lozano Chamizo, L.; Marciello, M.; Filice, M. Recent Advances in Multimodal Molecular Imaging of Cancer Mediated by Hybrid Magnetic Nanoparticles. Polymers 2021, 13, 2989. https://doi.org/10.3390/polym13172989
Luengo Morato Y, Ovejero Paredes K, Lozano Chamizo L, Marciello M, Filice M. Recent Advances in Multimodal Molecular Imaging of Cancer Mediated by Hybrid Magnetic Nanoparticles. Polymers. 2021; 13(17):2989. https://doi.org/10.3390/polym13172989
Chicago/Turabian StyleLuengo Morato, Yurena, Karina Ovejero Paredes, Laura Lozano Chamizo, Marzia Marciello, and Marco Filice. 2021. "Recent Advances in Multimodal Molecular Imaging of Cancer Mediated by Hybrid Magnetic Nanoparticles" Polymers 13, no. 17: 2989. https://doi.org/10.3390/polym13172989