Magnetic nanoparticles for MRI of brain tumors

Current Pharmaceutical Biotechnology

Volumn 13, Issue 12, 2012, Pages 2403-2416

  Wang, Jianxin ^a,b   Huang, Yongzhuo ^b,c   David, Allan E ^b   Chertok, Beata ^b   Zhang, Lei ^b   Yu, Faquan ^b   Yang, Victor C ^b,d  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF MICHIGAN   (United States)

^c SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^d TIANJIN UNIVERSITY   (China)

Author keywords

Brain tumors; Imaging; Iron oxide nanoparticles; MRI; Targeting

Indexed keywords

AMINOLEVULINIC ACID; FLUORESCEIN SODIUM; FLUORINE 18; FLUORODEOXYGLUCOSE F 18; GADOLINIUM; INDOCYANINE GREEN; IODINE 123; IODINE 125; LOW MOLECULAR WEIGHT HEPARIN; MONOCRYSTALLINE IRON OXIDE NANOPARTICLE; NITROGEN 13; OXYGEN 15; QUANTUM DOT; TECHNETIUM 99M; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE;

AREA UNDER THE CURVE; BRAIN TUMOR; CANCER PROGNOSIS; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; DRUG ACCUMULATION; DRUG BLOOD LEVEL; FLUORESCENCE MICROSCOPY; HUMAN; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; ULTRASOUND;

ANIMALS; BRAIN DISEASES; CONTRAST MEDIA; DIAGNOSTIC IMAGING; FERUMOXYTOL; HUMANS; NANOPARTICLES;

EID: 84867723306     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920112803341824     Document Type: Review

References (103)

1. Nathoo, N.; Toms, S.A.;Barnett, G.H. Metastases to the brain: current management perspectives. Expert Rev. Neurother., 2004, 4, 633-640.
2. American Cancer Society. Cancer Facts and Figures 2004, 2004.
3. Mason, W.P.;Cairncross, J.G. Drug insight: temozolomide as a treatment for malignant glioma--impact of a recent trial. Nat. Clin. Pract. Neurol., 2005, 1, 88-95.
4. Dancey, G.; Begent, R.H.;Meyer, T. Imaging in targeted delivery of therapy to cancer. Target Oncol., 2009, 4, 201-17.
5. Fass, L. Imaging and cancer: a review. Mol. Oncol., 2008, 2, 115-152.
6. Te Velde, E.A.; Veerman, T.; Subramaniam, V.; Ruers, T. The use of fluorescent dyes and probes in surgical oncology. Eur. J Surg. Oncol., 2010, 36, 6-15.
7. Maniatis, V.; Chrysikopoulos, H.;Roussakis, A. CT imaging of the "target sign" in brain metastases. Eur. Radiol., 2001, 11, 903-904.
8. Panigrahy, A.;Bluml, S. Neuroimaging of pediatric brain tumors: from basic to advanced magnetic resonance imaging (MRI). J. Child Neurol., 2009, 24, 1343-1365.
9. van Velthoven, V. Intraoperative ultrasound imaging: comparison of pathomorphological findings in US versus CT, MRI and intraoperative findings. Acta. Neurochir. Suppl., 2003, 85, 95-99.
10. Renner, C.; Lindner, D.; Schneider, J.P.;Meixensberger, J. Evaluation of intra-operative ultrasound imaging in brain tumor resection: a prospective study. Neurol. Res., 2005, 27, 351-357.
11. Hayat, M.A. Cancer imaging: lung and breast carcinomas, Elsevier Academic Press: Burlington: 2008.
12. Wong, T.Z.; van der Westhuizen, G. J.; Coleman, R.E. Positron emission tomography imaging of brain tumors. Neuroimaging Clin. N. Am., 2002, 12, 615-626.
13. Newberg, A.B.; Alavi, A. The role of PET imaging in the management of patients with central nervous system disorders. Radiol. Clin. North Am., 2005, 43, 49-65.
14. Filippi, L.; Schillaci, O.; Santoni, R.; Manni, C.; Danieli, R.;Simonetti, G. Usefulness of SPECT/CT with a hybrid camera for the functional anatomical mapping of primary brain tumors by [Tc99m]tetrofosmin. Cancer Biother. Radiopharm., 2006, 21, 41-48.
15. Luker, G.D.; Luker, K.E. Optical imaging: current applications and future directions. J. Nucl. Med., 2008, 49, 1-4.
16. Raabe, A.; Beck, J.; Gerlach, R.; Zimmermann, M.;Seifert, V. Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery., 2003, 52, 132-139; discussion 139.
17. Haglund, M.M.; Hochman, D.W.; Spence, A.M.;Berger, M.S. Enhanced optical imaging of rat gliomas and tumor margins. Neurosurgery., 1994, 35, 930-40; discussion 940-941.
18. Haglund, M.M.; Berger, M.S.; Hochman, D.W. Enhanced optical imaging of human gliomas and tumor margins. Neurosurgery., 1996, 38, 308-317.
19. Ruge, J.R.; Liu, J. Use of 5-aminolevulinic acid for visualization and resection of a benign pediatric brain tumor. J. Neurosurg. Pediatr., 2009, 4, 484-486.
20. Friesen, S.A.; Hjortland, G.O.; Madsen, S.J.; Hirschberg, H.; Engebraten, O.; Nesland, J.M.; Peng, Q. 5-Aminolevulinic acidbased photodynamic detection and therapy of brain tumors (review). Int. J. Oncol., 2002, 21, 577-582.
21. Okuda, T.; Kataoka, K.; Yabuuchi, T.; Yugami, H.; Kato, A. Fluorescence-guided surgery of metastatic brain tumors using fluorescein sodium. J. Clin. Neurosci., 2010, 17, 118-121.
22. Ichioka, T.; Miyatake, S.; Asai, N.; Kajimoto, Y.; Nakagawa, T.; Hayashi, H.;Kuroiwa, T. Enhanced detection of malignant glioma xenograft by fluorescein-human serum albumin conjugate. J. Neurooncol., 2004, 67, 47-52.
23. Nioka, S.; Chance, B. NIR spectroscopic detection of breast cancer. Technol. Cancer. Res. Treat., 2005, 4, 497-512.
24. Becker, A.; Hessenius, C.; Licha, K.; Ebert, B.; Sukowski, U.; Semmler, W.; Wiedenmann, B.; Grotzinger, C. Receptor-targeted optical imaging of tumors with near-infrared fluorescent ligands. Nat. Biotechnol., 2001, 19, 327-331.
25. Smith, A.M.; Duan, H.; Mohs, A.M.; Nie, S. Bioconjugated quantum dots for in vivo molecular and cellular imaging. Adv. Drug Deliv. Rev., 2008, 60, 1226-1240.
26. Alivisatos, A.P. Semiconductor clusters, nanocrystals, and quantum dots. Science, 1996, 271, 933-937.
27. Gao, X.; Chen, J.; Wu, B.; Chen, H.; Jiang, X. Quantum dots bearing lectin-functionalized nanoparticles as a platform for in vivo brain imaging. Bioconjug. Chem., 2008, 19, 2189-2195.
28. Wang, J.; Yong, W.H.; Sun, Y.; Vernier, P.T.; Koeffler, H.P.; Gundersen, M.A.;Marcu, L. Receptor-targeted quantum dots: fluorescent probes for brain tumor diagnosis. J. Biomed. Opt., 2007, 12, 044021.
29. Ghoroghchian, P.P.; Frail, P.R.; Susumu, K.; Blessington, D.; Brannan, A.K.; Bates, F.S.; Chance, B.; Hammer, D.A.;Therien, M.J. Near-infrared-emissive polymersomes: self-assembled soft matter for in vivo optical imaging. Proc. Natl. Acad. Sci. USA, 2005, 102, 2922-2927.
30. Kirchner, C.; Liedl, T.; Kudera, S.; Pellegrino, T.; Munoz Javier, A.; Gaub, H.E.; Stolzle, S.; Fertig, N.; Parak, W.J. Cytotoxicity of colloidal CdSe and CdSe/ZnS nanoparticles. Nano. Lett., 2005, 5, 331-8.
31. Dubertret, B.; Skourides, P.; Norris, D.J.; Noireaux, V.; Brivanlou, A.H.; Libchaber, A. In vivo imaging of quantum dots encapsulated in phospholipid micelles. Science, 2002, 298, 1759-1762.
32. Stroh, M.; Zimmer, J.P.; Duda, D.G.; Levchenko, T.S.; Cohen, K.S.; Brown, E.B.; Scadden, D.T.; Torchilin, V.P.; Bawendi, M.G.; Fukumura, D.; Jain, R.K. Quantum dots spectrally distinguish multiple species within the tumor milieu in vivo. Na. t Med., 2005, 11, 678-682.
33. Jaiswal, J.K.; Mattoussi, H.; Mauro, J.M.; Simon, S.M. Long-term multiple color imaging of live cells using quantum dot bioconjugates. Nat. Biotechnol., 2003, 21, 47-51.
34. Kim, S.W.; Zimmer, J.P.; Ohnishi, S.; Tracy, J.B.; Frangioni, J.V.; Bawendi, M.G. Engineering InAs(x)P(1-x)/InP/ZnSe III-V alloyed core/shell quantum dots for the near-infrared. J. Am. Chem. Soc., 2005, 127, 10526-10532.
35. Weissleder, R. Molecular imaging in cancer. Science, 2006, 312, 1168-1171.
36. Rutten, G.J.; Ramsey, N.F. The role of functional magnetic resonance imaging in brain surgery. Neurosurg. Focus., 2010, 28, E4.
37. Haacke, E.M.; Brown, R.W.; Thompson, M.R.; Venkatesan, R. Magnetic resonance imaging: physical principles and sequence design, Wiley: New York: 1999.
38. Kozlowska, D.; Foran, P.; MacMahon, P.; Shelly, M.J.; Eustace, S.; O'Kennedy, R. Molecular and magnetic resonance imaging: The value of immunoliposomes. Adv. Drug Deliv. Rev., 2009, 61, 1402-1411.
39. Caravan, P.; Ellison, J.J.; McMurry, T.J.; Lauffer, R. B. Gadolinium(III) Chelates as MRI contrast agents: structure, dynamics, and applications. Chem. Rev., 1999, 99, 2293-352.
40. Sun, C.; Lee, J.S.H.;Zhang, M.Q. Magnetic nanoparticles in MR imaging and drug delivery. Adv. Drug Deliv. Rev., 2008, 60, 1252-1265.
41. Wang, Y.X.; Hussain, S.M.;Krestin, G.P. Superparamagnetic iron oxide contrast agents: physicochemical characteristics and applications in MR imaging. Eur. Radiol., 2001, 11, 2319-2331.
42. Neuwelt, E.A.; Varallyay, P.; Bago, A.G.; Muldoon, L.L.; Nesbit, G.;Nixon, R. Imaging of iron oxide nanoparticles by MR and light microscopy in patients with malignant brain tumours. Neuropathol. Appl. Neurobiol., 2004, 30, 456-471.
43. Benderbous, S.; Corot, C.; Jacobs, P.;Bonnemain, B. Superparamagnetic agents: physicochemical characteristics and preclinical imaging evaluation. Acad. Radiol., 1996, 3 (Suppl. 2), S292-4.
44. Murillo, T.P.; Sandquist, C.; Jacobs, P.M.; Nesbit, G.; Manninger, S.; Neuwelt, E.A. Imaging brain tumors with ferumoxtran-10, a nanoparticle magnetic resonance contrast agent. Therapy, 2005, 2, 871-882.
45. Enochs, W.S.; Harsh, G.; Hochberg, F.; Weissleder, R. Improved delineation of human brain tumors on MR images using a longcirculating, superparamagnetic iron oxide agent. J. Magn. Reson. Imaging, 1999, 9, 228-232.
46. Saravanakumar, G.; Kim, K.; Park, J.H.; Rhee, K.; Kwon, I.C. Current status of nanoparticle-based imaging agents for early diagnosis of cancer and atherosclerosis. J. Biomed. Nanotechnol., 2009, 5, 20-35.
47. Lanza, G.M.; Winter, P.; Caruthers, S.; Schmeider, A.; Crowder, K.; Morawski, A.; Zhang, H.; Scott, M.J.;Wickline, S.A. Novel paramagnetic contrast agents for molecular imaging and targeted drug delivery. Curr. Pharm. Biotechnol., 2004, 5, 495-507.
48. Kozlowska, D.; Foran, P.; MacMahon, P.; Shelly, M.J.; Eustace, S.;O'Kennedy, R. Molecular and magnetic resonance imaging: The value of immunoliposomes. Adv. Drug Deliv. Rev., 2009, 61, 1402-1411.
49. DeAngelis, L.M. Medical progress: Brain tumors. N. Engl. J. Med., 2001, 344, 114-123.
50. Tartaj, P.; Morales, M.D.; Veintemillas-Verdaguer, S.; Gonzalez-Carreno, T.; Serna, C.J. The preparation of magnetic nanoparticles for applications in biomedicine. J. Phys. D Appl. Phys., 2003, 36, R182-R197.
51. Bjornerud, A.; Johansson, L. The utility of superparamagnetic contrast agents in MRI: theoretical consideration and applications in the cardiovascular system. NMR Biomed., 2004, 17, 465-477.
52. Jun, Y.W.; Jang, J.T.;Cheon, J. In: Nanomaterials for cancer diagnosis, Kumar, C., ed.; WILEY-VCH: Weinheim, 2007, pp. 148.
53. Hafeli, U.O.; Lobedann, M.A.; Steingroewer, J.; Moore, L.R.; Riffle, J. Optical method for measurement of magnetophoretic mobility of individual magnetic microspheres in defined magnetic field. J. Magn. Magn. Mater., 2005, 293, 224-239.
54. Yu, F.Q.; Zhang, L.; Huang, Y.Z.; Sun, K.; David, E.A.; Yang, V.C. The magnetophoretic mobility and superparamagnetism of core-shell iron oxide nanoparticles with dual targeting and imaging functionality. Biomaterials, 2010, 22, 5842-5848.
55. Chertok, B.; David, A.E.; Huang, Y.Z.; Yang, V.C. Glioma selectivity of magnetically targeted nanoparticles: A role of abnormal tumor hydrodynamics. J. Control Release., 2007, 122, 315-323.
56. Laurent, S.; Forge, D.; Port, M.; Roch, A.; Robic, C.; Elst, L.V.; Muller, R.N. Magnetic iron oxide nanoparticles: Synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem. Rev., 2008, 108, 2064-2110.
57. Kattumuri, V.; Katti, K.; Bhaskaran, S.; Boote, E.J.; Casteel, S.W.; Fent, G.M.; Robertson, D.J.; Chandrasekhar, M.; Kannan, R.; Katti, K.V. Gum arabic as a phytochemical construct for the stabilization of gold nanoparticles: in vivo pharmacokinetics and X-ray-contrastimaging studies. Small, 2007, 3, 333-341.
58. Fent, G.M.; Casteel, S.W.; Kim, D.Y.; Kannan, R.; Katti, K.;Chanda, N. Biodistribution of maltose and gum arabic hybrid gold nanoparticles after intravenous injection in juvenile swine. Nanomedicine, 2009, 5, 128-135.
59. Williams, D.; Gold, K.; Holoman, T.; Ehrman, S.; Wilson, O. Surface modification of magnetic nanoparticles using gum arabic. J. Nanopart Res., 2006, 8, 749-753.
60. Zhang, L.; Yu, F.; Cole, A.J.; Chertok, B.; David, A.E.; Wang, J.; Yang, V.C. Gum arabic-coated magnetic nanoparticles for potential application in simultaneous magnetic targeting and tumor imaging. AAPS J., 2009, 11, 693-699.
61. Gil, E.S.; Li, J.; Xiao, H.; Lowe, T.L. Quaternary ammonium betacyclodextrin nanoparticles for enhancing doxorubicin permeability across the in vitro blood-brain barrier. Biomacromolecules, 2009.
62. Lu, W.; Sun, Q.; Wan, J.; She, Z.; Jiang, X.G. Cationic albuminconjugated pegylated nanoparticles allow gene delivery into brain tumors via intravenous administration. Cancer Res., 2006, 66, 11878-11887.
63. Zhou, J.H.; Huang, L.; Wang, W.W.; Pang, J.; Zou, Y.; Shuai, X.T.; Gao, X. Prostate cancer targeted MRI nanoprobe based on superparamagnetic iron oxide and copolymer of poly(ethylene glycol) and polyethyleneimin. Chin. Sci. Bull., 2009, 54, 3137-3146.
64. Benns, J.M.; Choi, J.S.; Mahato, R.I.; Park, J.S.; Kim, S.W. pHsensitive cationic polymer gene delivery vehicle: N-Ac-poly(Lhistidine)-graft-poly(L-lysine) comb shaped polymer. Bioconjug. Chem., 2000, 11, 637-645.
65. Choi, J.S.; MacKay, J.A.; Szoka, F.C., Jr. Low-pH-sensitive PEGstabilized plasmid-lipid nanoparticles: preparation and characterization. Bioconjug. Chem., 2003, 14, 420-429.
66. Li, W.; Huang, Z.; MacKay, J.A.; Grube, S.; Szoka, F.C., Jr. LowpH-sensitive poly(ethylene glycol) (PEG)-stabilized plasmid nanolipoparticles: effects of PEG chain length, lipid composition and assembly conditions on gene delivery. J. Gene Med., 2005, 7, 67-79.
67. Xiong, M.P.; Bae, Y.; Fukushima, S.; Forrest, M.L.; Nishiyama, N.; Kataoka, K.; Kwon, G.S. pH-responsive Multi-PEGylated dual cationic nanoparticles enable charge modulations for safe gene delivery. ChemMedChem., 2007, 2, 1321-1327.
68. Kwon, Y.M.; Li, Y.T.; Liang, J.F.; Park, Y.J.; Chang, L.C.; Yang, V.C. PTD-modified ATTEMPTS system for enhanced asparaginase therapy: a proof-of-concept investigation. J. Control Release., 2008, 130, 252-258.
69. Huang, Y.Z.; Park, Y.S.; Wang, J.X.; Moon, C.; Kwon, Y.M.; Park, Y.J.;Yang, V.C. ATTEMPTS system: a macromolecular prodrug strategy for cancer drug delivery. Curr. Pharm. Des., 2010, 16(21),2369-2376.
70. Li, Y.T.; Kwon, Y.M.; Spangrude, G.J.; Liang, J.F.; Chung, H.S.; Park, Y.J.; Yang, V.C. Preliminary in vivo evaluation of the protein transduction domain-modified ATTEMPTS approach in enhancing asparaginase therapy. J. Biomed. Mater Res. A., 2009, 91, 209-220.
71. Moon, C.; Kwon, Y.M.; Lee, W.K.; Park, Y.J.; Chang, L.C.; Yang, V.C. A novel polyrotaxane-based intracellular delivery system for camptothecin: in vitro feasibility evaluation. J. Biomed. Mater Res. A., 2008, 84, 238-246.
72. Park, Y.J.; Liang, J.F.; Song, H.; Li, Y.T.; Naik, S.; Yang, V.C. ATTEMPTS: a heparin/protamine-based triggered release system for the delivery of enzyme drugs without associated side-effects. Adv. Drug Deliv. Rev., 2003, 55, 251-265.
73. Chertok, B.; David, A.E.; Moffat, B.A.; Yang, V.C. Substantiating in vivo magnetic brain tumor targeting of cationic iron oxide nanocarriers via adsorptive surface masking. Biomaterials, 2009, 30, 6780-6787.
74. Suh, J.S.; Lee, J.Y.; Choi, Y.S.; Yu, F.; Yang, V.; Lee, S.J.; Chung, C.P.; Park, Y.J. Efficient labeling of mesenchymal stem cells using cell permeable magnetic nanoparticles. Biochem. Biophys. Res. Commun., 2009, 379, 669-675.
75. Veiseh, O.; Gunn, J. W.; Zhang, M.Q. Design and fabrication of magnetic nanoparticles for targeted drug delivery and imaging. Adv. Drug. Deliv. Rev., 2010, 62, 284-304.
76. Shi, Z.L.; Neoh, K.G.; Kang, E.T.; Shuter, B.; Wang, S.C.; Poh, C.; Wan, W. (Carboxymethyl) chitosan-modified superparamagnetic iron oxide nanoparticles for magnetic resonance imaging of stem cells. ACS. Appl. Mater Interfaces., 2009, 1, 328-335.
77. Bae, K.H.; Ha, Y.J.; Kim, C.; Lee, K.R.; Park, T.G. Pluronic/chitosan shell cross-linked nanocapsules encapsulating magnetic nanoparticles. J. Biomater. Sci. Polym. Ed., 2008, 19, 1571-1583.
78. Mahmoudi, M.; Simchi, A.; Imani, M.; Milani, A.S.; Stroeve, P. Optimal design and characterization of superparamagnetic iron oxide nanoparticles coated with polyvinyl alcohol for targeted delivery and imaging. J. Phys. Chem. B., 2008, 112, 14470-14481.
79. Babic, M.; Horak, D.; Trchova, M.; Jendelova, P.; Glogarova, K.; Lesny, P.; Herynek, V.; Hajek, M.; Sykova, E. Poly(L-lysine)-modified iron oxide nanoparticles for stem cell labeling. Bioconjug. Chem., 2008, 19, 740-750.
80. Okassa, L.N.; Marchais, H.; Douziech-Eyrolles, L.; Cohen-Jonathan, S.; Souce, M.; Dubois, P.; Chourpa, I. Development and characterization of sub-micron poly(D, L-lactide-co-glycolide) particles loaded with magnetite/maghemite nanoparticles. Int. J. Pharm., 2005, 302, 187-196.
81. Okassa, L.N.; Marchais, H.; Douziech-Eyrolles, L.; Herve, K.; Cohen-Jonathan, S.; Munnier, E.; Souce, M.; Linassier, C.; Dubois, P.; Chourpa, I. Optimization of iron oxide nanoparticles encapsulation within poly(D, L-lactide-co-glycolide) sub-micron particles. Eur. J. Pharm. Biopharm., 2007, 67, 31-38.
82. Gupta, A.K.; Naregalkar, R.R.; Vaidya, V.D.; Gupta, M. Recent advances on surface engineering of magnetic iron oxide nanoparticles and their biomedical applications. Nanomedicine, 2007, 2, 23-39.
83. Gupta, A.K.;Gupta, M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials., 2005, 26, 3995-4021.
84. Lu, J.; Ma, S.L.; Sun, J.Y.; Xia, C.C.; Liu, C.; Wang, Z.Y.; Zhao, X.N.; Gao, F.B.; Gong, Q.Y.; Song, B.; Shuai, X.T.; Ai, H.; Gu, Z.W. Manganese ferrite nanoparticle micellar nanocomposites as MRI contrast agent for liver imaging. Biomaterials, 2009, 30, 2919-2928.
85. Maeda, H.; Wu, J.; Sawa, T.; Matsumura, Y.; Hori, K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J. Control Release, 2000, 65, 271-284.
86. Chertok, B.; Moffat, B.A.; David, A.E.; Yu, F.Q.; Bergemann, C.; Ross, B.D.; Yang, V.C. Iron oxide nanoparticles as a drug delivery vehicle for MRI monitored magnetic targeting of brain tumors. Biomaterials, 2008, 29, 487-496.
87. Jiang, X.G.; Lu, W. In: Nanotechnology-based drug delivery systems targeting to glioma, American Association of Pharmaceutical Scientists (AAPS) Annual Meeting, Los Angeles, California, USA, 2009.
88. Mahmoudi, M.; Simchi, A.; Milani, A.S.; Stroeve, P. Cell toxicity of superparamagnetic iron oxide nanoparticles. J. Colloid Interface Sci., 2009, 336, 510-518.
89. Muldoon, L.L.; Sandor, M.; Pinkston, K.E.; Neuwelt, E.A. Imaging, distribution, and toxicity of superparamagnetic iron oxide magnetic resonance nanoparticles in the rat brain and intracerebral tumor. Neurosurgery, 2005, 57, 785-796; discussion 785-796.
90. Liu, S.; Han, Y.; Yin, L.; Long, L.; Liu, R. Toxicology studies of a superparamagnetic iron oxide nanoparticle in vivo. Adv. Materials Res., 2008, 47-50, 1097-1100.
91. Dousset, V.; Delalande, C.; Ballarino, L.; Quesson, B.; Seilhan, D.; Coussemacq, M.; Thiaudiere, E.; Brochet, B.; Canioni, P.; Caille, J.M. In vivo macrophage activity imaging in the central nervous system detected by magnetic resonance. Magn. Reson. Med., 1999, 41, 329-333.
92. Rausch, M.; Sauter, A.; Fröhlich, J.; Neubacher, U.; Radü, E.W.; Rudin, M. Dynamic patterns of USPIO enhancement can be observed in macrophages after ischemic brain damage. Magn. Reson. Med., 2001, 46, 1018-1022.
93. Dirnagl, U.; Iadecola, C.; Moskowitz, M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci., 1999, 22, 391-397.
94. Becker, K.J. Targeting the central nervous system inflammatory response in ischemic stroke. Curr. Opin. Neurol., 2001, 14, 349-353.
95. Jander, S.; Schroeter, M.; Saleh, A. Imaging inflammation in acute brain ischemia. Stroke, 2007, 38(Suppl. 2), 642-645.
96. Saleh, A.; Wiedermann, D.; Schroeter, M.; Jonkmanns, C.; Jander, S.; Hoehn, M. Central nervous system inflammatory response after cerebral infarction as detected by magnetic resonance imaging. NMR Biomed., 2004, 17, 163-169.
97. Saleh, A.; Schroeter, M.; Jonkmanns, C.; Hartung, H.P.; Mödder, U.; Jander, S. In vivo MRI of brain inflammation in human ischaemic stroke. Brain, 2004, 127, 1670-1677.
98. Saleh, A.; Schroeter, M.; Ringelstein, A.; Hartung, H.P.; Siebler, M.; Mödder. U.; Jander, S. Iron oxide particle-enhanced MRI suggests variability of brain inflammation at early stages after ischemic stroke. Stroke, 2007, 38, 2733-2737.
99. Xu, S.; Jordan, E.; Brocke, S.; Bulte, J.W.; Quigley, L.; Tresser, N.; Ostuni, J.L.; Yang, Y.; McFarland, H.F.; Frank, J.A. Study of relapsing remitting experimental allergic encephalomyelitis SJL mouse model using MION-46L enhanced in vivo MRI: early histopathological correlation. J. Neurosci. Res., 1998, 52, 549-558.
100. 1-weighted MR images in rats with experimental autoimmune encephalomyelitis. Am. J. Neuroradiol., 1999, 20, 223-227.
101. Floris, S.; Blezer, E.L.; Schreibelt, G.; Döpp, E.; van der Pol, S.M.; Schadee-Eestermans, I.L.; Nicolay, K.; Dijkstra, C.D.; de Vries, H.E. Blood-brain barrier permeability and monocyte infiltration in experimental allergic encephalomyelitis. Brain, 2004, 127(Pt 3), 616-627.
102. Rausch, M.; Hiestand, P.; Baumann, D.; Cannet, C.; Rudin, M. MRIbased monitoring of inflammation and tissue damage in acute and chronic relapsing EAE. Magn. Reson. Med., 2003, 50, 309-314.
103. Corot, C.; Petry, K.G.; Trivedi, R.; Saleh, A.; Jonkmanns, C.; Le Bas, J.F.; Blezer, E.; Rausch, M.; Brochet, B.; Foster-Gareau, P.; Balériaux, D.; Gaillard, S.; Dousset, V. Macrophage imaging in central nervous system and in carotid atherosclerotic plaque using ultrasmall superparamagnetic iron oxide in magnetic resonance imaging. Invest. Radiol., 2004, 39, 619-625.