Clinical applications of iron oxide nanoparticles for magnetic resonance imaging of brain tumors

Nanomedicine

Volumn 10, Issue 6, 2015, Pages 993-1008

  Iv, Michael ^a   Telischak, Nicholas ^a   Feng, Dan ^a   Holdsworth, Samantha J ^b   Yeom, Kristen W ^a   Daldrup Link, Heike E ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

brain tumor; ferucarbotran; ferumoxtran; ferumoxytol; macrophage; MRI; ultrasmall superparamagnetic iron oxide nanoparticles

Indexed keywords

FERUCARBOTRAN; FERUMOXYTOL; MONOCRYSTALLINE IRON OXIDE NANOPARTICLE; SUPERPARAMAGNETIC IRON OXIDE; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE; FERRIC ION; FERRIC OXIDE; MAGNETITE; METAL NANOPARTICLE;

BRAIN TUMOR; DEVICE SAFETY; GLIOBLASTOMA; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REVIEW; ANIMAL; BRAIN NEOPLASMS; CANCER TRANSPLANTATION; CHEMISTRY; DIAGNOSTIC USE; GLIOMA; NANOMEDICINE; PATIENT SAFETY; PROCEDURES; PROGNOSIS; RAT; TRENDS;

ANIMALS; BRAIN NEOPLASMS; FERRIC COMPOUNDS; FERROSOFERRIC OXIDE; GLIOMA; HUMANS; MAGNETIC RESONANCE IMAGING; METAL NANOPARTICLES; NANOMEDICINE; NEOPLASM TRANSPLANTATION; PATIENT SAFETY; PROGNOSIS; RATS;

EID: 84928167324     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.14.203     Document Type: Review

References (147)

1. Cha S. Update on brain tumor imaging: from anatomy to physiology. Am. J. Neuroradiol. 27(3), 475-487 (2006).
2. Thakor AS, Gambhir SS. Nanooncology: the future of cancer diagnosis and therapy. CA Cancer J. Clin. 63(6), 395-418 (2013).
3. Provenzale JM, Silva GA. Uses of nanoparticles for central nervous system imaging and therapy. Am. J. Neuroradiol. 30(7), 1293-1301 (2009).
4. Meyers JD, Doane T, Burda C, Basilion JP. Nanoparticles for imaging and treating brain cancer. Nanomedicine 8(1), 123-143 (2013).
5. Kono K, Inoue Y, Nakayama K et al. The role of diffusion-weighted imaging in patients with brain tumors. Am. J. Neuroradiol. 22(6), 1081-1088 (2001).
6. Yu CS, Li KC, Xuan Y, Ji XM, Qin W. Diffusion tensor tractography in patients with cerebral tumors: a helpful technique for neurosurgical planning and postoperative assessment. Eur. J. Radiol. 56(2), 197-204 (2005).
7. Law M, Young RJ, Babb JS et al. Gliomas: predicting time to progression or survival with cerebral blood volume measurements at dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. Radiology 247(2), 490-498 (2008).
8. Bulakbasi N, Kocaoglu M, Farzaliyev A, Tayfun C, Ucoz T, Somuncu I. Assessment of diagnostic accuracy of perfusion MR imaging in primary and metastatic solitary malignant brain tumors. Am. J. Neuroradiol. 26(9), 2187-2199 (2005).
9. Roberts HC, Roberts TP, Brasch RC, Dillon WP. Quantitative measurement of microvascular permeability in human brain tumors achieved using dynamic contrast-enhanced MR imaging: correlation with histologic grade. Am. J. Neuroradiol. 21(5), 891-899 (2000).
10. Astrakas LG, Zurakowski D, Tzika AA et al. Noninvasive magnetic resonance spectroscopic imaging biomarkers to predict the clinical grade of pediatric brain tumors. Clin. Cancer Res. 10(24), 8220-8228 (2004).
11. Cheng Y, Morshed RA, Auffinger B, Tobias AL, Lesniak MS. Multifunctional nanoparticles for brain tumor imaging and therapy. Adv. Drug Deliv. Rev. 66, 42-57 (2014).
12. Covarrubias DJ, Rosen BR, Lev MH. Dynamic magnetic resonance perfusion imaging of brain tumors. Oncologist 9(5), 528-537 (2004).
13. Earnest FT, Kelly PJ, Scheithauer BW et al. Cerebral astrocytomas: histopathologic correlation of MR and CT contrast enhancement with stereotactic biopsy. Radiology 166(3), 823-827 (1988).
14. Nie G, Hah HJ, Kim G et al. Hydrogel nanoparticles with covalently linked coomassie blue for brain tumor delineation visible to the surgeon. Small 8(6), 884-891 (2012).
15. Spickler EM, Dion JE, Lufkin RB et al. The MR appearance of endovascular embolic agents in vitro with clinical correlation. Comp. Med. Imaging Graph. 14(6), 415-423 (1990).
16. Forsting M, Albert FK, Kunze S, Adams HP, Zenner D, Sartor K. Extirpation of glioblastomas: MR and CT follow-up of residual tumor and regrowth patterns. Am. J. Neuroradiol. 14(1), 77-87 (1993).
17. Spiller M, Tenner MS, Couldwell WT. Effect of absorbable topical hemostatic agents on the relaxation time of blood: an in vitro study with implications for postoperative magnetic resonance imaging. J. Neurosurg. 95(4), 687-693 (2001).
18. Benderbous S, Corot C, Jacobs P, Bonnemain B. Superparamagnetic agents: physicochemical characteristics and preclinical imaging evaluation. Acad. Radiol. 3(Suppl. 2), S292-S294 (1996).
19. Varallyay P, Nesbit G, Muldoon LL et al. Comparison of two superparamagnetic viral-sized iron oxide particles ferumoxides and ferumoxtran-10 with a gadolinium chelate in imaging intracranial tumors. Am. J. Neuroradiol. 23(4), 510-519 (2002).
20. Beckmann N, Cannet C, Babin AL et al. In vivo visualization of macrophage infiltration and activity in inflammation using magnetic resonance imaging. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 1(3), 272-298 (2009).
21. Corot C, Robert P, Idee JM, Port M. Recent advances in iron oxide nanocrystal technology for medical imaging. Adv. Drug Deliv. Rev. 58(14), 1471-1504 (2006).
22. Giesel FL, Mehndiratta A, Essig M. High-relaxivity contrast-enhanced magnetic resonance neuroimaging: a review. Eur. Radiol. 20(10), 2461-2474 (2010).
23. Cotton F, Hermier M. The advantage of high relaxivity contrast agents in brain perfusion. Eur. Radiol. 16(Suppl. 7), M16-M26 (2006).
24. Simon GH, Von Vopelius-Feldt J, Fu Y et al. Ultrasmall supraparamagnetic iron oxide-enhanced Magn. Reson. Imaging of antigen-induced arthritis: a comparative study between SHU 555 C, ferumoxtran-10, and ferumoxytol. Invest. Radiol. 41(1), 45-51 (2006).
25. Jung CW, Jacobs P. Physical and chemical properties of superparamagnetic iron oxide MR contrast agents: ferumoxides, ferumoxtran, ferumoxsil. Magn. Reson. Imaging 13(5), 661-674 (1995).
26. Daldrup-Link HE, Golovko D, Ruffell B et al. MRI of tumor-associated macrophages with clinically applicable iron oxide nanoparticles. Clin. Cancer Res. 17(17), 5695-5704 (2011).
27. Harisinghani MG, Barentsz J, Hahn PF et al. Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N. Engl. J. Med. 348(25), 2491-2499 (2003).
28. Anzai Y, Piccoli CW, Outwater EK et al. Evaluation of neck and body metastases to nodes with ferumoxtran 10-enhanced MR imaging: phase III safety and efficacy study. Radiology 228(3), 777-788 (2003).
29. Heesakkers RA, Futterer JJ, Hovels AM et al. Prostate cancer evaluated with ferumoxtran-10-enhanced T2∗-weighted MR Imaging at 1.5 and 3.0 T: early experience. Radiology 239(2), 481-487 (2006).
30. Heesakkers RA, Hovels AM, Jager GJ et al. MRI with a lymph-node-specific contrast agent as an alternative to CT scan and lymph-node dissection in patients with prostate cancer: a prospective multicohort study. Lancet Oncol. 9(9), 850-856 (2008).
31. Neuwelt EA, Varallyay CG, Manninger S et al. The potential of ferumoxytol nanoparticle magnetic resonance imaging, perfusion, and angiography in central nervous system malignancy: a pilot study. Neurosurgery 60(4), 601-611; discussion 611-602 (2007).
32. Lu M, Cohen MH, Rieves D, Pazdur R. FDA report: Ferumoxytol for intravenous iron therapy in adult patients with chronic kidney disease. Am. J. Hematol. 85(5), 315-319 (2010).
33. Daldrup-Link H, Coussens LM. MR imaging of tumor-associated macrophages. Oncol. Immunol. 1(4), 507-509 (2012).
34. Stabi KL, Bendz LM. Ferumoxytol use as an intravenous contrast agent for magnetic resonance angiography. Ann. Pharmacother. 45(12), 1571-1575 (2011).
35. Li W, Tutton S, Vu AT et al. First-pass contrast-enhanced magnetic resonance angiography in humans using ferumoxytol, a novel ultrasmall superparamagnetic iron oxide (USPIO)-based blood pool agent. J. Magn. Reson. Imaging 21(1), 46-52 (2005).
36. Prince MR, Zhang HL, Chabra SG, Jacobs P, Wang Y. A pilot investigation of new superparamagnetic iron oxide (ferumoxytol) as a contrast agent for cardiovascular MRI. J. Xray Sci. Technol. 11(4), 231-240 (2003).
37. Ersoy H, Jacobs P, Kent CK, Prince MR. Blood pool MR angiography of aortic stent-graft endoleak. Am. J. Roentgenol. 182(5), 1181-1186 (2004).
38. Li W, Salanitri J, Tutton S et al. Lower extremity deep venous thrombosis: evaluation with ferumoxytol-enhanced MR imaging and dual-contrast mechanism-preliminary experience. Radiology 242(3), 873-881 (2007).
39. Simon GH, Bauer J, Saborovski O et al. T1 and T2 relaxivity of intracellular and extracellular USPIO at 1.5T and 3T clinical MR scanning. Eur. Radiol. 16(3), 738-745 (2006).
40. Corot C, Petry KG, Trivedi R et al. Macrophage imaging in central nervous system and in carotid atherosclerotic plaque using ultrasmall superparamagnetic iron oxide in magnetic resonance imaging. Invest. Radiol. 39(10), 619-625 (2004).
41. Chambon C, Clement O, Le Blanche A, Schouman-Claeys E, Frija G. Superparamagnetic iron oxides as positive MR contrast agents: in vitro and in vivo evidence. Magn. Reson. Imaging 11(4), 509-519 (1993).
42. Girard OM, Ramirez R, Mccarty S, Mattrey RF. Toward absolute quantification of iron oxide nanoparticles as well as cell internalized fraction using multiparametric MRI. Contrast Media Mol. Imaging 7(4), 411-417 (2012).
43. Feng D, Nagy JA, Hipp J, Dvorak HF, Dvorak AM. Vesiculo-vacuolar organelles and the regulation of venule permeability to macromolecules by vascular permeability factor, histamine, and serotonin. J. Exp. Med. 183(5), 1981-1986 (1996).
44. Stewart PA, Hayakawa K, Hayakawa E, Farrell CL, Del Maestro RF. A quantitative study of blood-brain barrier permeability ultrastructure in a new rat glioma model. Acta Neuropathol. 67(1-2), 96-102 (1985).
45. Black KL, Ningaraj NS. Modulation of brain tumor capillaries for enhanced drug delivery selectively to brain tumor. Cancer Control 11(3), 165-173 (2004).
46. Renkin EM. Multiple pathways of capillary permeability. Circ. Res. 41(6), 735-743 (1977).
47. Schlageter KE, Molnar P, Lapin GD, Groothuis DR. Microvessel organization and structure in experimental brain tumors: microvessel populations with distinctive structural and functional properties. Microvasc. Res. 58(3), 312-328 (1999).
48. Beaumont M, Lemasson B, Farion R, Segebarth C, Remy C, Barbier EL. Characterization of tumor angiogenesis in rat brain using iron-based vessel size index MRI in combination with gadolinium-based dynamic contrast-enhanced MRI. J. Cereb. Blood Flow Metabol. 29(10), 1714-1726 (2009).
49. Henning TD, Wendland MF, Golovko D et al. Relaxation effects of ferucarbotran-labeled mesenchymal stem cells at 1.5T and 3T: discrimination of viable from lysed cells. Magn. Reson. Med. 62(2), 325-332 (2009).
50. Weissleder R, Elizondo G, Wittenberg J, Rabito CA, Bengele HH, Josephson L. Ultrasmall superparamagnetic iron oxide: characterization of a new class of contrast agents for MR imaging. Radiology 175(2), 489-493 (1990).
51. Zimmer C, Weissleder R, Poss K, Bogdanova A, Wright SC Jr, Enochs WS. MR imaging of phagocytosis in experimental gliomas. Radiology 197(2), 533-538 (1995).
52. Schulze E, Ferrucci JT Jr, Poss K, Lapointe L, Bogdanova A, Weissleder R. Cellular uptake and trafficking of a prototypical magnetic iron oxide label in vitro. Invest. Radiol. 30(10), 604-610 (1995).
53. Levy M, Luciani N, Alloyeau D et al. Long term in vivo biotransformation of iron oxide nanoparticles. Biomaterials 32(16), 3988-3999 (2011).
54. Bourrinet P, Bengele HH, Bonnemain B et al. Preclinical safety and pharmacokinetic profile of ferumoxtran-10, an ultrasmall superparamagnetic iron oxide magnetic resonance contrast agent. Invest. Radiol. 41(3), 313-324 (2006).
55. Bernd H, De Kerviler E, Gaillard S, Bonnemain B. Safety and tolerability of ultrasmall superparamagnetic iron oxide contrast agent: comprehensive analysis of a clinical development program. Invest. Radiol. 44(6), 336-342 (2009).
56. Daldrup-Link HE, Rydland J, Helbich TH et al. Quantification of breast tumor microvascular permeability with feruglose-enhanced MR imaging: initial phase II multicenter trial. Radiology 229(3), 885-892 (2003).
57. Reimer P, Bremer C, Allkemper T et al. Myocardial perfusion and MR angiography of chest with SH U 555 C: results of placebo-controlled clinical phase i study. Radiology 231(2), 474-481 (2004).
58. Tombach B, Reimer P, Bremer C et al. First-pass and equilibrium-MRA of the aortoiliac region with a superparamagnetic iron oxide blood pool MR contrast agent (SH U 555 C): results of a human pilot study. NMR Biomed. 17(7), 500-506 (2004).
59. Murphy KP, Szopinski KT, Cohan RH, Mermillod B, Ellis JH. Occurrence of adverse reactions to gadolinium-based contrast material and management of patients at increased risk: a survey of the American Society of Neuroradiology Fellowship Directors. Acad. Radiol. 6(11), 656-664 (1999).
60. Nelson KL, Gifford LM, Lauber-Huber C, Gross CA, Lasser TA. Clinical safety of gadopentetate dimeglumine. Radiology 196(2), 439-443 (1995).
61. Niendorf H, Alhassan A, Balzer T, Claub W, Greens V. Safety and risk of gadolinium-DTPA: extended clinical experience after more than 20 million applications. In: Magnevist.Felix R, Hosten N, Hricak H (Eds). Blackwell Science, Berlin, Germany, 17-27 (1998).
62. Kuo PH, Kanal E, Abu-Alfa AK, Cowper SE. Gadolinium-based MR contrast agents and nephrogenic systemic fibrosis. Radiology 242(3), 647-649 (2007).
63. Deo A, Fogel M, Cowper SE. Nephrogenic systemic fibrosis: a population study examining the relationship of disease development to gadolinium exposure. Clin. J. Am. Soc. Nephrol. 2(2), 264-267 (2007).
64. Elmholdt TR, Olesen AB, Jorgensen B et al. Nephrogenic systemic fibrosis in Denmarka nationwide investigation. PLoS ONE 8(12), e82037 (2013).
65. Kalber TL, Smith CJ, Howe FA et al. A longitudinal study of R2∗ and R2 Magnetic Resonance Imaging relaxation rate measurements in murine liver after a single administration of 3 different iron oxide-based contrast agents. Invest. Radiol. 40(12), 784-791 (2005).
66. Biesenbach G, Kaiser W, Zazgornik J. Incidence of acute oligoanuric renal failure in dextran 40 treated patients with acute ischemic stroke stage III or IV. Renal Fail. 19(1), 69-75 (1997).
67. Schinco MA, Hughes D, Santora TA. Complications of 32% dextran-70 in 10% dextrose. A case report. J. Reprod. Med. 41(6), 455-458 (1996).
68. Bishu K, Agarwal R. Acute injury with intravenous iron and concerns regarding long-term safety. Clin. J. Am. Soc. Nephrol. 1(Suppl. 1), S19-S23 (2006).
69. Pai AB, Garba AO. Ferumoxytol: a silver lining in the treatment of anemia of chronic kidney disease or another dark cloud? J. Blood Med. 3, 77-85 (2012).
70. Landry R, Jacobs PM, Davis R, Shenouda M, Bolton WK. Pharmacokinetic study of ferumoxytol: a new iron replacement therapy in normal subjects and hemodialysis patients. Am. J. Nephrol. 25(4), 400-410 (2005).
71. Neuwelt EA, Hamilton BE, Varallyay CG et al. Ultrasmall superparamagnetic iron oxides (USPIOs): a future alternative magnetic resonance (MR) contrast agent for patients at risk for nephrogenic systemic fibrosis (NSF)? Kidney Int. 75(5), 465-474 (2009).
72. Auerbach M, Strauss W, Auerbach S, Rineer S, Bahrain H. Safety and efficacy of total dose infusion of 1,020 mg of ferumoxytol administered over 15 min. Am. J. Hematol. 88(11), 944-947 (2013).
73. Enochs WS, Harsh G, Hochberg F, Weissleder R. Improved delineation of human brain tumors on MR images using a long-circulating, superparamagnetic iron oxide agent. J. Magn. Reson. Imaging 9(2), 228-232 (1999).
74. Hunt MA, Bago AG, Neuwelt EA. Single-dose contrast agent for intraoperative MR imaging of intrinsic brain tumors by using ferumoxtran-10. Am. J. Neuroradiol. 26(5), 1084-1088 (2005).
75. Murillo TP, Sandquist C, Jacobs PM, Nesbit G, Manninger S, Neuwelt EA. Imaging brain tumors with ferumoxtran-10, a nanoparticle magnetic resonance contrast agent. Therapy 2, 871-882 (2005).
76. Neuwelt EA, Varallyay P, Bago AG, Muldoon LL, Nesbit G, Nixon R. Imaging of iron oxide nanoparticles by MR and light microscopy in patients with malignant brain tumours. Neuropathol. Appl. Neurobiol. 30(5), 456-471 (2004).
77. Taschner CA, Wetzel SG, Tolnay M, Froehlich J, Merlo A, Radue EW. Characteristics of ultrasmall superparamagnetic iron oxides in patients with brain tumors. Am. J. Roentgenol. 185(6), 1477-1486 (2005).
78. Moore A, Marecos E, Bogdanov A Jr, Weissleder R. Tumoral distribution of long-circulating dextran-coated iron oxide nanoparticles in a rodent model. Radiology 214(2), 568-574 (2000).
79. Muldoon LL, Sandor M, Pinkston KE, Neuwelt EA. Imaging, distribution, and toxicity of superparamagnetic iron oxide magnetic resonance nanoparticles in the rat brain and intracerebral tumor. Neurosurgery785-796 (2005).
80. Rainov NG, Zimmer C, Chase M et al. Selective uptake of viral and monocrystalline particles delivered intra-arterially to experimental brain neoplasms. Hum. Gene Ther. 6(12), 1543-1552 (1995).
81. Zimmer C, Wright SC Jr, Engelhardt RT et al. Tumor cell endocytosis imaging facilitates delineation of the glioma-brain interface. Exp. Neurol. 143(1), 61-69 (1997).
82. Kremer S, Pinel S, Vedrine PO et al. Ferumoxtran-10 enhancement in orthotopic xenograft models of human brain tumors: an indirect marker of tumor proliferation? J. Neurooncol. 83(2), 111-119 (2007).
83. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4(1), 71-78 (2004).
84. Crowther M, Brown NJ, Bishop ET, Lewis CE. Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumors. J. Leukoc. Biol. 70(4), 478-490 (2001).
85. Lin EY, Li JF, Gnatovskiy L et al. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 66(23), 11238-11246 (2006).
86. Mantovani A, Bottazzi B, Colotta F, Sozzani S, Ruco L. The origin and function of tumor-associated macrophages. Immunol. Today 13(7), 265-270 (1992).
87. Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J. Pathol. 196(3), 254-265 (2002).
88. Nishie A, Ono M, Shono T et al. Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas. Clin. Cancer Res. 5(5), 1107-1113 (1999).
89. Rossi ML, Jones NR, Candy E et al. The mononuclear cell infiltrate compared with survival in high-grade astrocytomas. Acta Neuropathol. 78(2), 189-193 (1989).
90. Corot C, Warlin D. Superparamagnetic iron oxide nanoparticles for MRI: contrast media pharmaceutical company R&D perspective. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 5(5), 411-422 (2013).
91. Dosa E, Guillaume DJ, Haluska M et al. Magnetic Resonance Imaging of intracranial tumors: intra-patient comparison of gadoteridol and ferumoxytol. Neurooncology 13(2), 251-260 (2011).
92. Manninger SP, Muldoon LL, Nesbit G, Murillo T, Jacobs PM, Neuwelt EA. An exploratory study of ferumoxtran-10 nanoparticles as a blood-brain barrier imaging agent targeting phagocytic cells in CNS inflammatory lesions. Am. J. Neuroradiol. 26(9), 2290-2300 (2005).
93. Holness CL, Simmons DL. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 81(6), 1607-1613 (1993).
94. Knauth M, Egelhof T, Roth SU, Wirtz CR, Sartor K. Monocrystalline iron oxide nanoparticles: possible solution to the problem of surgically induced intracranial contrast enhancement in intraoperative MR imaging. Am. J. Neuroradiol. 22(1), 99-102 (2001).
95. Aronen HJ, Gazit IE, Louis DN et al. Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology 191(1), 41-51 (1994).
96. Sugahara T, Korogi Y, Kochi M et al. Correlation of MR imaging-determined cerebral blood volume maps with histologic and angiographic determination of vascularity of gliomas. Am. J. Roentgenol. 171(6), 1479-1486 (1998).
97. Gahramanov S, Muldoon LL, Varallyay CG et al. Pseudoprogression of glioblastoma after chemo-and radiation therapy: diagnosis by using dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging with ferumoxytol versus gadoteridol and correlation with survival. Radiology 266(3), 842-852 (2013).
98. Barajas RF Jr, Chang JS, Segal MR et al. Differentiation of recurrent glioblastoma multiforme from radiation necrosis after external beam radiation therapy with dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. Radiology 253(2), 486-496 (2009).
99. Thompson EM, Guillaume DJ, Dosa E et al. Dual contrast perfusion MRI in a single imaging session for assessment of pediatric brain tumors. J. Neuro Oncol. 109(1), 105-114 (2012).
100. Claes A, Gambarota G, Hamans B et al. Magnetic resonance imaging-based detection of glial brain tumors in mice after antiangiogenic treatment. Int. J. Cancer 122(9), 1981-1986 (2008).
101. Gahramanov S, Muldoon LL, Li X, Neuwelt EA. Improved perfusion MR imaging assessment of intracerebral tumor blood volume and antiangiogenic therapy efficacy in a rat model with ferumoxytol. Radiology 261(3), 796-804 (2011).
102. Varallyay CG, Muldoon LL, Gahramanov S et al. Dynamic MRI using iron oxide nanoparticles to assess early vascular effects of antiangiogenic versus corticosteroid treatment in a glioma model. J. Cereb. Blood Flow Metabol. 29(4), 853-860 (2009).
103. Christoforidis GA, Yang M, Kontzialis MS et al. High resolution ultra high field Magn. Reson. Imaging of glioma microvascularity and hypoxia using ultra-small particles of iron oxide. Invest. Radiol. 44(7), 375-383 (2009).
104. Gambarota G, Leenders W, Maass C et al. Characterisation of tumour vasculature in mouse brain by USPIO contrast-enhanced MRI. Br. J. Cancer 98(11), 1784-1789 (2008).
105. Tropres I, Lamalle L, Peoc'h M et al. In vivo assessment of tumoral angiogenesis. Magn. Reson. Med. 51(3), 533-541 (2004).
106. Christen T, Ni W, Qiu D et al. High-resolution cerebral blood volume imaging in humans using the blood pool contrast agent ferumoxytol. Magn. Reson. Med. 70(3), 705-710 (2013).
107. Varallyay CG, Nesbit E, Fu R et al. High-resolution steady-state cerebral blood volume maps in patients with central nervous system neoplasms using ferumoxytol, a superparamagnetic iron oxide nanoparticle. J. Cereb. Blood Flow Metabol. 33(5), 780-786 (2013).
108. Gahramanov S, Varallyay C, Tyson RM et al. Diagnosis of pseudoprogression using MRI perfusion in patients with glioblastoma multiforme may predict improved survival. CNS Oncol. 3(6), 389-400 (2014).
109. Weller M, Stupp R, Reifenberger G et al. MGMT promoter methylation in malignant gliomas: ready for personalized medicine? Nat. Rev. Neurol. 6(1), 39-51 (2010).
110. Nanegrungsunk D, Onchan W, Chattipakorn N, Chattipakorn SC. Current evidence of temozolomide and bevacizumab in treatment of gliomas. Neurol. Res. 37(2), 167-183 (2014).
111. ClinicalTrials.gov. Assessing dynamic magnetic resonance (MR) imaging in patients with recurrent high grade glioma receiving chemotherapy. http://clinicaltrials.gov
112. Lemasson B, Christen T, Tizon X et al. Assessment of multiparametric MRI in a human glioma model to monitor cytotoxic and anti-angiogenic drug effects. NMR Biomed. 24(5), 473-482 (2011).
113. Batchelor TT, Sorensen AG, Di Tomaso E et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11(1), 83-95 (2007).
114. Thomas AA, Omuro A. Current role of anti-angiogenic strategies for glioblastoma. Curr. Treat. Options Oncol. 15(4), 551-566 (2014).
115. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307(5706), 58-62 (2005).
116. Chinot OL, Wick W, Mason W et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N. Engl. J. Med. 370(8), 709-722 (2014).
117. Gilbert MR, Dignam JJ, Armstrong TS et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N. Engl. J. Med. 370(8), 699-708 (2014).
118. Field KM, Jordan JT, Wen PY, Rosenthal MA, Reardon DA. Bevacizumab and glioblastoma: Scientific review, newly reported updates, and ongoing controversies. Cancer doi: 10.1002/cncr.28935 (2014) (Epub ahead of print).
119. Emblem KE, Farrar CT, Gerstner ER et al. Vessel calibre-a potential MRI biomarker of tumour response in clinical trials. Nat. Rev. Clin. Oncol. 11(10), 566-584 (2014).
120. Tropres I, Pannetier N, Grand S et al. Imaging the microvessel caliber and density: Principles and applications of microvascular MRI. Magn. Reson. Med. doi: 10.1002/mrm.25396 (2014) (Epub ahead of print).
121. Dennie J, Mandeville JB, Boxerman JL, Packard SD, Rosen BR, Weisskoff RM. NMR imaging of changes in vascular morphology due to tumor angiogenesis. Magn. Reson. Med. 40(6), 793-799 (1998).
122. Lemasson B, Valable S, Farion R, Krainik A, Remy C, Barbier EL. In vivo imaging of vessel diameter, size, and density: a comparative study between MRI and histology. Magn. Reson. Med. 69(1), 18-26 (2013).
123. Pannetier N, Lemasson B, Christen T et al. Vessel size index measurements in a rat model of glioma: comparison of the dynamic (Gd) and steady-state (iron-oxide) susceptibility contrast MRI approaches. NMR Biomed. 25(2), 218-226 (2012).
124. Bouchet A, Lemasson B, Le Duc G et al. Preferential effect of synchrotron microbeam radiation therapy on intracerebral 9L gliosarcoma vascular networks. Int. J. Radiat. Oncol. Biol. Phys. 78(5), 1503-1512 (2010).
125. Kostourou V, Robinson SP, Whitley GS, Griffiths JR. Effects of overexpression of dimethylarginine dimethylaminohydrolase on tumor angiogenesis assessed by susceptibility magnetic resonance imaging. Cancer Res. 63(16), 4960-4966 (2003).
126. Quarles CC, Schmainda KM. Assessment of the morphological and functional effects of the anti-angiogenic agent SU11657 on 9L gliosarcoma vasculature using dynamic susceptibility contrast MRI. Magn. Reson. Med. 57(4), 680-687 (2007).
127. Serduc R, Christen T, Laissue J et al. Brain tumor vessel response to synchrotron microbeam radiation therapy: a short-term in vivo study. Phys. Med. Biol. 53(13), 3609-3622 (2008).
128. Emblem KE, Mouridsen K, Bjornerud A et al. Vessel architectural imaging identifies cancer patient responders to anti-angiogenic therapy. Nat. Med. 19(9), 1178-1183 (2013).
129. Sorensen AG, Batchelor TT, Zhang WT et al. A "vascular normalization index" as potential mechanistic biomarker to predict survival after a single dose of cediranib in recurrent glioblastoma patients. Cancer Res. 69(13), 5296-5300 (2009).
130. Batchelor TT, Gerstner ER, Emblem KE et al. Improved tumor oxygenation and survival in glioblastoma patients who show increased blood perfusion after cediranib and chemoradiation. Proc. Natl Acad. Sci. USA 110(47), 19059-19064 (2013).
131. Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, Brown JM. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J. Clin. Invest. 120(3), 694-705 (2010).
132. Ahn GO, Brown JM. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell 13(3), 193-205 (2008).
133. Martin BJ. Inhibiting vasculogenesis after radiation: a new paradigm to improve local control by radiotherapy. Semin. Radiat. Oncol. 23(4), 281-287 (2013).
134. Orringer DA, Koo YE, Chen T, Kopelman R, Sagher O, Philbert MA. Small solutions for big problems: the application of nanoparticles to brain tumor diagnosis and therapy. Clin. Pharmacol. Ther. 85(5), 531-534 (2009).
135. Reddy GR, Bhojani MS, Mcconville P et al. Vascular targeted nanoparticles for imaging and treatment of brain tumors. Clin. Cancer Res. 12(22), 6677-6686 (2006).
136. Cai W, Shin DW, Chen K et al. Peptide-labeled near-infrared quantum dots for imaging tumor vasculature in living subjects. Nano Lett. 6(4), 669-676 (2006).
137. Madhankumar AB, Slagle-Webb B, Mintz A, Sheehan JM, Connor JR. Interleukin-13 receptor-targeted nanovesicles are a potential therapy for glioblastoma multiforme. Mol. Cancer Ther. 5(12), 3162-3169 (2006).
138. Hadjipanayis CG, Machaidze R, Kaluzova M et al. EGFRvIII antibody-conjugated iron oxide nanoparticles for magnetic resonance imaging-guided convection-enhanced delivery and targeted therapy of glioblastoma. Cancer Res. 70(15), 6303-6312 (2010).
139. Aboody KS, Najbauer J, Metz MZ et al. Neural stem cell-mediated enzyme/prodrug therapy for glioma: preclinical studies. Sci. Transl. Med. 5(184), 184ra159 (2013).
140. Gutova M, Shackleford GM, Khankaldyyan V et al. Neural stem cell-mediated CE/CPT-11 enzyme/prodrug therapy in transgenic mouse model of intracerebellar medulloblastoma. Gene Ther. 20(2), 143-150 (2013).
141. Gutova M, Frank JA, D'apuzzo M et al. Magn. Reson. Imaging tracking of ferumoxytol-labeled human neural stem cells: studies leading to clinical use. Stem Cells Transl. Med. 2(10), 766-775 (2013).
142. Daldrup-Link HE, Rudelius M, Oostendorp RA et al. Targeting of hematopoietic progenitor cells with MR contrast agents. Radiology 228(3), 760-767 (2003).
143. Wankhede M, Bouras A, Kaluzova M, Hadjipanayis CG. Magnetic nanoparticles: an emerging technology for malignant brain tumor imaging and therapy. Expert Rev. Clin. Pharmacol. 5(2), 173-186 (2012).
144. Weinstein JS, Varallyay CG, Dosa E et al. Superparamagnetic iron oxide nanoparticles: diagnostic Magn. Reson. Imaging and potential therapeutic applications in neurooncology and central nervous system inflammatory pathologies, a review. J. Cereb. Blood Flow Metabol. 30(1), 15-35 (2010).
145. Maier-Hauff K, Ulrich F, Nestler D et al. Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J. Neurooncol. 103(2), 317-324 (2011).
146. Tani N, Joly O, Iwamuro H et al. Direct visualization of non-human primate subcortical nuclei with contrast-enhanced high field MRI. Neuroimage 58(1), 60-68 (2011).
147. Burrell JS, Walker-Samuel S, Baker LC et al. Evaluation of novel combined carbogen USPIO (CUSPIO) imaging biomarkers in assessing the antiangiogenic effects of cediranib (AZD2171) in rat C6 gliomas. Int. J. Cancer 131(8), 1854-1862 (2012).