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

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1 Cha S. Update on brain tumor imaging: from anatomy to physiology. Am. J. Neuroradiol. 27(3), 475–487 (2006).• Provides excellent review on current state of brain tumor imaging.
  Medline CASGoogle Scholar
• 2 Thakor AS, Gambhir SS. Nanooncology: the future of cancer diagnosis and therapy. CA Cancer J. Clin. 63(6), 395–418 (2013).
  MedlineGoogle Scholar
• 3 Provenzale JM, Silva GA. Uses of nanoparticles for central nervous system imaging and therapy. Am. J. Neuroradiol. 30(7), 1293–1301 (2009).
  Medline CASGoogle Scholar
• 4 Meyers JD, Doane T, Burda C, Basilion JP. Nanoparticles for imaging and treating brain cancer. Nanomedicine 8(1), 123–143 (2013).
  CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 12 Covarrubias DJ, Rosen BR, Lev MH. Dynamic magnetic resonance perfusion imaging of brain tumors. Oncologist 9(5), 528–537 (2004).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).•• Provides excellent review of iron oxide nanoparticles.
  Medline CASGoogle Scholar
• 22 Giesel FL, Mehndiratta A, Essig M. High-relaxivity contrast-enhanced magnetic resonance neuroimaging: a review. Eur. Radiol. 20(10), 2461–2474 (2010).
  MedlineGoogle Scholar
• 23 Cotton F, Hermier M. The advantage of high relaxivity contrast agents in brain perfusion. Eur. Radiol. 16(Suppl. 7), M16–M26 (2006).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).• Provides timeline for ferumoxytol enhancement in malignant tumors observed on MRI.
  MedlineGoogle Scholar
• 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).•• Discusses important US FDA report reviewing the safety profile of ferumoxytol.
  Medline CASGoogle Scholar
• 33 Daldrup-Link H, Coussens LM. MR imaging of tumor-associated macrophages. Oncol. Immunol. 1(4), 507–509 (2012).
  Google Scholar
• 34 Stabi KL, Bendz LM. Ferumoxytol use as an intravenous contrast agent for magnetic resonance angiography. Ann. Pharmacother. 45(12), 1571–1575 (2011).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 46 Renkin EM. Multiple pathways of capillary permeability. Circ. Res. 41(6), 735–743 (1977).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 53 Levy M, Luciani N, Alloyeau D et al. Long term in vivo biotransformation of iron oxide nanoparticles. Biomaterials 32(16), 3988–3999 (2011).
  Medline CASGoogle Scholar
• 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).• Provides excellent review of ferumoxtran-10.
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 60 Nelson KL, Gifford LM, Lauber-Huber C, Gross CA, Lasser TA. Clinical safety of gadopentetate dimeglumine. Radiology 196(2), 439–443 (1995).
  Medline CASGoogle Scholar
• 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).
  Google Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 64 Elmholdt TR, Olesen AB, Jorgensen B et al. Nephrogenic systemic fibrosis in Denmark‐‐a nationwide investigation. PLoS ONE 8(12), e82037 (2013).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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. Neurosurgery 785–796 (2005).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 83 Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4(1), 71–78 (2004).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 93 Holness CL, Simmons DL. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 81(6), 1607–1613 (1993).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).• Provides important data for distinguishing treatment effects from viable tumor using ferumoxytol.
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 105 Tropres I, Lamalle L, Peoc'h M et al. In vivo assessment of tumoral angiogenesis. Magn. Reson. Med. 51(3), 533–541 (2004).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 111 ClinicalTrials.gov. Assessing dynamic magnetic resonance (MR) imaging in patients with recurrent high grade glioma receiving chemotherapy. http://clinicaltrials.gov/ct2/show/NCT00769093?term=ferumoxytol&rank=30.
  Google Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 114 Thomas AA, Omuro A. Current role of anti-angiogenic strategies for glioblastoma. Curr. Treat. Options Oncol. 15(4), 551–566 (2014).
  MedlineGoogle Scholar
• 115 Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307(5706), 58–62 (2005).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 133 Martin BJ. Inhibiting vasculogenesis after radiation: a new paradigm to improve local control by radiotherapy. Semin. Radiat. Oncol. 23(4), 281–287 (2013).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Google Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar
• 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).•• Provides excellent review of iron oxide nanoparticles in brain tumor imaging.
  Medline CASGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  MedlineGoogle Scholar
• 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).
  Medline CASGoogle Scholar