A comprehensive literatures update of clinical researches of superparamagnetic resonance iron oxide nanoparticles for magnetic resonance imaging

Yì Xiáng J Wáng, Jean-Marc Idée, Yì Xiáng J Wáng, Jean-Marc Idée

Abstract

This paper aims to update the clinical researches using superparamagnetic iron oxide (SPIO) nanoparticles as magnetic resonance imaging (MRI) contrast agent published during the past five years. PubMed database was used for literature search, and the search terms were (SPIO OR superparamagnetic iron oxide OR Resovist OR Ferumoxytol OR Ferumoxtran-10) AND (MRI OR magnetic resonance imaging). The literature search results show clinical research on SPIO remains robust, particularly fuelled by the approval of ferumoxytol for intravenously administration. SPIOs have been tested on MR angiography, sentinel lymph node detection, lymph node metastasis evaluation; inflammation evaluation; blood volume measurement; as well as liver imaging. Two experimental SPIOs with unique potentials are also discussed in this review. A curcumin-conjugated SPIO can penetrate brain blood barrier (BBB) and bind to amyloid plaques in Alzheime's disease transgenic mice brain, and thereafter detectable by MRI. Another SPIO was fabricated with a core of Fe3O4 nanoparticle and a shell coating of concentrated hydrophilic polymer brushes and are almost not taken by peripheral macrophages as well as by mononuclear phagocytes and reticuloendothelial system (RES) due to the suppression of non-specific protein binding caused by their stealthy ''brush-afforded'' structure. This SPIO may offer potentials for the applications such as drug targeting and tissue or organ imaging other than liver and lymph nodes.

Keywords: MR angiography, sentinel lymph node; Superparamagnetic resonance iron oxide; contrast agent; lymph node metastasis; magnetic resonance imaging (MRI); superparamagnetic iron oxide (SPIO).

Conflict of interest statement

Conflicts of Interest: JM Idée is an employee of Guerbet group, France. Guerbet group manufactures and markets a number of contrast agents for diagnostic and interventional imaging. And other author has no conflicts of interest to declare.

Figures

Figure 1
Figure 1
Schematic representation of (A) spinal crystal structure for SPIO domain, (B) SPIO crystal with multiple magnetic domains of random orientation and (C) complete SPIO contrast agent particle, with multiple SPIO crystals and coating materials. (D) SPIO crystal in the absence of an external magnetic field, the orientation of the magnetic domains is random. (E) An external magnetic field (B0) causes the magnetic domains of the SPIO crystal to reorient according to B0, which is reversible after the Bo is removed. SPIO, superparamagnetic iron oxide.
Figure 2
Figure 2
Superparamagnetic property of SPIO. (A) Homogeneous SPIO particle homogeneous suspension in a vial; (B) SPIO particles are attracted by a magnet placed close to one side wall of a vial; (C) after the remove of the external magnet, the SPIO particles can be homogeneously dispersed again, with no residual magnetic property. SPIO, superparamagnetic iron oxide.
Figure 3
Figure 3
A picture of Sienna plus® and its detector Sentimag® (Copyright: Endomagentics Ltd).
Figure 4
Figure 4
Comparison of TOF MR angiography, ferumoxytol enhanced MR angiography, and X-ray digital DSA. (A-C) MIP images of radiocephalic wrist fistula (1 month after surgery). TOF MIP image shows low signal intensity in the arterial inflow and side branch on the venous outflow (arrows); these regions are clearly depicted on the ferumoxytol-enhanced MR angiography MIP image. Note that the TOF coverage of the vascular anatomy is only half the coverage of the ferumoxytol-enhanced MR angiogram. Absence of stenosis was confirmed by using DSA; (D-F) MIP images of brachiocephalic elbow fistula (8 months after surgery). TOF MIP image illustrates two stenotic regions (arrows). Ferumoxytol-enhanced MR angiography MIP image shows three stenotic regions, two distal to the anastomosis (arrows) and one proximate that appears occluded (*). Note the improved volume coverage of the ferumoxytol-enhanced MR angiography that enables detection of stenosis missed at TOF imaging. All three stenotic regions were confirmed on DSA image [Reprinted with permission (49)]. MIP, maximum intensity projection; TOF, time of flight; DSA, digital subtraction angiography.
Figure 5
Figure 5
Schematic representation of the sentinel lymph node localization procedure, showing the peritumoral injection site, and tracer travelling to two sentinel lymph nodes which can be biopsied and further evaluated for histopathologically.
Figure 6
Figure 6
Three-dimensional CT lymphography reconstructed from the first post-iodinated contrast images (A). Iodinated contrast agent is injected intradermally into the skin overlying the breast tumor and the subareolar skin. Lymphatic vessels are drained into a single axillary sentinel node (arrow, A). Images of CT lymphography (B) and T2*-weighted axial MR images (C) at the same level are compared to specify the node (arrow) on T2*-weighted axial MRI corresponding to the sentinel node (arrow) identified by CT lymphography. If necessary, images of CT lymphography and T2*-weighted axial MR images can be merged on a workstation (D) [Reprinted with permission (53)].
Figure 7
Figure 7
Resovist enhanced MRI demonstrates metastasis negative and positive lymph nodes. (A) CT lymphography demonstrates a sentinel node (arrow); (B) the corresponding node is identified on pre-SPIO-contrast T2*-weighted axial MRI (arrow), showing high signal intensity; (C) after administration of SPIO, the node shows strong SPIO enhancement and was diagnosed as benign (arrow); (D) histologic findings confirmed it as benign; (E) CT lymphography demonstrates a sentinel node (arrow); (F) the corresponding node is identified on pre-SPIO-contrast T2*-weighted axial MRI (arrow), showing high signal; (G) after administration of SPIO, the node shows no SPIO enhancement and is diagnosed as malignant (arrow); (H) histologic findings confirmed it as malignant. This node is almost entirely replaced by metastatic tissue (arrowheads) [Reprinted with permission (53)]. SPIO, superparamagnetic iron oxide; MRI, magnetic resonance imaging.
Figure 8
Figure 8
This figure shows that how small lymph nodes supposed to be benign due to their size can be malignant. Images on the left hand are pre-contrast images, while the post-ferumoxtran-10 images on the right show hypersignal intensity small lymph nodes, which is a sign of malignancies. MRI at 3T allows depiction of these small lesions with high spatial resolution [Reprinted with permission (1)]. MRI, magnetic resonance imaging.
Figure 9
Figure 9
Mismatch between gadolinium- and ferumoxtran-10 enhanced images obtained at baseline in a 23-year-old woman with active relapsing-remitting MS without disease-modifying treatment. Left, axial unenhanced T2-weighted image shows multiple hyperintense lesions. Middle, axial gadolinium-enhanced T1-weighted image shows three enhanced lesions (arrows). Right, axial T1-weighted image obtained 24–48 hours after injection of Ferumoxtran-10 shows the same three lesions along with three additional active lesions that enhanced only with ferumoxtran-10 (arrows) [Reprinted with permission (94)].
Figure 10
Figure 10
Ferumoxytol-enhanced MRI detects depict macrophage distribution in intracranial aneurysm walls. (A) T2* gradient echo MRI sequence at baseline and 24 hours postinfusion of Ferumoxytol showing early signal changes in the walls of 3 cerebral aneurysms. A1–4, corresponds with a patient a right vertebral artery aneurysm; B1–4, corresponds with a patient with a left supraclinoid internal carotid artery aneurysm; and C1–4, corresponds with a patient with a fusiform vertebrobasilar artery aneurysm). Difference images demonstrate the relative signal loss after ferumoxytol infusion. All 3 aneurysms ruptured within 6 months. (B) T2* gradient echo MRI sequence at baseline and 24 hours postinfusion of Ferumoxytol, and subtraction images showing no early signal changes in 3 aneurysms from three patients (A1–3, right internal carotid artery terminus aneurysm; B1–3, anterior communicating artery aneurysm; and C1–3, right cavernous internal carotid artery aneurysm). None of these aneurysms ruptured during the follow-up period [Reprinted with permission (109)]. MRI, magnetic resonance imaging.
Figure 11
Figure 11
Color map of MRI of an AAA. Red and yellow pixels indicate areas of increased T2* value, indicative of USPIO uptake [Reprinted with permission (114)]. AAA, abdominal aortic aneurysm; MRI, magnetic resonance imaging.
Figure 12
Figure 12
Ferumoxytol enhanced MRI of pancreas shows increased pancreatic SPIO accumulation in patients with type-1 diabetes 3D volume sets of a representative patient with recently diagnosed type-1 diabetes (A) and a normal control subject (B). (C) Comparison of the two cohorts examined by MRI. Plots of global pancreatic delta R2* (i.e., =1/T2*) values are shown for 11 patients with type-1 diabetes and ten normal controls [Reprinted with permission (115), Copyright [2015] National Academy of Sciences of USA]. MRI, magnetic resonance imaging; SPIO, superparamagnetic iron oxide.
Figure 13
Figure 13
Combined contrast enhanced (ferumoxides and Gd-DTPA) MR images at various stages of fibrosis. Combined contrast enhanced images in adults with chronic hepatitis C virus infection and histologically determined Metavir fibrosis stages F0, F1, F2, F3, and F4. Subjectively, the reticular texture of the liver parenchyma becomes progressively more pronounced with increasing Metavir fibrosis stage [Reprinted with permission (127)].
Figure 14
Figure 14
A small (1 cm) capillary hemangioma, proven by biopsy, was located in the segment VIII; dynamic MR images after gadolinium (Gd) administration show focal faint enhancement by the lesion (white circle) only in the arterial phase (A) with no focal abnormality in portal (B) and equilibrium (C) phases (false positive finding); T2 weighted MR images before (D) and after (E) SPIO administration show homogeneous contrast distribution in the liver with diffuse hypointensity and no focal abnormalities (true negative finding) [Reprinted with permission (130)]. SPIO, superparamagnetic iron oxide.
Figure 15
Figure 15
A small (1 cm) dysplastic nodule, proven by biopsy, was located in the segment VIII; dynamic MR images after gadolinium (Gd) administration show focal faint enhancement by the lesion (white circle) only in the arterial phase (A) with no focal abnormality in portal (B) and equilibrium (C) phases (false positive finding); T2 weighted MR images before (D) and after (E) SPIO administration show homogeneous contrast distribution in the liver with diffuse hypointensity and no focal abnormalities (true negative finding) [Reprinted with permission (130)]. SPIO, superparamagnetic iron oxide.
Figure 16
Figure 16
A small (5 mm) hepatocellular carcinoma (HCC), proven by biopsy, was located in the segment VI; dynamic MR images after gadolinium (Gd) administration show no focal abnormalities in the arterial (A), portal (B) and equilibrium (C) phases (false negative finding); T2 weighted MR images before (D) and after (E) SPIO administration show diffuse liver hypointensity and focal faint hyperintensity (white circle) in the VI hepatic segment in the post-contrast MR image (E) (true positive finding) [Reprinted with permission (130)]. HCC, hepatocellular carcinoma; SPIO, superparamagnetic iron oxide.
Figure 17
Figure 17
The process of creating SS-cerebral blood volume (CBV) maps. Using pre (A) and post (B) ferumoxytol T2*-weighted (T2*w) images, deltaR2* (=1/T2*) maps (C) can be calculated. deltaR2* is assumed to be linearly proportional to contrast agent concentration. Since there is no substantial extravasation of this blood pool agent, deltaR2* is derived from the intravascular compartment only and deltaR2* maps can be used as SS-CBV maps. To eliminate the noisy background caused by the logarithmic calculation, images were masked (D). The CBV maps are typically displayed with color coding (E) [Reprinted with permission (136)]. SS, steady state; CBV, cerebral blood volume.
Figure 18
Figure 18
Ferumoxytol enhanced MRI facilitates differentiation between brain tumor progression and pseudoprogression. (A) MR images of a patient with glioblastoma multiforme show pseudoprogression of disease. T1-weighted MR images without contrast enhancement and with gadoteridol obtained before and 3 months after chemoradiotherapy show increased contrast enhancement after treatment. Low rCBV (1.75) is apparent on parametric maps obtained by using ferumoxytol (Fe-rCBV), gadoteridol (Gd-rCBV), and gadoteridol with leakage correction (Gd-rCBV LC), which indicates true tumor progression (arrows). No contrast agent extravasation is seen on leakage map with Fe but small leakage in the lateral aspect of the tumor is seen with gadoteridol [Reprinted with permission (140)].
Figure 19
Figure 19
Plot of liver Ferumoxytol uptake. Patients with NASH have decreased hepatic Ferumoxytol uptake, as reflected by a lower delta R2* 72 hours after Ferumoxytol infusion compared with patients with simple steatosis and healthy control subjects [Reprinted with permission (147)].
Figure 20
Figure 20
(A) Axial, (B) sagittal, and (C) coronal MP images show Ferucarbotran-labeled balloon catheter. The catheter is delineable in the 3-dimensional FOV of 20×36×36 mm3 [Reprinted with permission (150)].
Figure 21
Figure 21
Particle size characterizations of Cur-MNP. (A) Sizes of pure SPIO and Cur-SPIO (freshly made and after 24 h dialysis) measured by dynamic light scattering analyzer; (B) TEM images of pure SPIO (left) and Cur-SPIO (right); (C) AFM images of a Cur-SPIO in morphology mode (left) and in phase difference mode (right); (D) Step-wise process of making Cur-SPIO [Reprinted with permission (154)]. SPIO, superparamagnetic iron oxide; Cur-MNP, Curcumin SPIO nanoparticles.
Figure 22
Figure 22
Iron staining, fluorescence, and immunohistochemistry reveal co-localization of SPIO and Curcumin on amyloid plaques. (A) Bright view of histochemically labeled Alzheimer’s disease transgenic mouse brain section. Immunohistochemically labeled amyloid plaques (red) and Prussian blue stained iron oxide (blue). Inset: 40× magnification of a region displaying co-localization of iron oxide with a plaque; (B) match between the black dots of 7 Tesla MRI (left) and plaques labeled immunohistochemically (red) and by Cur-SPIO (blue). Left inset: iron (blue) anchored on plaques (red). Right inset: curcumin (fluorescent) co-localization on the plaques. Insets: 100× magnification of plaques [Reprinted with permission (154)]. SPIO, superparamagnetic iron oxide.
Figure 23
Figure 23
There is a close to linear correlation between signal intensity and concentration by UTE (ultrashort TE). Whereas with gradient echo the signal intensity relationship is complex with an initial increase from T1 effects and T2* causing signal decrease at concentrations >0.2 mM [Reprinted with permission (93)].

References

    1. Wang YX, Xuan S, Port M, Idee JM. Recent advances in superparamagnetic iron oxide nanoparticles for cellular imaging and targeted therapy research. Curr Pharm Des 2013;19:6575-93. 10.2174/1381612811319370003
    1. Wang YX, Hussain SM, Krestin GP. Superparamagnetic iron oxide contrast agents: physicochemical characteristics and applications in MR imaging. Eur Radiol 2001;11:2319-31. 10.1007/s003300100908
    1. Wáng YX, Idée JM, Corot C. Scientific and industrial challenges of developing nanoparticle-based theranostics and multiple-modality contrast agents for clinical application. Nanoscale 2015;7:16146-50. 10.1039/C5NR03887A
    1. Wang YX. Chapter 2: Superparamagnetic iron oxide particle nanoparticles for cellular imaging and targeted therapy: Opportunities and changes for clinical translation. In: Zhang B. editor. Nano Imaging: From fundamental Principles to Translational Medical Applications. Singapore: World Scientific, 2017:29-51.
    1. Wang YX. Current status of superparamagnetic iron oxide contrast agents for liver magnetic resonance imaging. World J Gastroenterol 2015;21:13400-2. 10.3748/wjg.v21.i47.13400
    1. Schleich N, Danhier F, Préat V. Iron oxide-loaded nanotheranostics: Major obstacles to in vivo studies and clinical translation. J Control Release 2015;198:35-54. 10.1016/j.jconrel.2014.11.024
    1. Dassler K, Roohi F, Lohrke J, Ide A, Remmele S, Hütter J, Pietsch H, Pison U, Schütz G. Current limitations of molecular magnetic resonance imaging for tumors as evaluated with high-relaxivity CD105-specific iron oxide nanoparticles. Invest Radiol 2012;47:383-91. 10.1097/RLI.0b013e31824c5a57
    1. Idée JM, Louguet S, Ballet S, Corot C. Theranostics and contrast-agents for medical imaging: a pharmaceutical company viewpoint. Quant Imaging Med Surg 2013;3:292-7.
    1. Wáng YX, Choi Y, Chen Z, Laurent S, Gibbs SL. Molecular imaging: from bench to clinic. Biomed Res Int 2014;2014:357258.
    1. Wang YX. Medical imaging in pharmaceutical clinical trials: what radiologists should know. Clin Radiol 2005;60:1051-7. 10.1016/j.crad.2005.04.016
    1. Choi HS, Frangioni JV. Nanoparticles for biomedical imaging: fundamentals of clinical translation. Mol Imaging 2010;9:291-310.
    1. Corot C, Warlin D. Superparamagnetic iron oxide nanoparticles for MRI: contrast media pharmaceutical company R&D perspective. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2013;5:411-22.
    1. Wáng YX. Systematic review and meta-analysis of diagnostic imaging technologies. Quant Imaging Med Surg 2016;6:615-8. 10.21037/qims.2016.10.08
    1. Vasanawala SS, Nguyen KL, Hope MD, Bridges MD, Hope TA, Reeder SB, Bashir MR. Safety and technique of ferumoxytol administration for MRI. Magn Reson Med 2016;75:2107-11. 10.1002/mrm.26151
    1. Kim JE, Shin JY, Cho MH. Magnetic nanoparticles: an update of application for drug delivery and possible toxic effects. Arch Toxicol 2012;86:685-700. 10.1007/s00204-011-0773-3
    1. Santosh S, Podaralla P, Miller B. Anaphylaxis with elevated serum tryptase after administration of intravenous ferumoxytol. NDT Plus 2010;3:341-2.
    1. Bailie GR. Comparison of rates of reported adverse events associated with i.v. iron products in the United States. Am J Health Syst Pharm 2012;69:310-20. 10.2146/ajhp110262
    1. Pai AB, Garba AO. Ferumoxytol: a silver lining in the treatment of anemia of chronic kidney disease or another dark cloud? J Blood Med 2012;3:77-85.
    1. Muehe AM, Feng D, von Eyben R, Luna-Fineman S, Link MP, Muthig T, Huddleston AE, Neuwelt EA, Daldrup-Link HE. Safety Report of Ferumoxytol for Magnetic Resonance Imaging in Children and Young Adults. Invest Radiol 2016;51:221-7. 10.1097/RLI.0000000000000230
    1. Food_and_Drug_Administration. Feraheme Package Insert. Available online:
    1. Food_and_Drug_Administration. Isovue Package Insert. Available online:
    1. McCulley L, Gelperin K, Bird S, Harris S, Wang C, Waldron P. Reports to FDA of fatal anaphylaxis associated with intravenous iron products. Am J Hematol 2016;91:E496-E497. 10.1002/ajh.24531
    1. Chang YK, Liu YP, Ho JH, Hsu SC, Lee OK. Amine-surface-modified superparamagnetic iron oxide nanoparticles interfere with differentiation of human mesenchymal stem cells. J Orthop Res 2012;30:1499-506. 10.1002/jor.22088
    1. Cromer Berman SM, Kshitiz C, Wang J, Orukari I, Levchenko A, Bulte JW, Walczak P. Cell motility of neural stem cells is reduced after SPIO-labeling, which is mitigated after exocytosis. Magn Reson Med 2013;69:255-62. 10.1002/mrm.24216
    1. Wang YX. Superparamagnetic iron oxide based MRI contrast agents: Current status of clinical application. Quant Imaging Med Surg 2011;1:35-40.
    1. Corot C, Robert P, Idée JM, Port M. Recent advances in iron oxide nanocrystal technology for medical imaging. Adv Drug Deliv Rev 2006;58:1471-1504. 10.1016/j.addr.2006.09.013
    1. Klein C, Nagel E, Schnackenburg B, Bornstedt A, Schalla S, Hoffmann V, Lehning A, Fleck E. The intravascular contrast agent Clariscan (NC 100150 injection) for 3D MR coronary angiography in patients with coronary artery disease. MAGMA 2000;11:65-7. 10.1007/BF02678498
    1. Wagner M, Wagner S, Schnorr J, Schellenberger E, Kivelitz D, Krug L, Dewey M, Laule M, Hamm B, Taupitz M. Coronary MR angiography using citrate-coated very small superparamagnetic iron oxide particles as blood-pool contrast agent: initial experience in humans. J Magn Reson Imaging 2011;34:816-23. 10.1002/jmri.22683
    1. Polakova K, Mocikova I, Purova D, Tucek P, Novak P, Novotna K, Izak N, Bielik R, Zboril R, Miroslav H. Magnetic resonance cholangiopancreatography (MRCP) using new negative per-oral contrast agent based on superparamagnetic iron oxide nanoparticles for extrahepatic biliary duct visualization in liver cirrhosis. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2016;160:512-7.
    1. Bashir MR, Bhatti L, Marin D, Nelson RC. Emerging applications for ferumoxytol as a contrast agent in MRI. J Magn Reson Imaging 2015;41:884-98. 10.1002/jmri.24691
    1. Albaramki J, Hodson EM, Craig JC, Webster AC. Parenteral versus oral iron therapy for adults and children with chronic kidney disease. Cochrane Database Syst Rev 2012;1:CD007857.
    1. McCullough BJ, Kolokythas O, Maki JH, Green DE. Ferumoxytol in clinical practice: implications for MRI. J Magn Reson Imaging 2013;37:1476-9. 10.1002/jmri.23879
    1. Schieda N. Parenteral ferumoxytol interaction with magnetic resonance imaging: a case report, review of the literature and advisory warning. Insights Imaging 2013;4:509-12. 10.1007/s13244-013-0262-8
    1. Gunn AJ, Seethamraju RT, Hedgire S, Elmi A, Daniels GH, Harisinghani MG. Imaging behavior of the normal adrenal on ferumoxytol-enhanced MRI: preliminary findings. AJR Am J Roentgenol 2013;201:117-21. 10.2214/AJR.12.9357
    1. Storey P, Arbini AA. Bone marrow uptake of ferumoxytol: a preliminary study in healthy human subjects. J Magn Reson Imaging 2014;39:1401-10. 10.1002/jmri.24320
    1. Harisinghani MG, Barentsz J, Hahn PF, Deserno WM, Tabatabaei S, van de Kaa CH, de la Rosette J, Weissleder R. Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N Engl J Med 2003;348:2491-9. 10.1056/NEJMoa022749
    1. European Medicines Agency. Withdrawal assessment report for sinerem. Available online:
    1. Fortuin AS, Smeenk RJ, Meijer HJ, Witjes AJ, Barentsz JO. Lymphotropic nanoparticle-enhanced MRI in prostate cancer: value and therapeutic potential. Curr Urol Rep 2014;15:389. 10.1007/s11934-013-0389-7
    1. Broome DR, Girguis MS, Baron PW, Cottrell AC, Kjellin I, Kirk GA. Gadodiamide-associated nephrogenic systemic fibrosis: why radiologists should be concerned. AJR Am J Roentgenol 2007;188:586-92. 10.2214/AJR.06.1094
    1. Grobner T. Gadolinium—a specific trigger for the development of nephrogenic fibrosing dermopathy and nephrogenic systemic fibrosis? Nephrol Dial Transplant 2006;21:1104-8. 10.1093/ndt/gfk062
    1. Sadowski EA, Bennett LK, Chan MR, Wentland AL, Garrett AL, Garrett RW, Djamali A. Nephrogenic systemic fibrosis: risk factors and incidence estimation. Radiology 2007;243:148-57. 10.1148/radiol.2431062144
    1. Wáng YX, Schroeder J, Siegmund H, Idée JM, Fretellier N, Jestin-Mayer G, Factor C, Deng M, Kang W, Morcos SK. Total gadolinium tissue deposition and skin structural findings following the administration of structurally different gadolinium chelates in healthy and ovariectomized female rats. Quant Imaging Med Surg 2015;5:534-45.
    1. Schwein A, Chinnadurai P, Shah DJ, Lumsden AB, Bechara CF, Bismuth J. Feasibility of three-dimensional magnetic resonance angiography-fluoroscopy image fusion technique in guiding complex endovascular aortic procedures in patients with renal insufficiency. J Vasc Surg 2016. [Epub ahead of print]. doi: .10.1016/j.jvs.2016.10.083
    1. Schubert T, Motosugi U, Kinner S, Colgan TJ, Sharma SD, Hetzel S, Wells S, Campo CA, Reeder SB. Crossover comparison of ferumoxytol and gadobenate dimeglumine for abdominal MR-angiography at 3.0 tesla: Effects of contrast bolus length and flip angle. J Magn Reson Imaging 2016. [Epub ahead of print]. doi: .10.1002/jmri.25513
    1. Zhou Z, Han F, Rapacchi S, Nguyen KL, Brunengraber DZ, Kim GJ, Finn JP, Hu P. Accelerated ferumoxytol-enhanced 4D multiphase, steady-state imaging with contrast enhancement (MUSIC) cardiovascular MRI: validation in pediatric congenital heart disease. NMR Biomed 2017;30. [Epub ahead of print]. doi: 10.1002/nbm.3663
    1. Lai LM, Cheng JY, Alley MT, Zhang T, Lustig M, Vasanawala SS. Feasibility of ferumoxytol-enhanced neonatal and young infant cardiac MRI without general anesthesia. J Magn Reson Imaging 2016. [Epub ahead of print]. doi: 10.1002/jmri.25482
    1. Luhar A, Khan S, Finn JP, Ghahremani S, Griggs R, Zaritsky J, Salusky I, Hall TR. Contrast-enhanced magnetic resonance venography in pediatric patients with chronic kidney disease: initial experience with ferumoxytol. Pediatr Radiol 2016;46:1332-40. 10.1007/s00247-016-3605-z
    1. Ning P, Zucker EJ, Wong P, Vasanawala SS. Hemodynamic safety and efficacy of ferumoxytol as an intravenous contrast agents in pediatric patients and young adults. Magn Reson Imaging 2016;34:152-8. 10.1016/j.mri.2015.10.019
    1. Sigovan M, Gasper W, Alley HF, Owens CD, Saloner D. USPIO-enhanced MR angiography of arteriovenous fistulas in patients with renal failure. Radiology 2012;265:584-90. 10.1148/radiol.12112694
    1. Ersoy H, Jacobs P, Kent CK, Prince MR. Blood pool MR angiography of aortic stent-graft endoleak. AJR Am J Roentgenol 2004;182:1181-6. 10.2214/ajr.182.5.1821181
    1. Cochran AJ, Essner R, Rose DM, Glass EC. Principles of sentinel lymph node identification: background and clinical implications. Langenbecks Arch Surg 2000;385:252-60. 10.1007/s004230000143
    1. Bézu C, Coutant C, Salengro A, Daraï E, Rouzier R, Uzan S. Anaphylactic response to blue dye during sentinel lymph node biopsy. Surg Oncol 2011;20: e55-e59. 10.1016/j.suronc.2010.10.002
    1. Motomura K, Ishitobi M, Komoike Y, Koyama H, Noguchi A, Sumino H, Kumatani Y, Inaji H, Horinouchi T, Nakanishi K. SPIO-enhanced magnetic resonance imaging for the detection of metastases in sentinel nodes localized by computed tomography lymphography in patients with breast cancer. Ann Surg Oncol 2011;18:3422-9. 10.1245/s10434-011-1710-7
    1. Motomura K, Izumi T, Tateishi S, Sumino H, Noguchi A, Horinouchi T, Nakanishi K. Correlation between the area of high-signal intensity on SPIO-enhanced MR imaging and the pathologic size of sentinel node metastases in breast cancer patients with positive sentinel nodes. BMC Med Imaging 2013;13:32. 10.1186/1471-2342-13-32
    1. Shiozawa M, Kobayashi S, Sato Y, Maeshima H, Hozumi Y, Lefor AT, Kurihara K, Sata N, Yasuda Y. Magnetic resonance lymphography of sentinel lymph nodes in patients with breast cancer using superparamagnetic iron oxide: a feasibility study. Breast Cancer 2014;21:394-401. 10.1007/s12282-012-0401-y
    1. Motoyama S, Ishiyama K, Maruyama K, Narita K, Minamiya Y, Ogawa J. Estimating the need for neck lymphadenectomy in submucosal esophageal cancer using superparamagnetic iron oxide-enhanced magnetic resonance imaging: clinical validation study. World J Surg 2012;36:83-9. 10.1007/s00268-011-1322-1
    1. Motomura K, Izumi T, Tateishi S, Tamaki Y, Ito Y, Horinouchi T, Nakanishi K. Superparamagnetic iron oxide-enhanced MRI at 3 T for accurate axillary staging in breast cancer. Br J Surg 2016;103:60-9. 10.1002/bjs.10040
    1. Kuijs VJ, Moossdorff M, Schipper RJ, Beets-Tan RG, Heuts EM, Keymeulen KB, Smidt ML, Lobbes MB. The role of MRI in axillary lymph node imaging in breast cancer patients: a systematic review. Insights Imaging 2015;6:203-15. 10.1007/s13244-015-0404-2
    1. Mizokami D, Kosuda S, Tomifuji M, Araki K, Yamashita T, Shinmoto H, Shiotani A. Superparamagnetic iron oxide-enhanced interstitial magnetic resonance lymphography to detect a sentinel lymph node in tongue cancer patients. Acta Otolaryngol 2013;133:418-23. 10.3109/00016489.2012.744143
    1. Maki JH, Neligan PC, Briller N, Mitsumori LM, Wilson GJ. Dark Blood Magnetic Resonance Lymphangiography Using Dual-Agent Relaxivity Contrast (DARC-MRL): A Novel Method Combining Gadolinium and Iron Contrast Agents. Curr Probl Diagn Radiol 2016;45:174-9. 10.1067/j.cpradiol.2015.08.003
    1. Will O, Purkayastha S, Chan C, Althanasiou T, Darzi AW, Gedroyc W, Tekkis PP. Diagnostic precision of nanoparticle- enhanced MRI for lymph-node metastases: a meta-analysis. Lancet Oncol 2006;7:52-60. 10.1016/S1470-2045(05)70537-4
    1. Harnan SE, Cooper KL, Meng Y, Ward SE, Fitzgerald P, Papaioannou D, Ingram C, Lorenz E, Wilkinson ID, Wyld L. Magnetic resonance for assessment of axillary lymph node status in early breast cancer: a systematic review and meta-analysis. Eur J Surg Oncol 2011;37:928-36. 10.1016/j.ejso.2011.07.007
    1. Meng Y, Ward S, Cooper K, Harnan S, Wyld L. Cost effectiveness of MRI and PET imaging for the evaluation of axillary lymph node metastases in early stage breast cancer. Eur J Surg Oncol 2011;37:40-6. 10.1016/j.ejso.2010.10.001
    1. Minamiya Y, Ito M, Katayose Y, Saito H, Imai K, Sato Y, Ogawa J. Intraoperative sentinel lymph node mapping using a new sterilizable magnetometer in patients with nonsmall cell lung cancer. Ann Thorac Surg 2006;81:327-30. 10.1016/j.athoracsur.2005.06.005
    1. Imai K, Kawaharada Y, Ogawa J, Saito H, Kudo S, Takashima S, Saito Y, Atari M, Ito A, Terata K, Yoshino K, Sato Y, Motoyama S, Minamiya Y. Development of a New Magnetometer for Sentinel Lymph Node Mapping Designed for Video-Assisted Thoracic Surgery in Non-Small Cell Lung Cancer. Surg Innov 2015;22:401-5. 10.1177/1553350615585421
    1. Waanders S, Visscher M, Wildeboer RR, Oderkerk TO, Krooshoop HJ, Ten Haken B. A handheld SPIO-based sentinel lymph node mapping device using differential magnetometry. Phys Med Biol 2016;61:8120-34. 10.1088/0031-9155/61/22/8120
    1. Shiozawa M, Lefor AT, Hozumi Y, Kurihara K, Sata N, Yasuda Y, Kusakabe M. Sentinel lymph node biopsy in patients with breast cancer using superparamagnetic iron oxide and a magnetometer. Breast Cancer 2013;20:223-9. 10.1007/s12282-011-0327-9
    1. Karakatsanis A, Christiansen PM, Fischer L, Hedin C, Pistioli L, Sund M, Rasmussen NR, Jørnsgård H, Tegnelius D, Eriksson S, Daskalakis K, Wärnberg F, Markopoulos CJ, Bergkvist L. The Nordic SentiMag trial: a comparison of super paramagnetic iron oxide (SPIO) nanoparticles versus Tc(99) and patent blue in the detection of sentinel node (SN) in patients with breast cancer and a meta-analysis of earlier studies. Breast Cancer Res Treat 2016;157:281-94. 10.1007/s10549-016-3809-9
    1. Douek M, Klaase J, Monypenny I, Kothari A, Zechmeister K, Brown D, Wyld L, Drew P, Garmo H, Agbaje O, Pankhurst Q, Anninga B, Grootendorst M, Ten Haken B, Hall-Craggs MA, Purushotham A, Pinder S, SentiMAG Trialists Group . Sentinel node biopsy using a magnetic tracer versus standard technique: the SentiMAG Multicentre Trial. Ann Surg Oncol 2014;21:1237-45. 10.1245/s10434-013-3379-6
    1. Thill M, Kurylcio A, Welter R, van Haasteren V, Grosse B, Berclaz G, Polkowski W, Hauser N. The Central-European SentiMag study: sentinel lymph node biopsy with superparamagnetic iron oxide (SPIO) vs. radioisotope. Breast 2014;23:175-9. 10.1016/j.breast.2014.01.004
    1. Rubio IT, Diaz-Botero S, Esgueva A, Rodriguez R, Cortadellas T, Cordoba O, Espinosa-Bravo M. The superparamagnetic iron oxide is equivalent to the Tc99 radiotracer method for identifying the sentinel lymph node in breast cancer. Eur J Surg Oncol 2015;41:46-51. 10.1016/j.ejso.2014.11.006
    1. Piñero-Madrona A, Torró-Richart JA, de León-Carrillo JM, de Castro-Parga G, Navarro-Cecilia J, Domínguez-Cunchillos F, Román-Santamaría JM, Fuster-Diana C, Pardo-García R; Grupo de Estudios Senológicos de la Sociedad Española de Patologia Mamaria (SESPM). Superparamagnetic iron oxide as a tracer for sentinel node biopsy in breast cancer: A comparative non-inferiority study. Eur J Surg Oncol 2015;41:991-7. 10.1016/j.ejso.2015.04.017
    1. Ghilli M, Carretta E, Di Filippo F, Battaglia C, Fustaino L, Galanou I, Di Filippo S, Rucci P, Fantini MP, Roncella M. The superparamagnetic iron oxide tracer: a valid alternative in sentinel node biopsy for breast cancer treatment. Eur J Cancer Care (Engl) 2015. [Epub ahead of print]. doi: .10.1111/ecc.12385
    1. Houpeau JL, Chauvet MP, Guillemin F, Bendavid-Athias C, Charitansky H, Kramar A, Giard S. Sentinel lymph node identification using superparamagnetic iron oxide particles versus radioisotope: The French SentiMag feasibility trial. J Surg Oncol 2016;113:501-7. 10.1002/jso.24164
    1. Coufal O, Fait V, Lžičařová E, Chrenko V, Žaloudík J. SentiMag--the magnetic detection system of sentinel lymph nodes in breast cancer. Rozhl Chir 2015;94:283-8.
    1. Pouw JJ, Grootendorst MR, Bezooijen R, Klazen CA, De Bruin WI, Klaase JM, Hall-Craggs MA, Douek M, Ten Haken B. Pre-operative sentinel lymph node localization in breast cancer with superparamagnetic iron oxide MRI: the SentiMAG Multicentre Trial imaging subprotocol. Br J Radiol 2015;88:20150634. 10.1259/bjr.20150634
    1. Wang YX, Wang DW, Zhu XM, Zhao F, Leung KC. Carbon coated superparamagnetic iron oxide nanoparticles for sentinel lymph nodes mapping. Quant Imaging Med Surg 2012;2:53-6.
    1. Ahmed M, Usiskin SI, Hall-Craggs MA, Douek M. Is imaging the future of axillary staging in breast cancer? Eur Radiol 2014;24:288-93. 10.1007/s00330-013-3009-5
    1. Harisinghani MG, Saksena MA, Hahn PF, King B, Kim J, Torabi MT, Weissleder R. Ferumoxtran-10-enhanced MR lymphangiography: does contrast-enhanced imaging alone suffice for accurate lymph node characterization? AJR Am J Roentgenol 2006;186:144-8. 10.2214/AJR.04.1287
    1. Islam T, Harisinghani MG. Overview of nanoparticle use in cancer imaging. Cancer Biomark 2009;5:61-7. 10.3233/CBM-2009-0578
    1. Heesakkers RA, Hövels AM, Jager GJ, van den Bosch HC, Witjes JA, Raat HP, Severens JL, Adang EM, van der Kaa CH, Fütterer JJ, Barentsz J. 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 2008;9:850-6. 10.1016/S1470-2045(08)70203-1
    1. Lahaye MJ, Engelen SM, Kessels AG, de Bruïne AP, von Meyenfeldt MF, van Engelshoven JM, van de Velde CJ, Beets GL, Beets-Tan RG. USPIO-enhanced MR imaging for nodal staging in patients with primary rectal cancer: predictive criteria. Radiology 2008;246:804-11. 10.1148/radiol.2463070221
    1. Fortuin AS, Deserno WM, Meijer HJ, Jager GJ, Takahashi S, Debats OA, Reske SN, Schick C, Krause BJ, van Oort I, Witjes AJ, Hoogeveen YL, van Lin EN, Barentsz JO. Value of PET/CT and MR lymphography in treatment of prostate cancer patients with lymph node metastases. Int J Radiat Oncol Biol Phys 2012;84:712-8. 10.1016/j.ijrobp.2011.12.093
    1. Suzuki D, Yamaguchi M, Furuta T, Okuyama Y, Yoshikawa K, Fujii H. Central high signal in inflammatory swollen lymph nodes on SPIO-enhanced interstitial MR lymphograms: a mimic of lymph node metastasis. Magn Reson Med Sci 2012;11:61-3. 10.2463/mrms.11.61
    1. Triantafyllou M, Studer UE, Birkhäuser FD, Fleischmann A, Bains LJ, Petralia G, Christe A, Froehlich JM, Thoeny HC. Ultrasmall superparamagnetic particles of iron oxide allow for the detection of metastases in normal sized pelvic lymph nodes of patients with bladder and/or prostate cancer. Eur J Cancer 2013;49:616-24. 10.1016/j.ejca.2012.09.034
    1. Smith JT, Ward J, Guthrie JA, Sheridan MB, Boyes S, Wilson D, Wyatt JI, Treanor D, Robinson PJ. Detection of colorectal metastases in patients being treated with chemotherapy utilising SPIO-MRI: a radiological-pathological study. Magn Reson Imaging 2012;30:1446-53. 10.1016/j.mri.2012.04.016
    1. Fortuin AS, Barentsz JO. Comments on Ultrasmall superparamagnetic particles of iron oxide allow for the detection of metastases in normal sized pelvic lymph nodes of patients with bladder and/or prostate cancer, Triantafyllou et al., European Journal of Cancer, published online 22 October 2012. Eur J Cancer 2013;49:1789-90.
    1. Froehlich JM, Triantafyllou M, Fleischmann A, Vermathen P, Thalmann GN, Thoeny HC. Does quantification of USPIO uptake-related signal loss allow differentiation of benign and malignant normal-sized pelvic lymph nodes? Contrast Media Mol Imaging 2012;7:346-55. 10.1002/cmmi.503
    1. McDermott S, Thayer SP, Fernandez-Del Castillo C, Mino-Kenudson M, Weissleder R, Harisinghani MG. Accurate prediction of nodal status in preoperative patients with pancreatic ductal adenocarcinoma using next-gen nanoparticle. Transl Oncol 2013;6:670-5. 10.1593/tlo.13400
    1. Turkbey B, Agarwal HK, Shih J, Bernardo M, McKinney YL, Daar D, Griffiths GL, Sankineni S, Johnson L, Grant KB, Weaver J, Rais-Bahrami S, Harisinghani M, Jacobs P, Dahut W, Merino MJ, Pinto PA, Choyke PL. A Phase I Dosing Study of Ferumoxytol for MR Lymphography at 3 T in Patients With Prostate Cancer. AJR Am J Roentgenol 2015;205:64-9. 10.2214/AJR.14.13009
    1. Atri M, Zhang Z, Marques H, Gorelick J, Harisinghani M, Sohaib A, Koh DM, Raman S, Gee M, Choi H, Landrum L, Mannel R, Chuang L, Yu JQ, McCourt CK, Gold M. Utility of preoperative ferumoxtran-10 MRI to evaluate retroperitoneal lymph node metastasis in advanced cervical cancer: Results of ACRIN 6671/GOG 0233. Eur J Radiol Open 2015;2:11-8. 10.1016/j.ejro.2014.11.002
    1. Wang YX, Lam WW. Characterisation of brain disorders and evaluation of therapy by functional and molecular magnetic resonance techniques. Hong Kong Med J 2008;14:469-78.
    1. Crowe LA, Wang YX, Gatehouse P, Tessier J, Waterton J, obert R, Bydder G, Firmin DN. Ex vivo MR imaging of atherosclerotic rabbit aorta labeled with USPIO- enhancement of iron loaded regions in UTE imaging. Proc Intl Soc Mag Reson Med 2005:115 Available online:
    1. Tourdias T, Roggerone S, Filippi M, Kanagaki M, Rovaris M, Miller DH, Petry KG, Brochet B, Pruvo JP, Radüe EW, Dousset V. Assessment of disease activity in multiple sclerosis phenotypes with combined gadolinium- and superparamagnetic iron oxide-enhanced MR imaging. Radiology 2012;264:225-33. 10.1148/radiol.12111416
    1. Crimi A, Commowick O, Maarouf A, Ferré JC, Bannier E, Tourbah A, Berry I, Ranjeva JP, Edan G, Barillot C. Predictive value of imaging markers at multiple sclerosis disease onset based on gadolinium- and USPIO-enhanced MRI and machine learning. PLoS One 2014;9:e93024. 10.1371/journal.pone.0093024
    1. Maarouf A, Ferré JC, Zaaraoui W, Le Troter A, Bannier E, Berry I, Guye M, Pierot L, Barillot C, Pelletier J, Tourbah A, Edan G, Audoin B, Ranjeva JP. Ultra-small superparamagnetic iron oxide enhancement is associated with higher loss of brain tissue structure in clinically isolated syndrome. Mult Scler 2016;22:1032-9. 10.1177/1352458515607649
    1. Farrell BT, Hamilton BE, Dósa E, Rimely E, Nasseri M, Gahramanov S, Lacy CA, Frenkel EP, Doolittle ND, Jacobs PM, Neuwelt EA. Using iron oxide nanoparticles to diagnose CNS inflammatory diseases and PCNSL. Neurology 2013;81:256-63. 10.1212/WNL.0b013e31829bfd8f
    1. Kooi ME, Cappendijk VC, Cleutjens KB, Kessels AG, Kitslaar PJ, Borgers M, Frederik PM, Daemen MJ, van Engelshoven JM. Accumulation of ultrasmall superparamagnetic particles of iron oxide in human atherosclerotic plaques can be detected in vivo magnetic resonance imaging. Circulation 2003;107:2453-8. 10.1161/
    1. Trivedi RA, Mallawarachi C, U-King-Im JM, Graves MJ, Horsley J, Goddard MJ, Brown A, Wang L, Kirkpatrick PJ, Brown J, Gillard JH. Identifying inflamed carotid plaques using in vivo USPIO-enhanced MR imaging to label plaque macrophages. Arterioscler Thromb Vasc Biol 2006;26:1601-6. 10.1161/01.ATV.0000222920.59760.df
    1. Tang T, Howarth SP, Miller SR, Trivedi R, Graves MJ, King-Im JU, Li ZY, Brown AP, Kirkpatrick PJ, Gaunt ME, Gillard JH. Assessment of inflammatory burden contralateral to the symptomatic carotid stenosis using high resolution ultrasmall, superparamagnetic iron oxide-enhanced MRI. Stroke 2006;37:2266-70. 10.1161/01.STR.0000236063.47539.99
    1. Matijevic N, Wu KK, Howard AG, Wasserman B, Wang WY, Folsom AR, Sharrett AR: Association of blood monocyte and platelet markers with carotid artery characteristics: the Atherosclerosis Risk in Communities Carotid MRI study. Cerebrovasc Dis 2011;31:552-8. 10.1159/000324389
    1. Katsargyris A, Tsiodras S, Theocharis S, Giaginis K, Vasileiou I, Bakoyiannis C, Georgopoulos S, Bastounis E, Klonaris C: Toll-like receptor 4 immunohistochemical expression is enhanced in macrophages of symptomatic carotid atherosclerotic plaques. Cerebrovasc Dis 2011;31:29-36. 10.1159/000320259
    1. Howarth SP, Tang TY, Trivedi R, Weerakkody R, U-King-Im JM, Gaunt ME, Boyle JR, Li ZY, Miller SR, Graves MJ, Gillard JH: Utility of USPIO- enhanced MR imaging to identify inflammation and the fibrous cap: a comparison of symptomatic and asymptomatic individuals. Eur J Radiol 2009;70:555-60. 10.1016/j.ejrad.2008.01.047
    1. Degnan AJ, Patterson AJ, Tang TY, Howarth SP, Gillard JH. Evaluation of ultrasmall superparamagnetic iron oxide-enhanced MRI of carotid atherosclerosis to assess risk of cerebrovascular and cardiovascular events: follow-up of the ATHEROMA trial. Cerebrovasc Dis 2012;34:169-73. 10.1159/000339984
    1. Yancy AD, Olzinski AR, Hu TC, Lenhard SC, Aravindhan K, Gruver SM, Jacobs PM, Willette RN, Jucker BM. Differential uptake of ferumoxtran-10 and ferumoxytol ultrasmall superparamagnetic iron oxide contrast agents in rabbits: critical determinants of atherosclerotic plaque labeling. J. Magn Reson Imaging 2005;21:432-42. 10.1002/jmri.20283
    1. Jayaraman T, Berenstein V, Li X, Mayer J, Silane M, Shin YS, Niimi Y, Kiliç T, Gunel M, Berenstein A. Tumor necrosis factor alpha is a key modulator of inflammation in cerebral aneurysms. Neurosurgery 2005;57:558-564; discussion 64. 10.1227/01.NEU.0000170439.89041.D6
    1. Jayaraman T, Paget A, Shin YS, Li X, Mayer J, Chaudhry H, Niimi Y, Silane M, Berenstein A. TNF-alpha-mediated inflammation in cerebral aneurysms: a potential link to growth and rupture. Vasc Health Risk Manag 2008;4:805-17. 10.2147/VHRM.S2700
    1. Chalouhi N, Ali MS, Jabbour PM, Tjoumakaris SI, Gonzalez LF, Rosenwasser RH, Koch WJ, Dumont AS. Biology of intracranial aneurysms: role of inflammation. J Cereb Blood Flow Metab 2012;32:1659-76. 10.1038/jcbfm.2012.84
    1. Hasan D, Chalouhi N, Jabbour P, Dumont AS, Kung DK, Magnotta VA, Young WL, Hashimoto T, Winn HR, Heistad D. Early change in ferumoxytol-enhanced magnetic resonance imaging signal suggests unstable human cerebral aneurysm: a pilot study. Stroke 2012;43:3258-65. 10.1161/STROKEAHA.112.673400
    1. Hasan DM, Chalouhi N, Jabbour P, Magnotta VA, Kung DK, Young WL. Imaging aspirin effect on macrophages in the wall of human cerebral aneurysms using ferumoxytol-enhanced MRI: preliminary results. J Neuroradiol 2013;40:187-91. 10.1016/j.neurad.2012.09.002
    1. Hasan DM, Chalouhi N, Jabbour P, Dumont AS, Kung DK, Magnotta VA, Young WL, Hashimoto T, Richard Winn H, Heistad D. Evidence that acetylsalicylic acid attenuates inflammation in the walls of human cerebral aneurysms: preliminary results. J Am Heart Assoc 2013;2:e000019. 10.1161/JAHA.112.000019
    1. McBride OM, Joshi NV, Robson JM, MacGillivray TJ, Gray CD, Fletcher AM, Dweck MR, van Beek EJ, Rudd JH, Newby DE, Semple SI. Positron Emission Tomography and Magnetic Resonance Imaging of Cellular Inflammation in Patients with Abdominal Aortic Aneurysms. Eur J Vasc Endovasc Surg 2016;51:518-26. 10.1016/j.ejvs.2015.12.018
    1. Jalalzadeh H, Indrakusuma R, Planken RN, Legemate DA, Koelemay MJ, Balm R. Inflammation as a Predictor of Abdominal Aortic Aneurysm Growth and Rupture: A Systematic Review of Imaging Biomarkers. Eur J Vasc Endovasc Surg 2016;52:333-42. 10.1016/j.ejvs.2016.05.002
    1. McBride OM, Berry C, Burns P, Chalmers RT, Doyle B, Forsythe R, Garden OJ, Goodman K, Graham C, Hoskins P, Holdsworth R, MacGillivray TJ, McKillop G, Murray G, Oatey K, Robson JM, Roditi G, Semple S, Stuart W, van Beek EJ, Vesey A, Newby DE. MRI using ultrasmall superparamagnetic particles of iron oxide in patients under surveillance for abdominal aortic aneurysms to predict rupture or surgical repair: MRI for abdominal aortic aneurysms to predict rupture or surgery-the MA(3)RS study. Open Heart 2015;2:e000190. 10.1136/openhrt-2014-000190
    1. Gaglia JL, Harisinghani M, Aganj I, Wojtkiewicz GR, Hedgire S, Benoist C, Mathis D, Weissleder R. Noninvasive mapping of pancreatic inflammation in recent-onset type-1 diabetes patients. Proc Natl Acad Sci U S A 2015;112:2139-44. 10.1073/pnas.1424993112
    1. Malosio ML, Esposito A, Brigatti C, Palmisano A, Piemonti L, Nano R, Maffi P, De Cobelli F, Del Maschio A, Secchi A. MR imaging monitoring of iron-labeled pancreatic islets in a small series of patients: islet fate in successful, unsuccessful, and autotransplantation. Cell Transplant 2015;24:2285-96. 10.3727/096368914X684060
    1. Alam SR, Shah AS, Richards J, Lang NN, Barnes G, Joshi N, MacGillivray T, McKillop G, Mirsadraee S, Payne J, Fox KA, Henriksen P, Newby DE, Semple SI. Ultrasmall superparamagnetic particles of iron oxide in patients with acute myocardial infarction: early clinical experience. Circ Cardiovasc Imaging 2012;5:559-65. 10.1161/CIRCIMAGING.112.974907
    1. Yilmaz A, Rösch S, Yildiz H, Klumpp S, Sechtem U. First multiparametric cardiovascular magnetic resonance study using ultrasmall superparamagnetic iron oxide nanoparticles in a patient with acute myocardial infarction: new vistas for the clinical application of ultrasmall superparamagnetic iron oxide. Circulation 2012;126:1932-4. 10.1161/CIRCULATIONAHA.112.108167
    1. Yilmaz A, Dengler MA, van der Kuip H, Yildiz H, Rösch S, Klumpp S, Klingel K, Kandolf R, Helluy X, Hiller KH, Jakob PM, Sechtem U. Imaging of myocardial infarction using ultrasmall superparamagnetic iron oxide nanoparticles: a human study using a multi-parametric cardiovascular magnetic resonance imaging approach. Eur Heart J 2013;34:462-75. 10.1093/eurheartj/ehs366
    1. Richards JM, Shaw CA, Lang NN, Williams MC, Semple SI, MacGillivray TJ, Gray C, Crawford JH, Alam SR, Atkinson AP, Forrest EK, Bienek C, Mills NL, Burdess A, Dhaliwal K, Simpson AJ, Wallace WA, Hill AT, Roddie PH, McKillop G, Connolly TA, Feuerstein GZ, Barclay GR, Turner ML, Newby DE. In vivo mononuclear cell tracking using superparamagnetic particles of iron oxide: feasibility and safety in humans. Circ Cardiovasc Imaging 2012;5:509-17. 10.1161/CIRCIMAGING.112.972596
    1. Tanaka M, Nakashima O, Wada Y, Kage M, Kojiro M. Pathomorphological study of Kupffer cells in hepatocellular carcinoma and hyperplastic nodular lesions in the liver. Hepatology 1996;24:807-12. 10.1002/hep.510240409
    1. Kim YK, Kim CS, Kwak HS, Lee JM. Three-dimensional dynamic liver MR imaging using sensitivity encoding for detection of hepatocellular carcinomas: comparison with superparamagnetic iron oxide-enhanced MR imaging. J Magn Reson Imaging 2004;20:826-37. 10.1002/jmri.20188
    1. Lee JM, Park JW, Choi BI. 2014 KLCSG-NCC Korea Practice Guidelines for the management of hepatocellular carcinoma: HCC diagnostic algorithm. Dig Dis 2014;32:764-77. 10.1159/000368020
    1. Nishie A, Asayama Y, Ishigami K, Tajima T, Kakihara D, Nakayama T, Takayama Y, Okamoto D, Taketomi A, Shirabe K, Fujita N, Obara M, Yoshimitsu K, Honda H. MR prediction of liver fibrosis using a liver-specific contrast agent: Superparamagnetic iron oxide versus Gd-EOB-DTPA. J Magn Reson Imaging 2012;36:664-71. 10.1002/jmri.23691
    1. Saito K, Yoshimura N, Saguchi T, Park J, Sugimoto K, Akata S, Moriyasu F, Tokuuye K. MR characterization of focal nodular hyperplasia: gadoxetic acid versus superparamagnetic iron oxide imaging. Magn Reson Med Sci 2012;11:163-9. 10.2463/mrms.11.163
    1. Bahl G, Cruite I, Wolfson T, Gamst AC, Collins JM, Chavez AD, Barakat F, Hassanein T, Sirlin CB. Noninvasive classification of hepatic fibrosis based on texture parameters from double contrast-enhanced magnetic resonance images. J Magn Reson Imaging 2012;36:1154-61. 10.1002/jmri.23759
    1. Yokoo T, Wolfson T, Iwaisako K, Peterson MR, Mani H, Goodman Z, Changchien C, Middleton MS, Gamst AC, Mazhar SM, Kono Y, Ho SB, Sirlin CB. Evaluation of Liver Fibrosis Using Texture Analysis on Combined-Contrast-Enhanced Magnetic Resonance Images at 3.0T. Biomed Res Int 2015;2015:387653.
    1. Tanaka Y, Nakazawa T, Inoue T, Yamane K, Kubota K, Uojima H, Takada J, Okuwaki Y, Hidaka H, Shibuya A, Kokubu S, Matsunaga K, Koizumi W. SPIO-enhanced MRI is useful in predicting malignant potential of vascular transformation of hypointense hypovascular nodules on Gd-EOB-DTPA-enhanced MRI. Hepatol Res 2016. [Epub ahead of print]. doi: .10.1111/hepr.12850
    1. Teerasamit W, Saiviroonporn P, Pongpaibul A, Korpraphong P. Benefit of double contrast MRI in diagnosis of hepatocellular carcinoma in patients with chronic liver diseases. J Med Assoc Thai 2014;97:540-7.
    1. Maurea S, Mainenti PP, Tambasco A, Imbriaco M, Mollica C, Laccetti E, Camera L, Liuzzi R, Salvatore M. Diagnostic accuracy of MR imaging to identify and characterize focal liver lesions: comparison between gadolinium and superparamagnetic iron oxide contrast media. Quant Imaging Med Surg 2014;4:181-9.
    1. Liau J, Shiehmorteza M, Girard OM, Sirlin CB, Bydder M. Evaluation of MRI fat fraction in the liver and spine pre and post SPIO infusion. Magn Reson Imaging 2013;31:1012-6. 10.1016/j.mri.2013.01.016
    1. Mikolasevic I, Orlic L, Franjic N, Hauser G, Stimac D, Milic S. Transient elastography (FibroScan(®)) with controlled attenuation parameter in the assessment of liver steatosis and fibrosis in patients with nonalcoholic fatty liver disease - Where do we stand? World J Gastroenterol 2016;22:7236-51. 10.3748/wjg.v22.i32.7236
    1. Allkemper T, Sagmeister F, Cicinnati V, Beckebaum S, Kooijman H, Kanthak C, Stehling C, Heindel W. Evaluation of fibrotic liver disease with whole-liver T1ρ MR imaging: a feasibility study at 1.5 T. Radiology 2014;271:408-15. 10.1148/radiol.13130342
    1. Koon CM, Zhang X, Chen W, Chu ES, San Lau CB, Wáng YX. Black blood T1rho MR imaging may diagnose early stage liver fibrosis: a proof-of-principle study with rat biliary duct ligation model. Quant Imaging Med Surg 2016;6:353-363. 10.21037/qims.2016.08.11
    1. Karlas T, Petroff D, Sasso M, Fan JG, Mi YQ, de Lédinghen V, Kumar M, Lupsor-Platon M, Han KH, Cardoso AC, Ferraioli G, Chan WK, Wai-Sun Wong V, Myers RP, Chayama K, Friedrich-Rust M, Beaugrand M, Shen F, Hiriart JB, Sarin SK, Badea R, Sik Jung K, Marcellin P, Filice C, Mahadeva S, Lai-Hung Wong G, Crotty P, Masaki K, Bojunga J, Bedossa P, Keim V, Wiegand J. Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol 2016. [Epub ahead of print]. doi: .10.1016/j.jhep.2016.12.022
    1. Varallyay CG, Nesbit E, Fu R, Gahramanov S, Moloney B, Earl E, Muldoon LL, Li X, Rooney WD, Neuwelt EA. 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 Metab 2013;33:780-6. 10.1038/jcbfm.2013.36
    1. Hanneman K, Kino A, Cheng JY, Alley MT, Vasanawala SS. Assessment of the precision and reproducibility of ventricular volume, function, and mass measurements with ferumoxytol-enhanced 4D flow MRI. J Magn Reson Imaging 2016;44:383-92. 10.1002/jmri.25180
    1. Fredrickson J, Serkova NJ, Wyatt SK, Carano RA, Pirzkall A, Rhee I, Rosen LS, Bessudo A, Weekes C, de Crespigny A. Clinical translation of ferumoxytol-based vessel size imaging (VSI): Feasibility in a phase I oncology clinical trial population. Magn Reson Med 2017;77:814-25. 10.1002/mrm.26167
    1. Nasseri M, Gahramanov S, Netto JP, Fu R, Muldoon LL, Varallyay C, Hamilton BE, Neuwelt EA. Evaluation of pseudoprogression in patients with glioblastoma multiforme using dynamic magnetic resonance imaging with ferumoxytol calls RANO criteria into question. Neuro Oncol 2014;16:1146-54. 10.1093/neuonc/not328
    1. Gahramanov S, Muldoon LL, Varallyay CG, Li X, Kraemer DF, Fu R, Hamilton BE, Rooney WD, Neuwelt EA. 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 2013;266:842-52. 10.1148/radiol.12111472
    1. Netto JP, Schwartz D, Varallyay C, Fu R, Hamilton B, Neuwelt EA. Misleading early blood volume changes obtained using ferumoxytol-based magnetic resonance imaging perfusion in high grade glial neoplasms treated with bevacizumab. Fluids Barriers CNS 2016;13:23. 10.1186/s12987-016-0047-9
    1. Qiu D, Zaharchuk G, Christen T, Ni WW, Moseley ME. Contrast-enhanced functional blood volume imaging (CE-fBVI): enhanced sensitivity for brain activation in humans using the ultrasmall superparamagnetic iron oxide agent ferumoxytol. Neuroimage 2012;62:1726-31. 10.1016/j.neuroimage.2012.05.010
    1. Mandeville JB. IRON fMRI measurements of CBV and implications for BOLD signal. Neuroimage 2012;62:1000-8. 10.1016/j.neuroimage.2012.01.070
    1. Baumgartner R, Cho W, Coimbra A, Chen C, Wang Z, Struyk A, Venketasubramanian N, Low M, Gargano C, Zhao F, Williams D, Reese T, Seah S, Feng D, Apreleva S, Petersen E, Evelhoch JL. Evaluation of an fMRI USPIO-based assay in healthy human volunteers. J Magn Reson Imaging 2016. [Epub ahead of print]. doi: .10.1002/jmri.25499
    1. D'Arceuil H, Coimbra A, Triano P, Dougherty M, Mello J, Moseley M, Glover G, Lansberg M, Blankenberg F. Ferumoxytol enhanced resting state fMRI and relative cerebral blood volume mapping in normal human brain. Neuroimage 2013;83:200-9. 10.1016/j.neuroimage.2013.06.066
    1. Florian A, Ludwig A, Rösch S, Yildiz H, Klumpp S, Sechtem U, Yilmaz A. Positive effect of intravenous iron-oxide administration on left ventricular remodelling in patients with acute ST-elevation myocardial infarction - a cardiovascular magnetic resonance (CMR) study. Int J Cardiol 2014;173:184-9. 10.1016/j.ijcard.2014.02.016
    1. Smits LP, Coolen BF, Panno MD, Runge JH, Nijhof WH, Verheij J, Nieuwdorp M, Stoker J, Beuers UH, Nederveen AJ, Stroes ES. Noninvasive Differentiation between Hepatic Steatosis and Steatohepatitis with MR Imaging Enhanced with USPIOs in Patients with Nonalcoholic Fatty Liver Disease: A Proof-of-Concept Study. Radiology 2016;278:782-91. 10.1148/radiol.2015150952
    1. Gleich B, Weizenecker J. Tomographic imaging using the nonlinear response of magnetic particles. Nature 2005;435:1214-7. 10.1038/nature03808
    1. Konkle JJ, Goodwill PW, Carrasco-Zevallos OM, Conolly SM. Projection reconstruction magnetic particle imaging. IEEE Trans Med Imaging 2013;32:338-47. 10.1109/TMI.2012.2227121
    1. Haegele J, Rahmer J, Gleich B, Borgert J, Wojtczyk H, Panagiotopoulos N, Buzug TM, Barkhausen J, Vogt FM. Magnetic particle imaging: visualization of instruments for cardiovascular intervention. Radiology 2012;265:933-8. 10.1148/radiol.12120424
    1. Haegele J, Panagiotopoulos N, Cremers S, Rahmer JR, Franke J, Duschka RL, Vaalma S, Heidenreich M, Borgert JR, Borm P, Barkhausen JR, Vogt FM. Magnetic Particle Imaging: A Resovist Based Marking Technology for Guide Wires and Catheters for Vascular Interventions. IEEE Trans Med Imaging 2016;35:2312-8. 10.1109/TMI.2016.2559538
    1. Haegele J, Vaalma S, Panagiotopoulos N, Barkhausen J, Vogt FM, Borgert J, Rahmer J. Multi-color magnetic particle imaging for cardiovascular interventions. Phys Med Biol 2016;61:N415-26.
    1. Kakite S, Fujii S, Nakamatsu S, Kanasaki Y, Yamashita E, Matsusue E, Ouchi Y, Kaminou T, Tokunaga S, Koda M, Ogawa T. Usefulness of administration of SPIO prior to RF ablation for evaluation of the therapeutic effect: an experimental study using miniature pigs. Eur J Radiol 2011;78:282-6. 10.1016/j.ejrad.2011.01.048
    1. Cheng KK, Chan PS, Fan S, Kwan SM, Yeung KL, Wáng YX, Chow AH, Wu EX, Baum L. Curcumin-conjugated magnetic nanoparticles for detecting amyloid plaques in Alzheimer's disease mice using magnetic resonance imaging (MRI). Biomaterials 2015;44:155-72. 10.1016/j.biomaterials.2014.12.005
    1. Haacke EM, Xu Y, Cheng YC, Reichenbach JR. Susceptibility weighted imaging (SWI). Magn Reson Med 2004;52:612-8. 10.1002/mrm.20198
    1. Sehgal V, Delproposto Z, Haacke EM, Tong KA, Wycliffe N, Kido DK, Xu Y, Neelavalli J, Haddar D, Reichenbach JR. Clinical applications of neuroimaging with susceptibility-weighted imaging. J Magn Reson Imaging 2005;22:439-50. 10.1002/jmri.20404
    1. Acosta-Cabronero J, Williams GB, Cardenas-Blanco A, Arnold RJ, Lupson V, Nestor PJ. In vivo quantitative susceptibility mapping (QSM) in Alzheimer's disease. PLoS One 2013;8:e81093. 10.1371/journal.pone.0081093
    1. Patil R, Gangalum PR, Wagner S, Portilla-Arias J, Ding H, Rekechenetskiy A, Konda B, Inoue S, Black KL, Ljubimova JY, Holler E. Curcumin Targeted, Polymalic Acid-Based MRI Contrast Agent for the Detection of Aβ Plaques in Alzheimer's Disease. Macromol Biosci 2015;15:1212-7. 10.1002/mabi.201500062
    1. Ohno K, Akashi T, Tsujii Y, Yamamoto M, Tabata Y. Blood clearance and biodistribution of polymer brush-afforded silica particles prepared by surface-initiated living radical polymerization. Biomacromolecules 2012;13:927-36. 10.1021/bm201855m
    1. Ohno K, Mori C, Akashi T, Yoshida S, Tago Y, Tsujii Y, Tabata Y. Fabrication of contrast agents for magnetic resonance imaging from polymer-brush-afforded iron oxide magnetic nanoparticles prepared by surface-initiated living radical polymerization. Biomacromolecules 2013;14:3453-62. 10.1021/bm400770n
    1. Chen T, Mori Y, Inui-Yamamoto C, Komai Y, Tago Y, Yoshida S, Takabatake Y, Isaka Y, Ohno K, Yoshioka Y. Polymer-brush-afforded SPIO Nanoparticles Show a Unique Biodistribution and MR Imaging Contrast in Mouse Organs. Magn Reson Med Sci 2017. [Epub ahead of print]. doi: .10.2463/mrms.mp.2016-0067
    1. Cukur T, Yamada M, Overall WR, Yang P, Nishimura DG. Positive contrast with alternating repetition time SSFP (PARTS): a fast imaging technique for SPIO-labeled cells. Magn Reson Med 2010;63:427-37. 10.1002/mrm.22241
    1. Chen W. Artifacts correction for T1rho imaging with constant amplitude spin-lock. J Magn Reson 2017;274:13-23. 10.1016/j.jmr.2016.11.002
    1. Chen W. Errors in quantitative T1rho imaging and the correction methods. Quant Imaging Med Surg 2015;5:583-91.
    1. Stuber M, Gilson WD, Schär M, Kedziorek DA, Hofmann LV, Shah S, Vonken EJ, Bulte JW, Kraitchman DL. Positive contrast visualization of iron oxide-labeled stem cells using inversion-recovery with ON-resonant water suppression (IRON). Magn Reson Med 2007;58:1072-7. 10.1002/mrm.21399
    1. Pelot NA, Bowen CV. Quantification of superparamagnetic iron oxide using inversion recovery balanced steady-state free precession. Magn Reson Imaging 2013;31:953-60. 10.1016/j.mri.2013.03.010
    1. Wang L, Corum CA, Idiyatullin D, Garwood M, Zhao Q. T1 estimation for aqueous iron oxide nanoparticle suspensions using a variable flip angle SWIFT sequence. Magn Reson Med 2013;70:341-7. 10.1002/mrm.24831
    1. Moonen RP, van der Tol P, Hectors SJ, Starmans LW, Nicolay K, Strijkers GJ. Spin-lock MR enhances the detection sensitivity of superparamagnetic iron oxide particles. Magn Reson Med 2015;74:1740-9. 10.1002/mrm.25544

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