Positive Contrast Visualization of Iron Oxide-Labeled Stem Cells using Inversion-Recovery With ON-Resonant Water Suppression (IRON)

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1 Magnetic Resonance in Medicine 58: (2007) Positive Contrast Visualization of Iron Oxide-Labeled Stem Cells using Inversion-Recovery With ON-Resonant Water Suppression (IRON) Matthias Stuber, 1 3 * Wesley D. Gilson, 1 Michael Schär, 1,4 Dorota A. Kedziorek, 1,5 Lawrence V. Hofmann, 6 Saurabh Shah, 1 Evert-Jan Vonken, 1 Jeff W.M. Bulte, 1,5,7 and Dara L. Kraitchman 1 In proton magnetic resonance imaging (MRI) metallic substances lead to magnetic field distortions that often result in signal voids in the adjacent anatomic structures. Thus, metallic objects and superparamagnetic iron oxide (SPIO)-labeled cells appear as hypointense artifacts that obscure the underlying anatomy. The ability to illuminate these structures with positive contrast would enhance noninvasive MR tracking of cellular therapeutics. Therefore, an MRI methodology that selectively highlights areas of metallic objects has been developed. Inversion-recovery with ON-resonant water suppression (IRON) employs inversion of the magnetization in conjunction with a spectrally-selective on-resonant saturation prepulse. If imaging is performed after these prepulses, positive signal is obtained from off-resonant protons in close proximity to the metallic objects. The first successful use of IRON to produce positive contrast in areas of metallic spheres and SPIO-labeled stem cells in vitro and in vivo is presented. Magn Reson Med 58: , Wiley-Liss, Inc. Key words: positive contrast imaging; off-resonance imaging; SPIO-labeled stem cells; metallic objects; white-marker objects In magnetic resonance imaging (MRI), a homogeneous main magnetic field B 0 is mandatory for unambiguous image formation. Even minor perturbations can cause significant problems and should be avoided. However, this 1 Russell H. Morgan Department of Radiology and Radiological Science, Division of MR Research, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA. 2 Department of Electrical and Computer Engineering, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA. 3 Department of Medicine, Cardiology Division, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA. 4 Philips Medical Systems, Cleveland, Ohio, USA. 5 Institute for Cell Engineering, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA. 6 Interventional Radiology, Stanford University School of Medicine, Stanford, California, USA. 7 Department of Chemical and Biomolecular Engineering, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA. Grant sponsor: Biomedical Engineering Grant, Whitaker Foundation; Grant number: RG ; Grant sponsor: National Institutes of Health (NIH); Grant numbers: RO1 HL084186, RO1 HL061912, RO1 HL073223, RO1 NS045062, RO1 K08 EB Matthias Stuber is compensated as a consultant by Philips Medical Systems NL, the manufacturer of equipment described in this presentation. The terms of this arrangement have been approved by the Johns Hopkins University in accordance with its conflict of interest policies. *Correspondence to: Matthias Stuber, PhD, The Johns Hopkins University School of Medicine, Russell H. Morgan Department of Radiology and Radiological Science; JHOC 4223, 601 North Caroline St., Baltimore, MD, mstuber@mri.jhu.edu Received 21 February 2007; revised 15 June 2007; accepted 1 August DOI /mrm Published online in Wiley InterScience ( Wiley-Liss, Inc sensitivity to magnetic field disturbances has also been exploited (1) for the visualization and tracking of superparamagnetic iron oxide (SPIO)-labeled cellular therapeutics (2). The magnetic field susceptibility created by these SPIOs can be detected as signal voids in the MR images (3). Therefore, specific regions of signal loss on MRI are associated with cell persistence or migration. Unfortunately, it is often challenging to distinguish signal voids associated with the SPIOs from other competing sources of hypointense signal, such as motion artifacts, calcifications, signal cancellations at water-fat interfaces, or air. Therefore, MRI methods that generate positive contrast in regions of magnetic field susceptibility have recently been developed (4 6). However, these techniques are limited to either gradient-echo (GRE) (5,6) or spin-echo imaging (4), require a modification of the imaging part of the MR sequence (4 6), or employ projection imaging only (4) with inability to perform two-dimensional (2D) slice selection or 3D spatial encoding as associated shortcomings. Accordingly, it was our objective to develop a versatile MRI methodology (inversion recovery with ON-resonant water suppression IRON) that enables the positive contrast visualization of the surroundings of magnetically labeled stem cells in 2D and 3D without requiring modifications of the imaging part of the MR sequence. The in vitro and in vivo results obtained with IRON are presented. MATERIALS AND METHODS Background and Concept Consider a spherical object with a susceptibility gradient coefficient in a homogeneous static magnetic field B 0. This object with the radius a generates an external magnetic field disturbance described by B r, External K a 3 3 r 3 3cos 2 1 B 0 [1] where r refers to any given point distant from the object ( r a) and to the angle between r and B 0. With the gyromagnetic ratio for protons, the external frequency shift generated by this object is External B External. [2] Using Eqs. [1] and [2], it is evident that the presence of an object that leads to a susceptibility gradient coefficient

2 Positive-Contrast With IRON MRI 1073 characteristically introduces components to the frequency spectrum which are distinct from 0 B 0 (Fig. 1a). By deliberately adding a spectrally selective on-resonant radio frequency (RF) saturation pulse with a limited bandwidth ( BW Sat ) prior to the imaging part of a pulse sequence, signal originating from on-resonant water protons is suppressed (Fig. 1b). However, this saturation pulse does not affect off-resonant protons near the susceptibilitygenerating particle (Fig. 1b). Therefore, positive contrast in close proximity to these particles can be generated. The size of the area with positive signal can simply be controlled by BW Sat, and the level of background suppression can be adjusted with the angle Sat of this RF pulse. A pulse sequence diagram is displayed in Fig. 1c together with the longitudinal magnetization of off-resonant (Fig. 1d) and on-resonant (Fig. 1e) protons. With on-resonant water suppression, the longitudinal magnetization of on-resonant protons can be nulled at the imaging time point. Simultaneously, the longitudinal magnetization of off-resonant protons and fat remains unaffected. Therefore, if this saturation pulse precedes the imaging part of the sequence, signal from off-resonant protons is maintained while that of on-resonant protons is suppressed. Selective fat signal suppression is achieved by the additional use of a broadband dual-inversion prepulse (Fig. 2c), which nulls signal from species with short T 1 such as fat. Implementation IRON was implemented on commercial 1.5T Intera and 3T Achieva MRI systems (Philips Medical Systems, Best, NL). Volumetric shimming was used at 1.5T (linear) and at 3T (second order) (7). FIG. 1. IRON concept. a,b: Schematic of the signal of an MR image in the frequency (w) domain. a: In an imaged sample that contains water and fat, on-resonant frequency components ( protons onresonance ) originating from water and off-resonant frequency components originating from fat are expected. By adding SPIOlabeled nanoparticles ( susceptibility-generating objects) to this imaged sample, a broadening of the on-resonant peak occurs, which results in additional frequency components (gray area, protons off-resonance ). b: By deliberately suppressing the signal originating from the on-resonant protons (w 0 ) in a narrow frequency band (BW Sat ), only frequency components induced by the susceptibility-generating objects, and fat will contribute to the MR image. c,e: Schematic of the inversion recovery with ON-resonant water suppression (IRON) pulse sequence. In (c), the imaging part of the sequence ( acquisition ) is preceded by prepulses that include a broadband dual-inversion prepulse for fat signal suppression ( fat suppression ) and on-resonant water suppression with the bandwidth BW Sat and the RF pulse angle Sat. Except for this water suppression prepulse, all other RF pulses are nonspectrally selective. In (d), the longitudinal magnetization of both fat and off-resonant protons is displayed as a function of time. Both magnetization components are unaffected by the frequency selective on-resonant saturation prepulse (BW Sat and Sat ). At the start of image acquisition and because of the dual-inversion broadband magnetization preparation, fat signal is nulled (short T 1 ) while a high signal from off-resonant protons is obtained. In (e), Td 1 and Td 2 refer to the time delay between the dual-inversion broadband magnetization preparation and the imaging sequence, respectively. The frequency-selective on-resonant saturation prepulse reduces the longitudinal magnetization (protons on-resonance), which leads to background signal-nulling at image acquisition. Experiments In Vitro Studies A 0.5 mm diameter stainless-steel sphere was embedded in gelatin (Jell-O; Kraft Foods, Northfield, IL, USA) and IRON imaging using either 3D segmented k-space GRE or fast spin-echo (FSE) signal-readouts was performed at 3T using an eight-element phased-array head coil. ECG-triggered data collection was performed using an artificial ECG (RR duration 870 ms). For GRE, the parameters of the on-resonant water suppression prepulse were BW Sat 100 Hz and Sat 100. For FSE, three different datasets with different suppression BWs (BW Sat 100 Hz, 170 Hz, and 340 Hz) and saturation angles ( Sat 120, 107, and 95 ) were obtained together with one acquisition in which the on-resonant water suppression prepulse was disabled. A square field of view (FOV) and sampling matrix were used (GRE: FOV/matrix 120 mm/120, echo time (TE) 3.1 ms, repetition time (TR) 24 ms, number of signal averages (NSA) 1, RF excitation angle 18, six RF excitations per RR interval, mm thick slices, total scan time 6 min; FSE: FOV/matrix 120 mm/120, TE 8 ms, interecho spacing 8 ms, TR 870 ms, echo train length (ETL) 10, 15 2-mm thick slices, total scan time 7 min). On the resultant images (Fig. 2), the volume of positive signal was computed by thresholding at three SD above the mean of the signal from a region of interest (ROI) in the background. The average positive signal ( S1) was then related to the average background signal ( S2) and the attenuation was quantified in db as 20 log (S1/S2).

3 1074 Stuber et al. FIG. 2. In vitro 3T imaging in a coronal plane of a stainless steel sphere embedded in a cylindrical gelatin phantom. The center slices of five different 3D acquisitions are shown. a: 3D FSE imaging without frequency-selective on-resonant saturation prepulse. The gelatin appears bright while a signal void is observed in the area of the stainless steel sphere (solid black arrow). b d: FSE IRON imaging was repeated with different settings of the frequency-selective on-resonant saturation prepulse. BW Sat was decreased from 340 Hz (b), to 170 Hz (c), and finally to 100 Hz (d). Note the gradual increase of area of positive signal surrounding the stainless steel sphere (dashed white arrows). The on-resonant background signal is attenuated but residual positive signal attributable to B 1 inhomogeneity (dotted white arrows) and B 0 inhomogeneity (solid white arrows) is still observed. e: The FSE signal-readout from (d) was replaced with a gradient echo signal-readout (GRE). B 0 main magnetic field. To demonstrate that IRON is capable of preserving positive signal in the surroundings of SPIO-labeled cells, while signal from fat can be attenuated, an agarose cell phantom that contained wells filled with approximately two million labeled cells or mineral oil (Fig. 3) was prepared. For cell labeling, canine mesenchymal stem cells (MSCs) were labeled as previously described (8). The phantom was then imaged at 3T using 2D FSE imaging (FOV/matrix 220 mm/512, TE/TR 7.4 ms/3000 ms, interecho spacing 7.4 ms, ETL 24, NSA 2, slice FIG. 3. In vitro 3T FSE imaging in a coronal plane of well plates containing agarose and SPIO-labeled clustered canine MSC or mineral oil (Oil). a: To remove concomitant fat signal, an additional dual-inversion broadband prepulse that exploits the short longitudinal relaxation time (T 1 ) of mineral oil is used. Simultaneously, bright signal from the SPIO-labeled MSCs persists. No enhancement at the Plexiglas-agarose interface is seen (dotted white arrows). b: Using FSE with the frequency-selective on-resonant saturation prepulse only, signal suppression of agarose is obtained resulting in concomitant positive signal from both the labeled cells and mineral oil. B 0 main magnetic field. thickness 3 mm, rectangular FOV 80%, total scan time 3.5 min). An on-resonant prepulse with BW Sat 145Hz and Sat 95 preceded the imaging part of the sequence and was combined with a non-slice-selective, non-spectrally-selective, dual-inversion prepulse with Td ms, and Td 2 60 ms for fat signal suppression. This experiment was then repeated without the dual-inversion prepulse. A six-element phased-array cardiac coil was used. On the resultant images, the ratio between the positive signal surrounding the cells and the signal from the background as well as the ratio between fat signal and that from the background was measured as described above. Subsequently, an agarose gel phantom was designed using a 24-well culture plate. Wells were filled with agarose except for 100- l spaces in which cell dilutions of 2.0, 1.5, 0.75, 0.5, 0.2, and 0.1 million SPIO-labeled cells were injected (Fig. 4). Two-dimensional FSE imaging at 1.5T using a six-element phased-array head coil (FOV/matrix 180 mm/256, TE/TR 4.6 ms/2000 ms, interecho spacing 4.6 ms, BW 500 Hz/pixel, ETL 24, NSA 2, 2-mm slice thickness, total scan time 40 s) was performed with (BW Sat 100Hz, Sat 95 ) and without on-resonant water suppression. The scan with on-resonant water suppression was repeated with a 3D FSE signalreadout (FOV/matrix 180 mm/256, TE/TR 7.0 ms/ 2000 ms, interecho spacing 7.0 ms, BW 540 Hz/pixel, ETL 22, NSA 2, and mm thick slices, total scan time 17 min). A square FOV and sampling matrix was used for these scans. 2D 1.5T GRE images (FOV/matrix

4 Positive-Contrast With IRON MRI 1075 FIG. 4. (a) GRE, (b) FSE, and (c) FSE IRON images of well plates containing ,2 10 5,5 10 5, , , and SPIO-labeled stem cells (increasing concentrations from left to right). Images were obtained at 1.5T. Signal voids are observed in GRE (a) and FSE (b) images with significant distortions in GRE images. The FSE IRON images demonstrate areas of positive signal that increase in size with increasing cell concentrations. In (c), inhomogeneous background suppression is observed in the areas of 100,000 and 750,000 cells. This may be attributed to B 1 inhomogeneity. In (d), a plot of the linear regression of the volume of positive signal from FSE IRON imaging relative to the number of SPIO-labeled cells in the culture well (linear fit (black line ), y 147x 20, R ) is shown. B 0 main magnetic field. 180 mm/256, TE/TR 4.8 ms/20 ms, BW 43 Hz/pixel, NSA 2, RF excitation angle 30, 2-mm slice thickness, total scan time 1 min) without on-resonant water suppression were also collected at the same level and in the same orientation with a square FOV and sampling matrix. In the 3D FSE IRON images, ROIs of hyperintense signal were selected by thresholding at 3SD above the mean of the remote agarose gel signal. Using these ROIs, volumes of positive signal were quantified, and a linear correlation to labeled cell quantities was performed. In Vivo Study For in vivo imaging, rabbit MSCs were labeled using magnetoelectroporation (9,10). Multiple intramuscular injections ( cells/injection site) of SPIO-labeled MSCs were placed in the hindlimb of a New Zealand White Rabbit. Immediately following the cell injections, the rabbit was imaged at 3T using 3D FSE IRON imaging with a six-element phased-array cardiac coil (FOV/matrix 180 mm/400, TE/TR 11.6 ms/2000 ms, interecho spacing 11.6 ms, ETL 24, NSA 2, five 3-mm thick slices, rectangular FOV 72%, total scan time 7.5 min). Background suppression was obtained using an on-resonant suppression pulse with BW Sat 170 Hz and Sat 95 and fat saturation was used. RESULTS Proof of Concept In Vitro Using 3D FSE, a hypointense signal is observed in the region of the stainless steel sphere (Fig. 2a; solid arrow). Simultaneously, the surrounding gelatin does not appear signal suppressed. In contrast, with FSE IRON imaging (Fig. 2b), a positive signal (dashed arrow) surrounds the stainless-steel sphere while the background is signal-suppressed. However, slightly inhomogeneous signal attenuation is observed at the phantom borders (dotted arrows). As expected, the BW of the on-resonant prepulse had a significant effect on the size of the volume with positive signal. Lower BW Sat values resulted in larger volumes of positive signal (Fig. 2b d). If the FSE signal-readout is replaced with GRE, a multilobed area of positive signal similar to that obtained with FSE is observed (Fig. 2e). On the FSE IRON images, the measured volumes of positive signal were 693 l for a BW Sat of 100 Hz, 456 l for 170 Hz and 170 l for 340 Hz, respectively. The corresponding signal suppression was 22 db, 19 db, and 16 db. On the GRE IRON image, a 625- l volume of positive signal was measured together with a signal suppression of 19 db. Fat Signal Suppression As shown in Fig. 3a, the positive signal in the area of SPIO-labeled MSCs was preserved while fat signal was suppressed. No concomitant positive signal is observed between interfaces generated by agarose and polypropylene (test tube wall), e.g., Fig. 3a (dotted arrows). With fat saturation, a signal attenuation of 16 db was measured between the positive signal and the background while that between fat and the background was 6 db. Without fat suppression, the corresponding values were 16 db and 17 db. Cell Detection In the GRE images (Fig. 4a), both local signal voids and positive signal occur simultaneously, while the area of the signal void increases with higher cell concentrations. In the FSE images (Fig. 4b), the area of signal void surrounding the cells is better constrained as a result of the higher signal-readout BW, but other competing sources of signal voids originating from the well plate structure (Fig. 4b; arrowhead) remain. In contrast, exclusive positive signal of off-resonant protons in areas of the SPIO-labeled MSCs is obtained using IRON (Fig. 4c). Moreover, the volume of positive signal increases with the number of labeled cells and is directly proportional to the concentration of cells

5 1076 Stuber et al. FIG. 5. Adjacent double-oblique slices (a c) from an in vivo 3T FSE 3D IRON acquisition obtained in an ischemic rabbit hindlimb with two injection sites of SPIO-labeled stem cells (250,000 dotted white arrow and 125,000 solid white arrow). Note the excellent background suppression that leads to clear visualization of the stem cell injection sites with positive contrast and a larger volume of hyperintense signal for the 250,000-cell injection site. In the region of the dashed white arrow, imperfections in both on-resonant water suppression and off-resonant fat suppression are observed. This residual signal occurred in an area that was outside of the second order shim volume. B 0 main magnetic field. (Fig. 4d; R ). Positive contrast in vitro could be detected for all cell concentrations including the lowest one tested (100,000 in 100 l). In Vivo IRON Imaging Two injection sites can readily be detected as areas of positive signal (Fig. 5a c) in adjacent slices from a 3D IRON FSE dataset obtained in a rabbit hindlimb at 3T. A larger area of hyperintense signal is observed at the injection site with 250,000 cells as compared to that with 125,000 cells. DISCUSSION By exploiting the characteristic magnetic field disturbances induced by metallic objects, a technique was developed that enables the visualization of the surroundings of nondiamagnetic objects with positive signal rather than as a more traditional signal void. This was achieved by adding a frequency-selective prepulse for on-resonant signal suppression. Concomitant positive signal from fat can be suppressed by using T 1 -dependent fat signal nulling. In vitro and in vivo, IRON imaging has successfully been applied to visualize the surroundings of SPIO-labeled cells with positive signal while signal from both background and fat was effectively attenuated. For IRON imaging, no modification of the imaging part of the sequence is necessary, which facilitates the use of already well-established GRE or FSE imaging protocols, and which decouples the generation of the positive contrast from the imaging part of the sequence. However, using a GRE signal-readout, the volume of hyperintense signal may be TE-dependent (less positive signal with prolonged TE). Moreover, when combining IRON with an FSE signal-readout, an increased power deposition may pose further challenges, especially at higher magnetic field strength. Using IRON imaging, the volume of positive signal surrounding a metallic object can simply be controlled by BW Sat (Fig. 2). In practice, the optimum BW Sat will be application dependent and to maximize background signal suppression, Sat may have to be determined individually on a low spatial resolution scout image. In vitro, the concentration of SPIO-labeled cells was highly correlated to the volume of positive signal. Therefore, IRON may be a useful tool to not only noninvasively track the location of cellular therapeutics but also to quantify the actual amount of cells. Alternative MRI methods for positive contrast visualization of superparamagnetic objects have been reported (4 6). An innovative strategy uses spectral excitation in conjunction with spin-echo imaging (4) with a reported theoretical background suppression of 120 db. However, this suppression comes at the expense of limited flexibility, such that the technique uses temporally inefficient spinecho imaging, is based on a projection technique, and subsequently, requires a large volume of water to be suppressed (4). Potential improvements that were mentioned included the ability to perform slice selection and abbreviate the duration of the frequency selective RF excitations (4). While a background attenuation of up to 20 db only was obtained using IRON imaging, it still affords the advantage that 2D and 3D imaging is easily performed and that faster signal-readout schemes such as FSE and segmented k-space GRE can readily be employed. Moreover, since signal from positive and negative frequency components contribute to the signal, IRON imaging may be more signal efficient than the spectral excitation method, which attenuates 50% of the off-resonant signal components. Other powerful positive contrast approaches include the modification of the refocusing gradient after slice selection (5,6). While the use of GRadient echo Acquisition for Superparamagnetic particles/susceptibility (GRASP) and related techniques leads to positive signal from the area surrounding susceptibility-generating objects, positive signal may also be seen at tissue borders or in areas of abrupt changes in local signal intensity in the underlying anatomy. While superior background suppression as compared to IRON is expected, GRASP still necessitates the modification of the imaging part of the sequence and is currently limited to GRE.

6 Positive-Contrast With IRON MRI 1077 Further potential applications of IRON include atherosclerosis imaging using ultra small SPIOs (USPIOs). Ruehm et al. (11) have demonstrated that macrophage uptake of iron particles causes focal signal attenuation on MRIs of the atherosclerotic vessel wall. Based on similar findings of others (12,13), it is anticipated that IRON would lead to a positive contrast in areas of iron particles engulfed by macrophages. Finally, off-resonance characteristics of Gd have recently been exploited using offresonance contrast angiography (ORCA) (14) to generate positive contrast in angiograms. Therefore, assuming a microscopic distribution of a susceptibility-generating contrast agent, it is anticipated that IRON could be exploited for angiography as well. Limitations Alternative sources of off-resonance signal inevitably lead to positive signal that is not necessarily related to the presence of the susceptibility-generating objects of interest. This is primarily expected at tissue borders, or at air-tissue interfaces (B 0 inhomogeneities) (Fig. 2d; solid arrow). However, these effects are field strength dependent and higher-order volumetric shimming (7) can minimize this problem. Furthermore, B 1 inhomogeneity (Fig. 2) may lead to local over/undertipping of the magnetization and thus to residual background signal. This B 1 inhomogeneity effect will be more significant at higher field strength and may be alleviated by using adiabatic prepulses. Simultaneously, the effectiveness of the background suppression also depends on both the BW of the suppression pulse (prolonged T 1 -recovery period between suppression pulse and imaging for narrower BWs) and the imaging sequence used. For segmented k-space GRE imaging, e.g., T 1 recovery during the RF excitation train, has to be considered. When using dual-inversion for fat suppression, the longitudinal magnetization from off-resonant protons is T 1 dependent (Fig. 1d). Therefore, replacing the broad-band dual-inversion with a second spectrally-selective prepulse for fat saturation remains to be explored. While the size of the volume with positive signal depends on the number of SPIO-labeled cells, it also depends on their local concentration and spatial distribution. Some of these factors may be highly variable in vivo, particularly since cell migration may occur and cells may rapidly proliferate (diluting the SPIO) or die. In Fig. 4, the correlation between the volume of positive signal and the number of cells shows a slight offset. This may be attributed to the method of quantification (i.e., there will always be voxels with signal intensities 3SD above the mean of the background signal) or to errors in cell counting. Finally, small numbers of SPIO-labeled cells can be detected with negative contrast MRI (15,16). In the present study, as little as 100,000 labeled cells could be identified in vitro and 125,000 in vivo. While this is similar to the findings of others (4,17), the lowest detectability threshold of IRON remains to be determined. CONCLUSIONS Using a new MRI method, hyperintense signal is obtained in close vicinity to susceptibility-generating objects while signal from the background and from fat is effectively attenuated. This technique has successfully been applied to generate positive contrast in the surroundings of SPIOlabeled cells in vitro and in vivo. Since contrast generation is decoupled from imaging, IRON can easily be combined with an FSE or a GRE signal-readout while 2D and 3D imaging is supported. For a cluster of cells, the volume of positive signal showed a high correlation with SPIO-labeled cell concentration. IRON imaging is, therefore, an enabling MRI methodology for the visualization and potential quantification of SPIO-labeled cells. REFERENCES 1. Dias MHM, Lauterbur PC. Ferromagnetic particles as contrast agents for magnetic resonance imaging of liver and spleen. Magn Reson Med 1986;3: Bulte JW, Kraitchman DL. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 2004;17: Bulte JW, Brooks RA, Moskowitz BM, Bryant LH Jr, Frank JA. Relaxometry and magnetometry of the MR contrast agent MION-46L. Magn Reson Med 1999;42: Cunningham CH, Arai T, Yang PC, McConnell MV, Pauly JM, Conolly SM. Positive contrast magnetic resonance imaging of cells labeled with magnetic nanoparticles. Magn Reson Med 2005;53: Seppenwoolde JH, Viergever MA, Bakker CJ. Passive tracking exploiting local signal conservation: the white marker phenomenon. Magn Reson Med 2003;50: Mani V, Briley-Saebo KC, Hyafil F, Itskovich V, Fayad ZA. Positive magnetic resonance signal enhancement from ferritin using a GRASP (GRE acquisition for superparamagnetic particles) sequence: ex vivo and in vivo study. J Cardiovasc Magn Reson 2006;8: Schar M, Kozerke S, Fischer SE, Boesiger P. Cardiac SSFP imaging at 3 Tesla. Magn Reson Med 2004;51: Kraitchman DL, Heldman AW, Atalar E, Amado L, Martin BJ, Pittenger MF, Hare JM, Bulte J. In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation 2003;107: Walczak P, Kedziorek D, Gilad AA, Lin S, Bulte JW. Instant MR labeling of stem cells using magnetoelectroporation. Magn Reson Med 2005: Walczak P, Ruiz-Cabello J, Kedziorek DA, Gilad AA, Lin S, Barnett B, Qin L, Levitsky H, Bulte JW. Magnetoelectroporation: improved labeling of neural stem cells and leukocytes for cellular magnetic resonance imaging using a single FDA-approved agent. Nanomedicine 2006;2: Ruehm SG, Corot C, Vogt P, Kolb S, Debatin JF. Magnetic resonance imaging of atherosclerotic plaque with ultrasmall superparamagnetic particles of iron oxide in hyperlipidemic rabbits. Circulation 2001;103: Mani V, Briley-Saebo KC, Hyafil F, Fayad ZA. Feasibility of in vivo identification of endogenous ferritin with positive contrast MRI in rabbit carotid crush injury using GRASP. Magn Reson Med 2006;56: Mani V, Saebo KC, Itskovich V, Samber DD, Fayad ZA. Gradient echo acquisition for superparamagnetic particles with positive contrast (GRASP): sequence characterization in membrane and glass superparamagnetic iron oxide phantoms at 1.5T and 3T. Magn Reson Med 2006; 55: Edelman RR, Storey P, Dunkle E, Li W, Carrillo A, Vu A, Carroll TJ. Gadolinium-enhanced off-resonance contrast angiography. Magn Reson Med 2007;57: Foster-Gareau P, Heyn C, Alejski A, Rutt BK. Imaging single mammalian cells with a 1.5 T clinical MRI scanner. Magn Reson Med 2003;49: Heyn C, Bowen CV, Rutt BK, Foster PJ. Detection threshold of single SPIO-labeled cells with FIESTA. Magn Reson Med 2005;53: de Vries IJ, Lesterhuis WJ, Barentsz JO, Verdijk P, van Krieken JH, Boerman OC, Oyen WJ, Bonenkamp JJ, Boezeman JB, Adema GJ, Bulte JW, Scheenen TW, Punt CJ, Heerschap A, Figdor CG. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol 2005;23:

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