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6.  Steady-State Equilibrium Phase Inversion Recovery ON-resonant Water Suppression (IRON) Magnetic Resonance Angiography in Conjunction with Superparamagnetic Nanoparticles. A Robust Technique for Imaging within a Wide Range of Contrast Agent Dosages 
To investigate the ability of inversion recovery ON-resonant water suppression (IRON) in conjunction with P904 (superparamagnetic nanoparticles which consisting of a maghemite core coated with a low-molecular-weight amino-alcohol derivative of glucose) to perform steady-state equilibrium phase magnetic resonance angiography (MRA) over a wide dose range.
Materials and Methods
Experiments were approved by the institutional animal care committee. Rabbits (n=12) were imaged at baseline and serially after the administration of 10 incremental dosages of 0.57–5.7 mgFe/Kg P904. Conventional T1-weighted and IRON MRA were obtained on a clinical 1.5-T scanner to image the thoracic and abdominal aorta, and peripheral vessels. Contrast-to-noise ratios (CNR) and vessel sharpness were quantified.
Using IRON MRA, CNR and vessel sharpness progressively increased with incremental dosages of the contrast agent P904, exhibiting constantly higher contrast values than T1-weighted MRA over a very wide range of contrast agent doses (CNR of 18.8±5.6 for IRON versus 11.1±2.8 for T1-weighted MRA at 1.71 mgFe/kg, p=0.02 and 19.8±5.9 for IRON versus −0.8±1.4 for T1-weighted MRA at 3.99 mgFe/kg, p=0.0002). Similar results were obtained for vessel sharpness in peripheral vessels, (Vessel sharpness of 46.76±6.48% for IRON versus 33.20±3.53% for T1-weighted MRA at 1.71 mgFe/Kg, p=0.002, and of 48.66±5.50% for IRON versus 19.00±7.41% for T1-weighted MRA at 3.99 mgFe/Kg, p=0.003).
Our study suggests that quantitative CNR and vessel sharpness after the injection of P904 are consistently higher for IRON MRA when compared to conventional T1-weighted MRA. These findings apply for a wide range of contrast agent dosages.
PMCID: PMC3657577  PMID: 23418107
7.  Self-Navigation with Compressed Sensing for 2D Translational Motion Correction in Free-Breathing Coronary MRI: A Feasibility Study 
PLoS ONE  2014;9(8):e105523.
Respiratory motion correction remains a challenge in coronary magnetic resonance imaging (MRI) and current techniques, such as navigator gating, suffer from sub-optimal scan efficiency and ease-of-use. To overcome these limitations, an image-based self-navigation technique is proposed that uses “sub-images” and compressed sensing (CS) to obtain translational motion correction in 2D. The method was preliminarily implemented as a 2D technique and tested for feasibility for targeted coronary imaging.
During a 2D segmented radial k-space data acquisition, heavily undersampled sub-images were reconstructed from the readouts collected during each cardiac cycle. These sub-images may then be used for respiratory self-navigation. Alternatively, a CS reconstruction may be used to create these sub-images, so as to partially compensate for the heavy undersampling. Both approaches were quantitatively assessed using simulations and in vivo studies, and the resulting self-navigation strategies were then compared to conventional navigator gating.
Sub-images reconstructed using CS showed a lower artifact level than sub-images reconstructed without CS. As a result, the final image quality was significantly better when using CS-assisted self-navigation as opposed to the non-CS approach. Moreover, while both self-navigation techniques led to a 69% scan time reduction (as compared to navigator gating), there was no significant difference in image quality between the CS-assisted self-navigation technique and conventional navigator gating, despite the significant decrease in scan time.
CS-assisted self-navigation using 2D translational motion correction demonstrated feasibility of producing coronary MRA data with image quality comparable to that obtained with conventional navigator gating, and does so without the use of additional acquisitions or motion modeling, while still allowing for 100% scan efficiency and an improved ease-of-use. In conclusion, compressed sensing may become a critical adjunct for 2D translational motion correction in free-breathing cardiac imaging with high spatial resolution. An expansion to modern 3D approaches is now warranted.
PMCID: PMC4149508  PMID: 25171369
8.  Direct in vitro comparison of six 3D positive contrast methods for susceptibility marker imaging 
To compare different techniques for positive contrast imaging of susceptibility markers with MRI for 3D visualization. As several different techniques have been reported, the choice of the suitable method depends on its properties with regard to the amount of positive contrast and the desired background suppression, as well as other imaging constraints needed for a specific application.
Materials and methods
Six different positive contrast techniques are investigated for their ability to image at 3T a single susceptibility marker in vitro. The white marker method (WM), susceptibility gradient mapping (SGM), inversion recovery with on-resonant water suppression (IRON), frequency selective excitation (FSX), fast low flip-angle positive contrast SSFP (FLAPS), and iterative decomposition of water and fat with echo asymmetry and least-squares estimation (IDEAL) were implemented and investigated.
The different methods were compared with respect to the volume of positive contrast, the product of volume and signal intensity, imaging time, and the level of background suppression. Quantitative results are provided and strengths and weaknesses of the different approaches are discussed.
The appropriate choice of positive contrast imaging technique depends on the desired level of background suppression, acquisition speed, and robustness against artifacts, for which in vitro comparative data is now available.
PMCID: PMC3620818  PMID: 23281151
susceptibility imaging; off resonance; positive contrast
9.  A Spatially-selective Implementation of the Adiabatic T2Prep Sequence for Magnetic Resonance Angiography of the Coronary Arteries 
In coronary magnetic resonance angiography, a magnetization-preparation scheme for T2-weighting (T2Prep) is widely used to enhance contrast between the coronary blood-pool and the myocardium. This pre-pulse is commonly applied without spatial selection to minimize flow sensitivity, but the non-selective implementation results in a reduced magnetization of the in-flowing blood and a related penalty in signal-to-noise-ratio (SNR). It is hypothesized that a spatially-selective T2Prep would leave the magnetization of blood outside the T2Prep volume unaffected, and thereby lower the SNR penalty. To test this hypothesis, a spatially-selective T2Prep was implemented where the user could freely adjust angulation and position of the T2Prep slab to avoid covering the ventricular blood-pool and saturating the in-flowing spins. A time gap of 150ms was further added between the T2Prep and other pre-pulses to allow for in-flow of a larger volume of unsaturated spins. Consistent with numerical simulation, the spatially-selective T2Prep increased in vivo human coronary artery SNR (42.3±2.9 vs. 31.4±2.2, n=22, p<0.0001) and contrast-to-noise-ratio (18.6±1.5 vs. 13.9±1.2, p=0.009) as compared to those of the non-selective T2Prep. Additionally, a segmental analysis demonstrated that the spatially-selective T2Prep was most beneficial in proximal and mid segments where the in-flowing blood volume was largest compared to the distal segments.
PMCID: PMC3530637  PMID: 22915337
Coronary MR Angiography; Contrast Enhancement; T2Prep; Vessel Conspicuity; In-flowing Blood
10.  Determinants of Renal Tissue Oxygenation as Measured with BOLD-MRI in Chronic Kidney Disease and Hypertension in Humans 
PLoS ONE  2014;9(4):e95895.
Experimentally renal tissue hypoxia appears to play an important role in the pathogenesis of chronic kidney disease (CKD) and arterial hypertension (AHT). In this study we measured renal tissue oxygenation and its determinants in humans using blood oxygenation level-dependent magnetic resonance imaging (BOLD-MRI) under standardized hydration conditions. Four coronal slices were selected, and a multi gradient echo sequence was used to acquire T2* weighted images. The mean cortical and medullary R2* values ( = 1/T2*) were calculated before and after administration of IV furosemide, a low R2* indicating a high tissue oxygenation. We studied 195 subjects (95 CKD, 58 treated AHT, and 42 healthy controls). Mean cortical R2 and medullary R2* were not significantly different between the groups at baseline. In stimulated conditions (furosemide injection), the decrease in R2* was significantly blunted in patients with CKD and AHT. In multivariate linear regression analyses, neither cortical nor medullary R2* were associated with eGFR or blood pressure, but cortical R2* correlated positively with male gender, blood glucose and uric acid levels. In conclusion, our data show that kidney oxygenation is tightly regulated in CKD and hypertensive patients at rest. However, the metabolic response to acute changes in sodium transport is altered in CKD and in AHT, despite preserved renal function in the latter group. This suggests the presence of early renal metabolic alterations in hypertension. The correlations between cortical R2* values, male gender, glycemia and uric acid levels suggest that these factors interfere with the regulation of renal tissue oxygenation.
PMCID: PMC3997480  PMID: 24760031
11.  Robust volume-targeted balanced steady-state free-precession coronary magnetic resonance angiography in a breathhold at 3.0 Tesla: a reproducibility study 
Transient balanced steady-state free-precession (bSSFP) has shown substantial promise for noninvasive assessment of coronary arteries but its utilization at 3.0 T and above has been hampered by susceptibility to field inhomogeneities that degrade image quality. The purpose of this work was to refine, implement, and test a robust, practical single-breathhold bSSFP coronary MRA sequence at 3.0 T and to test the reproducibility of the technique.
A 3D, volume-targeted, high-resolution bSSFP sequence was implemented. Localized image-based shimming was performed to minimize inhomogeneities of both the static magnetic field and the radio frequency excitation field. Fifteen healthy volunteers and three patients with coronary artery disease underwent examination with the bSSFP sequence (scan time = 20.5 ± 2.0 seconds), and acquisitions were repeated in nine subjects. The images were quantitatively analyzed using a semi-automated software tool, and the repeatability and reproducibility of measurements were determined using regression analysis and intra-class correlation coefficient (ICC), in a blinded manner.
The 3D bSSFP sequence provided uniform, high-quality depiction of coronary arteries (n = 20). The average visible vessel length of 100.5 ± 6.3 mm and sharpness of 55 ± 2% compared favorably with earlier reported navigator-gated bSSFP and gradient echo sequences at 3.0 T. Length measurements demonstrated a highly statistically significant degree of inter-observer (r = 0.994, ICC = 0.993), intra-observer (r = 0.894, ICC = 0.896), and inter-scan concordance (r = 0.980, ICC = 0.974). Furthermore, ICC values demonstrated excellent intra-observer, inter-observer, and inter-scan agreement for vessel diameter measurements (ICC = 0.987, 0.976, and 0.961, respectively), and vessel sharpness values (ICC = 0.989, 0.938, and 0.904, respectively).
The 3D bSSFP acquisition, using a state-of-the-art MR scanner equipped with recently available technologies such as multi-transmit, 32-channel cardiac coil, and localized B0 and B1+ shimming, allows accelerated and reproducible multi-segment assessment of the major coronary arteries at 3.0 T in a single breathhold. This rapid sequence may be especially useful for functional imaging of the coronaries where the acquisition time is limited by the stress duration and in cases where low navigator-gating efficiency prohibits acquisition of a free breathing scan in a reasonable time period.
PMCID: PMC4006454  PMID: 24758168
Coronary artery angiography; 3.0 T magnetic resonance imaging; Balanced steady-state free-precession; Reproducibility; Image-based shimming
18.  Free-Breathing Inner-Volume Black-Blood Imaging of the Human Heart Using Two-dimensionally Selective Local Excitation at 3T 
Black-blood fast spin-echo imaging is a powerful technique for the evaluation of cardiac anatomy. To avoid fold-over artifacts, using a sufficiently large field of view in phase-encoding direction is mandatory. The related oversampling affects scanning time and respiratory chest motion artifacts are commonly observed. The excitation of a volume that exclusively includes the heart without its surrounding structures may help to improve scan efficiency and minimize motion artifacts. Therefore, and by building on previously reported inner-volume approach, the combination of a black-blood FSE sequence with a two-dimensionally selective radiofrequency pulse is proposed for selective “local excitation” small-FOV imaging of the heart. This local excitation technique has been developed, implemented, and tested in phantoms and in vivo. With this method, small-FOV imaging of a user-specified region in the human thorax is feasible, scanning becomes more time efficient, motion artifacts can be minimized and additional flexibility in the choice of imaging parameters can be exploited.
PMCID: PMC3524979  PMID: 22161817
2D-selective RF Pulses; Black-Blood; local excitation
19.  Dependence of Brain Intravoxel Incoherent Motion Perfusion Parameters on the Cardiac Cycle 
PLoS ONE  2013;8(8):e72856.
Measurement of microvascular perfusion with Intravoxel Incoherent Motion (IVIM) MRI is gaining interest. Yet, the physiological influences on the IVIM perfusion parameters (“pseudo-diffusion” coefficient D*, perfusion fraction f, and flow related parameter fD*) remain insufficiently characterized. In this article, we hypothesize that D* and fD*, which depend on blood speed, should vary during the cardiac cycle. We extended the IVIM model to include time dependence of D* = D*(t), and demonstrate in the healthy human brain that both parameters D* and fD* are significantly larger during systole than diastole, while the diffusion coefficient D and f do not vary significantly. The results non-invasively demonstrate the pulsatility of the brain’s microvasculature.
PMCID: PMC3758329  PMID: 24023649
20.  The Feasibility of 350 Micron Spatial Resolution Coronary MRA at 3T in Humans 
Investigative Radiology  2012;47(6):339-345.
The purpose of this study was to (1) develop a high resolution 3T MRA technique with in-plane resolution approximate to that of MDCT and a voxel size of 0.35 × 0.35 × 1.5 mm3 and to (2) investigate the image quality of this technique in healthy subjects and preliminarily in patients with known coronary artery disease (CAD).
Materials and Methods
A 3T coronary MRA technique optimized for an image acquisition voxel as small as 0.35 × 0.35 × 1.5mm3 (HRC) was implemented and the coronary arteries of twenty two subjects were imaged. These included 11 healthy subjects (average age 28.5 years old, five males) and 11 subjects (average age 52.9 years old, five females) with CAD as identified on multidetector coronary computed tomography (MDCT). Additionally, the 11 healthy subjects were imaged using a method with a more common spatial resolution of 0.7×1×3 mm3 (RRC). Qualitative and quantitative comparisons were made between the two MRA techniques.
Normal vessels and CAD lesions were successfully depicted at 350×350μm2 in-plane resolution with adequate signal-to-noise ratio (SNR) and contrast-to-noise ratio (CNR). The CAD findings were consistent among MDCT and HRC. The HRC showed a 47% improvement in sharpness despite a reduction in SNR (reduced by 72%) and CNR (reduced by 86%) compared to the RRC.
This study, as a first step towards substantial improvement in the resolution of coronary MRA, demonstrates the feasibility of obtaining at 3T a spatial resolution that approximates that of MDCT. The acquisition in-plane pixel dimensions are as small as 350μm × 350μm with a 1.5 mm slice thickness. While SNR is lower, the images have improved sharpness resulting in image quality that allowed qualitative identification of disease sites on MRA consistent with MDCT.
PMCID: PMC3349009  PMID: 22551651
21.  Regional Coronary Endothelial Function is Closely Related to Local Early Coronary Atherosclerosis in Patients with Mild Coronary Artery Disease: A Pilot Study 
Coronary endothelial function (endoFx) is abnormal in patients with established coronary artery disease (CAD) and was recently shown by MRI to relate to the severity of luminal stenosis. Recent advances in MRI now allow the non-invasive assessment of both anatomic and functional (endoFx) changes that previously required invasive studies. We tested the hypothesis that abnormal coronary endoFx is related to measures of early atherosclerosis such as increased coronary wall thickness (CWT).
Methods and Results
Seventeen arteries in fourteen healthy adults and seventeen arteries in fourteen patients with non-obstructive CAD were studied. To measure endoFx, coronary MRI was performed before and during isometric handgrip exercise, an endothelial-dependent stressor and changes in coronary cross-sectional area (CSA) and flow were measured. Black blood imaging was performed to quantify CWT and other indices of arterial remodeling. The mean stress-induced change in CSA was significantly higher in healthy adults (13.5%±12.8%, mean±SD, n=17) than in those with mildly diseased arteries (-2.2±6.8%, p<0.0001, n=17). Mean CWT was lower in healthy subjects (0.9±0.2mm) than in CAD patients (1.4±0.3mm, p<0.0001). In contrast to healthy subjects, stress-induced changes in CSA, a measure of coronary endoFx, correlated inversely with CWT in CAD patients (r= -0.73, p=0.0008).
There is an inverse relationship between coronary endothelial function and local CWT in CAD patients but not in healthy adults. These findings demonstrate that local endothelial-dependent functional changes are related to the extent of early anatomic atherosclerosis in mildly diseased arteries. This combined MRI approach enables the anatomic and functional investigation of early coronary disease.
PMCID: PMC3665274  PMID: 22492483
coronary disease; endothelium; magnetic resonance imaging
22.  Non-Invasive Detection of Coronary Endothelial Response to Sequential Handgrip Exercise in Coronary Artery Disease Patients and Healthy Adults 
PLoS ONE  2013;8(3):e58047.
Our objective is to test the hypothesis that coronary endothelial function (CorEndoFx) does not change with repeated isometric handgrip (IHG) stress in CAD patients or healthy subjects.
Coronary responses to endothelial-dependent stressors are important measures of vascular risk that can change in response to environmental stimuli or pharmacologic interventions. The evaluation of the effect of an acute intervention on endothelial response is only valid if the measurement does not change significantly in the short term under normal conditions. Using 3.0 Tesla (T) MRI, we non-invasively compared two coronary artery endothelial function measurements separated by a ten minute interval in healthy subjects and patients with coronary artery disease (CAD).
Twenty healthy adult subjects and 12 CAD patients were studied on a commercial 3.0 T whole-body MR imaging system. Coronary cross-sectional area (CSA), peak diastolic coronary flow velocity (PDFV) and blood-flow were quantified before and during continuous IHG stress, an endothelial-dependent stressor. The IHG exercise with imaging was repeated after a 10 minute recovery period.
In healthy adults, coronary artery CSA changes and blood-flow increases did not differ between the first and second stresses (mean % change ±SEM, first vs. second stress CSA: 14.8%±3.3% vs. 17.8%±3.6%, p = 0.24; PDFV: 27.5%±4.9% vs. 24.2%±4.5%, p = 0.54; blood-flow: 44.3%±8.3 vs. 44.8%±8.1, p = 0.84). The coronary vasoreactive responses in the CAD patients also did not differ between the first and second stresses (mean % change ±SEM, first stress vs. second stress: CSA: −6.4%±2.0% vs. −5.0%±2.4%, p = 0.22; PDFV: −4.0%±4.6% vs. −4.2%±5.3%, p = 0.83; blood-flow: −9.7%±5.1% vs. −8.7%±6.3%, p = 0.38).
MRI measures of CorEndoFx are unchanged during repeated isometric handgrip exercise tests in CAD patients and healthy adults. These findings demonstrate the repeatability of noninvasive 3T MRI assessment of CorEndoFx and support its use in future studies designed to determine the effects of acute interventions on coronary vasoreactivity.
PMCID: PMC3594224  PMID: 23536782
23.  Renal Tissue Oxygenation in Essential Hypertension and Chronic Kidney Disease 
Animal studies suggest that renal tissue hypoxia plays an important role in the development of renal damage in hypertension and renal diseases, yet human data were scarce due to the lack of noninvasive methods. Over the last decade, blood oxygenation level-dependent magnetic resonance imaging (BOLD-MRI), detecting deoxyhemoglobin in hypoxic renal tissue, has become a powerful tool to assess kidney oxygenation noninvasively in humans. This paper provides an overview of BOLD-MRI studies performed in patients suffering from essential hypertension or chronic kidney disease (CKD). In line with animal studies, acute changes in cortical and medullary oxygenation have been observed after the administration of medication (furosemide, blockers of the renin-angiotensin system) or alterations in sodium intake in these patient groups, underlining the important role of renal sodium handling in kidney oxygenation. In contrast, no BOLD-MRI studies have convincingly demonstrated that renal oxygenation is chronically reduced in essential hypertension or in CKD or chronically altered after long-term medication intake. More studies are required to clarify this discrepancy and to further unravel the role of renal oxygenation in the development and progression of essential hypertension and CKD in humans.
PMCID: PMC3590788  PMID: 23509612

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