Published online before print December 29, 2003, 10.1148/radiol.2302021230
(Radiology 2004;230:589-594.)
© RSNA, 2003
Shortening MR Image Acquisition Time for Volumetric Interpolated Breath-hold Examination with a Recently Developed Parallel Imaging Reconstruction Technique: Clinical Feasibility1
Charles A. McKenzie, PhD,
Daniel Lim, MD,
Bernard J. Ransil, MD, PhD,
Martina Morrin, MD,
Ivan Pedrosa, MD,
Ernest N. Yeh, M Eng,
Daniel K. Sodickson, MD, PhD and
Neil M. Rofsky, MD
1 From the Departments of Radiology (C.A.M., D.L., M.M., I.P., N.M.R.), Medicine (Cardiovascular Division) (D.K.S.), and Neurology (B.J.R.), Beth Israel Deaconess Medical Center, 330 Brookline Ave, Room AN-239, Boston, MA 02215; Harvard Medical School, Boston, Mass (C.A.M., D.L., M.M., I.P., D.K.S., N.M.R.); and Harvard-MIT Division of Health Sciences and Technology, Boston, Mass (E.N.Y., D.K.S.). Received October 7, 2002; revision requested December 3; final revision received June 2, 2003; accepted June 25. D.K.S. supported by National Institutes of Health grants R29 HL60802 and R01 EB00447 and by a Whitaker Foundation Biomedical Engineering grant. Address correspondence to C.A.M. (e-mail: charles_mckenzie@caregroup.harvard.edu).
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ABSTRACT
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A recently developed parallel magnetic resonance (MR) imaging technique, parallel imaging with an augmented radius in k space, was used to accelerate the volumetric interpolated breath-hold examination (VIBE) performed in 20 patients referred for clinical liver imaging. Nonaccelerated MR images were also acquired in these patients. A five-point scale was used to score the quality of the images. The acceleration resulted in reduced image quality: The nonaccelerated images had a significantly higher (P < .05) mean score3.8 ± 0.3 (SD), indicating good qualitythan the accelerated images3.0 ± 0.3, indicating acceptable quality. However, for three patients who could not hold their breath for the duration necessary for nonaccelerated imaging, less severe breathing artifacts on the accelerated images resulted in improved quality compared with the quality of the nonaccelerated images. Parallel MR imagingaccelerated VIBE may be beneficial for patients who have difficulty sustaining a breath hold for the duration necessary to perform nonaccelerated imaging.
© RSNA, 2003
Index terms: Magnetic resonance (MR), comparative studies, **.121412, **.121416, **.121432 Magnetic resonance (MR), reconstruction algorithms, **.121412, **.121416, **.12143 Magnetic resonance (MR), technology, **.121412, **.121416, **.12143 Magnetic resonance (MR), three-dimensional, **.121412, **.121416, **.12143
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INTRODUCTION
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The volumetric interpolated breath-hold examination (VIBE) sequence (1,2) can yield fat-saturated three-dimensional magnetic resonance (MR) images of the entire liver with high spatial resolution in all three dimensions. This technique has been shown to be reproducibly reliable for clinical evaluations of the upper part of the abdomen (2). Breath-hold times of longer than 20 seconds are often necessary for this technique, but some patients who are referred for liver imaging are not capable of holding their breath this long.
The results of previous works have shown that parallel MR imaging techniques such as simultaneous acquisition of spatial harmonics (SMASH) (3) and sensitivity encoding (SENSE) (4) can be used to dramatically shorten the time needed for data acquisition while preserving the spatial resolution and contrast of the original image. However, all parallel MR imaging techniques yield accelerated images with a lower signal-to-noise ratioand possibly more artifactsthan the equivalent nonaccelerated images.
Parallel MR imaging enables accelerated data acquisition by allowing one to skip the acquisition of the phase-encoding lines that would ordinarily be included in a nonaccelerated data acquisition. If the accelerated images were to be reconstructed in the same manner as the nonaccelerated reference images, the reduced phase encoding in the accelerated acquisitions would result in a reduced field of view and in images with substantial aliasing artifacts. A variety of parallel MR image reconstruction techniques to remove these aliasing artifacts from accelerated images have been developed. In general, this is accomplished by using knowledge of the spatial sensitivity profiles of the radiofrequency coils used for data reception to create appropriate linear combinations of the acquired data that can replace the omitted phase-encoding lines.
The purpose of this study was to evaluate the feasibility of a recently developed parallel MR image reconstruction technique that is used in VIBE liver imaging to accelerate image acquisition and shorten the required breath-hold times.
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Materials and Methods
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Study Population
We examined 20 consecutive adult patients (11 men with a mean age of 55 years ± 14 [SD] [age range, 2972 years]; nine women with a mean age of 50 years ± 13 [age range, 3269 years]) who had been referred because they were known to have or were suspected of having hepatobiliary disorders. The reasons for referral were abdominal pain in five, abnormal liver function examination results in five, history of hepatitis in three, carcinoma in four, and lymphoma in three patients. The institutional committee on clinical investigations of Beth Israel Deaconess Medical Center approved the research protocol, and written informed consent was obtained from all subjects.
Imaging Protocol
We obtained all MR images by using a 1.5-T system (Siemens Symphony; Siemens Medical Systems, Iselin, NJ) with a maximum gradient strength of 30 mT/m and a rise time of 300 µsec and a standard, commercially available four-element body array. Before the start of the examination, a 22-gauge intravenous catheter was placed in an antecubital or forearm vein and attached to an MR imagingcompatible power injector (Spectris; MedRad, Pittsburgh, Pa).
In each subject, we acquired a total of four gradient-echo VIBE MR images (4.2/1.88 [repetition time msec/echo time msec], 12° flip angle, 180-mm-thick slab, 3640 partitions interpolated to 7280 partitions, 225 x 300-mm field of view, 146 x 256 matrix, 5.00 [2.50 interpolated] x 1.54 x 1.17-mm spatial resolution) of the entire liver. One reference volume and one twofold-accelerated volume were acquired before, and two similar volumes were acquired 5 minutes after, contrast material (gadopentetate dimeglumine, Magnevist; Berlex Laboratories, Wayne, NJ) administration. The nonaccelerated volume was always acquired before the accelerated volume.
The order of the acquisitions was not expected to affect the comparison of the precontrast MR images, but it may have biased our results slightly against the postcontrast accelerated MR images. The signal-to-noise ratio on the postcontrast accelerated images, as compared with that on the nonaccelerated images, may have been reduced somewhat owing to clearance of the contrast material during the interval between the two data acquisitions. At all sequences, the patients were instructed to suspend respiration at end expiration. In all 20 patients, the MR imaging examinations were completed without complications.
MR Image Reconstruction
We reconstructed the nonaccelerated MR images by using a traditional sum-of-squares combination of component coil images (5). Hereafter, the combined nonaccelerated MR images are referred to as reference images. Each accelerated data set was reconstructed with the recently developed parallel imaging with augmented radius in k space (PARS) (6) technique. The coil sensitivity information required for the parallel image reconstructions was extracted from the data used to generate the reference images. Hereafter, the reconstructed accelerated MR images are referred to as PARS images.
Designed as a hybrid of SMASH and SENSE to capture the best features of both techniques, PARS involves the use of a k-space locality criterion to select a subset of acquired MR signal intensity data to be included in a generalized encoding matrix reconstruction (7). All acquired signal intensity data within a specified radius from the k-space coordinate of an omitted signal intensity datum are used to reconstruct that missing datum. In comparison, when reconstructing an omitted signal intensity datum with the SMASH technique, only the data acquired on a single adjacent k-space line are used, and when performing this reconstruction with the SENSE technique, all k-space data are used, no matter how distant they are from the point to be reconstructed. Thus, SMASH and SENSE techniques can be considered special forms of PARS with the k-space radii of the circles equal to 1 (with SMASH) or to the maximum k-space span (with SENSE).
The use of only a local cluster of k-space points enables one to use PARS to preserve the inherent numeric stability of SMASH MR imaging (8) while approaching the theoretically perfect fit of SENSE MR imaging (4). Preliminary study results have shown that images reconstructed with PARS at an intermediate k-space radius can have a better signal-to-noise ratio and less severe artifacts than images reconstructed from the same data by using either a k-space radius of 1 (ie, a SMASH-like reconstruction) or the maximum k-space radius (ie, a SENSE-like reconstruction) (6). Thus, for the present study, we chose to use PARS reconstructions with a k-space radius of 8 to acquire MR images.
Qualitative Image Analysis
Three radiologists (I.P., D.L., M.M.) with 28 years experience in reading abdominal MR images evaluated the images in a random and blinded manner. For each data set, each radiologist independently scored eight semiquantitative parameters of image quality. These parameters and the explanations of the scores for each of them are summarized in Table 1. The highest score indicated the most desirable extent (ie, presence or absence) of a given imaging feature. Before performing the described image evaluations, all three radiologists collectively reviewed a training data set and agreed on the interpretations and the scores for each of the evaluated parameters.
Quantitative Image Analysis
The total duration of each MR image acquisition was recorded. The three radiologists who performed the semiquantitative scoring also independently counted the number of hepatic lesions visible on each image. They also counted the number of the 10 major intrahepatic veins (ie, right, left, and middle hepatic vein; main, right, and left portal vein; both right segmental veins; and both left segmental veins) visible on each image.
Statistical Analyses
All values are presented as means (±1 SD, where appropriate). For each quantitative and qualitative parameter, the reference and PARS images acquired both before and after contrast material administration were compared by using two-way analysis of variance (PROPHET; GTE Internetworking, Cambridge, Mass). When significant differences were detected, pairwise comparisons between the four techniques (ie, pre- and postcontrast PARS and pre- and postcontrast reference [nonaccelerated]) were made by using the Newman-Keuls test (PROPHET). For all tests, P
.05 was deemed to indicate statistical significance. For each parameter assessed by the readers, the
2 test (PROPHET) was used to determine if there were more disagreements among the readers than would be expected by chance.
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Results
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Quantitative Results
The twofold accelerated PARS images were acquired in a mean time of 13.1 seconds ± 0.2, as compared with the mean time of 26.1 seconds ± 0.4 in which the nonaccelerated reference images were acquired. All other quantitative image measurements are summarized in Table 2. There were no significant differences in the detection of the major hepatic vessels or the hepatic lesions either among the readers or between the PARS and reference images, either with or without contrast material enhancement (P > .05 in all cases).
Semiquantitative Results
The mean semiquantitative ratings of the MR images obtained in this study are summarized in Figure 1. In no case was there a significant difference in rating either among the readers or between the pre- and postcontrast images, so to improve clarity, only the postcontrast image data, averaged among all the readers, are shown. The PARS reconstructed images did have a significantly (P < .05) lower mean score (4.0 ± 0.1) for aliasing artifacts than did the reference images (4.9 ± 0.1), but this corresponded only to the downgrading of a rating of "no aliasing artifact" to "mild aliasing artifact."

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Figure 1. Graph summarizes the results, in mean values ± SDs (lines at top of each bar), for the three reviewers in the semiquantitative analysis of the reference and PARS images obtained in the 20 patients. The only variables that were significantly different between the reference and PARS images were aliasing artifacts, vessel clarity, and overall image quality (P < .05 in all cases). For each of these variables, the PARS images had a lower mean score, but this represented only a mild reduction in quality since the reduction in score was always less than one point on the five-point scale. There were no significant differences between the pre- and postcontrast images, so only the postcontrast results are shown here.
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The scores for overall image quality showed a similarly slight but significant (P < .05) reduction when the PARS and reference MR images were compared. The reference images received a mean score of 3.8 ± 0.3, indicating good overall quality, whereas the PARS images received a mean score of 3.0 ± 0.3, indicating acceptable overall quality. Figure 2, A is a typical precontrast reference MR image, and Figure 2, B is the corresponding PARS image obtained in the same patient. Figures 2, C, and 2, D, are, respectively, postcontrast reference and PARS images obtained in this same patient.

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Figure 2. Transverse gradient-echo VIBE MR images (4.2/1.88, 12° flip angle, 180-mm-thick slab, 36 partitions interpolated to 72 partitions, 225 x 300-mm field of view, 146 x 256 matrix, 5.00 [2.50 interpolated] x 1.54 x 1.17-mm spatial resolution) obtained in 42-year-old man. A, Precontrast reference (acquisition time, 26 seconds); B, precontrast PARS (acquisition time, 13 seconds); C, postcontrast reference (acquisition time, 26 seconds); and, D, postcontrast PARS (acquisition time, 13 seconds) images are shown. Although the PARS images were acquired in half the time in which the reference images were acquired, the quality of the PARS images is largely preserved.
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The PARS images had consistently better mean scores for severity of breathing artifact than the reference images, although the difference was not significant. However, three of the 20 patients had difficulty holding their breath for the entire time required to acquire a reference VIBE MR image. For these patients, the breathing artifact severity scores for the PARS images were 30% better, resulting in overall image quality scores that were 20% higher than those for the corresponding reference images. No statistical conclusions could be drawn about this difference owing to the small number of patients who could not sustain the required breath hold.
Figure 3 shows examples of VIBE MR images obtained in a patient who could not sustain a breath hold for the entire time required to perform reference (ie, nonaccelerated) imaging. Figures 3, A, and 3, C, are, respectively, pre- and postcontrast reference MR images obtained in this patient. Breathing motioninduced artifacts are clearly visible on these images. This patient could sustain the shorter breath hold needed for accelerated imaging. Thus, the PARS images (Fig 3, B, D) had substantially higher ratings for breathing artifact and overall image quality than the reference images.

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Figure 3. Transverse gradient-echo VIBE MR images (4.2/1.88, 12° flip angle, 180-mm-thick slab, 36 partitions interpolated to 72 partitions, 225 x 300-mm field of view, 146 x 256 matrix, 5.00 [2.50 interpolated] x 1.54 x 1.17-mm spatial resolution) obtained in 70-year-old woman with a hepatic cyst (arrows) who could not sustain a breath hold for the duration of the reference MR imaging examination. A, Precontrast reference (acquisition time, 26 seconds); B, precontrast PARS (acquisition time, 13 seconds); C, postcontrast reference (acquisition time, 26 seconds); and, D, postcontrast PARS (acquisition time, 13 seconds) images are shown. Breathing motion-induced artifacts are clearly depicted on the reference images (A and C) as blurring and as horizontal bands across the entirety of the images. These artifacts are entirely absent from the PARS images (B and D). Thus, the PARS images had substantially higher ratings for breathing artifact and overall image quality than the reference images.
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Discussion
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The implementation of MR imaging systems with high performance gradients has made three-dimensional breath-hold imaging feasible (1,2,9,10). However, when trying to achieve a spatial resolution sufficient to generate meaningful multiplanar reformations and maximum intensity projections, the acquisition times can exceed the breath-hold capability of some individuals. Our study results demonstrate that it is possible to use PARS to accelerate VIBE MR imaging of the liver by a factor of two while preserving acceptable image quality. Furthermore, in the patients with limited breath-hold capability in our study, the shortened breath-hold times enabled by using PARS acceleration resulted in additional gains in image quality.
The semiquantitative measures reported herein reflect the clinically relevant details that a radiologist must incorporate when attempting to make a diagnosis. In the present study, the scores for these semiquantitative measures assigned to the PARS reconstructed MR images were comparable toand in some cases, higher thanthe scores assigned to the reference (ie, nonaccelerated) images, despite the fact that the PARS images were acquired in half the time in which the reference images were acquired.
One exception to this trend was that the PARS images had slightly lower aliasing artifact scores than the reference imageslargely because of aliasing artifacts in the abdominal wall, which is directly under the array elements. In general, when the breath-hold time differs between sensitivity calibration imaging and accelerated imaging, a mismatch between the estimated and actual coil sensitivities results. This mismatch reflects a displacement of the coil array between the two acquisitions, which in turn yields aliasing artifacts.
The abdominal wall is particularly prone to sensitivity mismatches because it lies just below the anterior elements of the coil array, where exceptionally high signal intensity is generated. Furthermore, substantial displacement of the anterior abdominal wall occurs during the respiratory cycle. One way to address misregistrations between the estimated and actual coil sensitivities is to perform a self-calibrating parallel MR imaging acquisition (11) to guarantee the correct measurement of the coil sensitivities. With self-calibrating approaches, aliasing artifacts can be avoided for improved image quality in parallel acquisitions.
On a strictly scientific basis, it would have been useful to compare the dynamic acquisitions of both the reference and PARS data sets. Such a comparison would have required a separate imaging session to generate distinct dynamic phases for both strategies, and we believed that the additional time and contrast material exposure were not warranted for this initial feasibility assessment. Our study results demonstrate the advantages and disadvantages of PARS for both precontrast and delayed postcontrast MR imaging examinations. These same features should apply to dynamic evaluations, in which shortened breath-hold times would allow the acquisition of satisfactory dynamic images in a larger group of patients. Alternatively, for patients without compromised breath-holding ability, the reduced acquisition time could be reinvested into the imaging strategy for better depiction of the arterial phase (12,13). This investment has the potential to improve the value of arterial phase imaging, particularly in patients with cirrhosis (1416).
The data collected for this study were acquired with a standard, commercially available coil array that had not been altered in any way for use with parallel MR imaging. The results of other authors works have shown that the arrangement and shape of the elements in the coil array can have a substantial effect on artifacts and the signal-to-noise ratio of the reconstructed images (1719). In addition, recent study results have shown that adding more elements to the array is expected to facilitate less severe artifacts and an improved signal-to-noise ratio on images (2023). Thus, we expect to see substantial improvements in the results seen in this study once arrays that are specifically designed for parallel imaging become available for clinical imaging.
In conclusion, the results of this study demonstrate the successful application of PARS reconstruction in VIBE parallel imaging with a standard coil array. Our study results suggest that using parallel MR imaging to accelerate VIBE imaging by a factor of two is feasible for general clinical imaging and may be particularly beneficial for the subpopulation of patients who have limited breath-hold capability.
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FOOTNOTES
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2**. Multiple body systems 
Abbreviations: PARS = parallel imaging with an augmented radius in k space,
SENSE = sensitivity encoding,
SMASH = simultaneous acquisition of spatial harmonics,
VIBE = volumetric interpolated breath-hold examination
Author contributions: Guarantor of integrity of entire study, C.A.M.; study concepts, D.K.S., C.A.M.; study design, D.K.S., C.A.M., N.M.R.; literature research, C.A.M.; clinical studies, C.A.M., D.L.; data acquisition, C.A.M., D.L.; data analysis/interpretation, C.A.M., D.L., I.P., M.M., E.N.Y; statistical analysis, B.J.R., C.A.M.; manuscript preparation and editing, C.A.M.; manuscript definition of intellectual content and final version approval, C.A.M., D.K.S., N.M.R.; manuscript revision/review, all authors
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