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High-resolution T1-weighted gradient echo imaging for liver MRI using parallel imaging at high-acceleration factors Jeong Hee Yoon, 1 Jeong Min Lee, 1,2 Mi Hye Yu, 1 Eun Ju Kim, 3 Joon Koo Han, 1,2 Byung Ihn Choi 1,2 1 Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul 110-744, Korea 2 Institute of Radiation Medicine, Seoul National University College of Medicine, Seoul, Korea 3 Philips Healthcare Korea, Seoul, Korea Abstract Purpose: To determine whether application of a high- acceleration parallel acquisition can provide three- dimensional (3D)-fat-suppressed T1-weighted gradient- recalled-echo (T1W-GRE) imaging at 3T for liver MR imaging. Materials and methods: This retrospective study was approved by our institutional review board. Seventy patients underwent liver MRI at a 3T scanner. After administration of a standard dose of Gadoxetic acid for 20 min, 3D-T1W-GRE images were obtained twice using sensitivity encoding with acceleration factors (AFs) 2.6 [332 9 298 matrix, 3-mm slice thickness (ST)] and 4 (380 9 320 matrix, 1.5-mm ST). The image qualities of the two image sets were graded using a five-point scale. Results: The high-resolution (HR) 3D-T1W-GRE image sets were obtained with an AF 4 within a single breath- hold (18.5 s). It showed a better anatomic depiction than conventional 3D-T1W-GRE image sets with an AF 2.6 (p < 0.05). Although the image noise was higher on the HR image sets (p < 0.05), the HR image sets showed better lesion conspicuity and overall image quality than the conventional image sets (p < 0.05). Conclusion: With the use of high AFs, HR 3D-T1W- GRE imaging was demonstrated to be clinically more feasible and advantageous than the conventional 3D- T1W-GRE. Key words: Three-dimensional (3D)-T1-weighted gradient echo (GRE) imaging—Sensitivity encoding (SENSE)-enhanced high-resolution isotropic volume excitation (eTHRIVE)—Dual-source parallel RF excitation—Direct digital receive technology— Gadoxetic acid-enhanced liver MR With advances in hardware, magnetic resonance (MR) imaging plays an increasingly important role in the evaluation of patients with liver diseases [1]. Contrast- enhanced dynamic MR imaging performed with gado- linium chelates is considered useful for detecting and characterizing focal liver lesions (FLLs) [2, 3]. In addi- tion, hepatocyte-specific contrast media (gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid [Gd- EOB-DTPA; Primovist; Bayer Healthcare, Berlin, Ger- many] or gadobenate dimeglumine [Gd-BOPTA; Multi- Hance; Bracco Diagnostics, Italy])-enhanced liver MRI has been increasingly used for the characterization FLLs and detection of liver malignancies [4, 5]. This may be due to the ability of these agents to provide an improved contrast between FLLs and the background liver parenchyma having the hepatocyte-related strong enhancement on the hepatobiliary phase (HBP) [6]. However, liver MR imaging still has shortcomings compared with CT, including image blurring related with the lower spatial resolution as well as a higher suscepti- bility to motion [79]. Therefore, to further improve the diagnostic performance of liver MRI, it would be advisable to improve the spatial resolution of the T1- weighted imaging (T1WI) for depicting small FLLs or fine anatomic details within a reasonable acquisition time which allows for acceptable breath-holding. Correspondence to: Jeong Min Lee; email: [email protected] ª Springer Science+Business Media New York 2014 Abdominal Imaging Abdom Imaging (2014) DOI: 10.1007/s00261-014-0099-8

High-resolution T1-weighted gradient echo imaging for liver MRI using parallel imaging at high-acceleration factors

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Page 1: High-resolution T1-weighted gradient echo imaging for liver MRI using parallel imaging at high-acceleration factors

High-resolution T1-weighted gradient echoimaging for liver MRI using parallel imagingat high-acceleration factors

Jeong Hee Yoon,1 Jeong Min Lee,1,2 Mi Hye Yu,1 Eun Ju Kim,3 Joon Koo Han,1,2

Byung Ihn Choi1,2

1Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine, 101 Daehak-ro,

Jongno-gu, Seoul 110-744, Korea2Institute of Radiation Medicine, Seoul National University College of Medicine, Seoul, Korea3Philips Healthcare Korea, Seoul, Korea

Abstract

Purpose: To determine whether application of a high-acceleration parallel acquisition can provide three-dimensional (3D)-fat-suppressed T1-weighted gradient-recalled-echo (T1W-GRE) imaging at 3T for liver MRimaging.Materials and methods: This retrospective study wasapproved by our institutional review board. Seventypatients underwent liver MRI at a 3T scanner. Afteradministration of a standard dose of Gadoxetic acid for20 min, 3D-T1W-GRE images were obtained twice usingsensitivity encoding with acceleration factors (AFs) 2.6[332 9 298 matrix, 3-mm slice thickness (ST)] and 4(380 9 320 matrix, 1.5-mm ST). The image qualities ofthe two image sets were graded using a five-point scale.Results: The high-resolution (HR) 3D-T1W-GRE imagesets were obtained with an AF 4 within a single breath-hold (18.5 s). It showed a better anatomic depiction thanconventional 3D-T1W-GRE image sets with an AF 2.6(p < 0.05). Although the image noise was higher on theHR image sets (p < 0.05), the HR image sets showedbetter lesion conspicuity and overall image quality thanthe conventional image sets (p < 0.05).Conclusion: With the use of high AFs, HR 3D-T1W-GRE imaging was demonstrated to be clinically morefeasible and advantageous than the conventional 3D-T1W-GRE.

Key words: Three-dimensional (3D)-T1-weightedgradient echo (GRE) imaging—Sensitivity encoding(SENSE)-enhanced high-resolution isotropic volumeexcitation (eTHRIVE)—Dual-source parallel RFexcitation—Direct digital receive technology—Gadoxetic acid-enhanced liver MR

With advances in hardware, magnetic resonance (MR)imaging plays an increasingly important role in theevaluation of patients with liver diseases [1]. Contrast-enhanced dynamic MR imaging performed with gado-linium chelates is considered useful for detecting andcharacterizing focal liver lesions (FLLs) [2, 3]. In addi-tion, hepatocyte-specific contrast media (gadoliniumethoxybenzyl diethylenetriamine pentaacetic acid [Gd-EOB-DTPA; Primovist; Bayer Healthcare, Berlin, Ger-many] or gadobenate dimeglumine [Gd-BOPTA; Multi-Hance; Bracco Diagnostics, Italy])-enhanced liver MRIhas been increasingly used for the characterization FLLsand detection of liver malignancies [4, 5]. This may bedue to the ability of these agents to provide an improvedcontrast between FLLs and the background liverparenchyma having the hepatocyte-related strongenhancement on the hepatobiliary phase (HBP) [6].However, liver MR imaging still has shortcomingscompared with CT, including image blurring related withthe lower spatial resolution as well as a higher suscepti-bility to motion [7–9]. Therefore, to further improve thediagnostic performance of liver MRI, it would beadvisable to improve the spatial resolution of the T1-weighted imaging (T1WI) for depicting small FLLs orfine anatomic details within a reasonable acquisitiontime which allows for acceptable breath-holding.Correspondence to: Jeong Min Lee; email: [email protected]

ª Springer Science+Business Media New York 2014

AbdominalImaging

Abdom Imaging (2014)

DOI: 10.1007/s00261-014-0099-8

Page 2: High-resolution T1-weighted gradient echo imaging for liver MRI using parallel imaging at high-acceleration factors

Until now, several approaches have been attemptedto shorten the acquisition time and to provide T1-weighted gradient echo (GRE) imaging with higherspatial resolution for contrast-enhanced liver MRI.These include the use of parallel imaging (PI), higherchannel phase array coils [10–16], echo-sharing tech-niques, non-Cartesian reconstruction algorithms [17, 18],and use of compressed sensing techniques [19–21].Among these techniques, PI techniques including Sensi-tivity encoding (SENSE) [10–12], the array spatial andsensitivity-encoding technique [22], and generalized aut-ocalibrating partially parallel acquisition [13, 14] havebeen the most widely used and well-established methods,especially for dynamic sequences in abdominal MRI.With the PI techniques, an acceleration factor (AF) oftwo in the phase-encoding direction has been commonlyused in abdominal MR acquisition because when a highAF is applied, it is expected to have a lower signal-to-noise ratio (SNR) and to have remaining unfolded arti-facts as trade-offs [10, 12, 23]. Therefore, to use higherAFs than two, at least two conditions are necessary: oneis the high SNR with good image homogeneity; and theother is the greater efficiency of the PI techniques andphased-array coils for controlling unfolded artifacts [23].Several previous studies have demonstrated that the useof the dual-source, parallel RF excitation technique on a3T unit can provide a homogenous B1 field as theamplitude and phase offset from the two different RFsources can be adjusted independently [24–26]. In addi-tion, the broadband, direct digital RF receive technique,which is achieved by implementing the analog to thedigital converter in the receive coils, may increase theSNR by minimizing signal loss during signal processing[27, 28]. Therefore, we anticipated that high-resolution(HR) T1W-GRE imaging could be achieved using PIwith high AFs, maintaining sufficient SNR in clinicalpractice.

The purpose of this study is to determine whether theuse of high AFs on a 3T scanner can provide high-quality3D-fat-suppressed (FS) T1W-GRE images during theHBP of Gd-EOB-DTPA-enhanced liver MRI.

Materials and methods

This retrospective study was approved by the institu-tional review board of our institution, and informedconsent was waived.

Preliminary phantom experiments

In order to establish a protocol of a HR 3D-T1W-GREsequence using high AF at a 3T scanner with dual-source, parallel RF excitation technology, and directdigitalized RF receive technology, we performed aphantom study to determine whether the combination ofdual RF transmitter (MultiTransmit) and direct digital

RF receive technology (dStream) reduces noise or arti-facts and improves the SNR. A 2000-cc and 1000-ccbottle L13 phantoms (filled with 1000 mL demi-water,770 mg CuSO4, H2O, 1 mL aquad (1% solution),0.15 mL H2SO4—0.1 N solution, and 2000 mg NaCl)were scanned on two different MR scanners: one wasequipped with a dual RF transmitter and digital RF re-ceive technology (Ingenia, Philips Healthcare), and theother did not have two technologies (Achieva, PhilipsHealthcare). Two phantoms were placed at the ISOcenter of the magnet and scanned in the transverse plane.For each scanner, a scanner-specific, phased-array bodycoil (Torso cardiac coil for the Achieva scanner; andbody coil for the Ingenia scanner) was used for thephantom study, and AFs of 2.6 and 4 were used for the3D-T1W-GRE sequence. The acquired voxel size was1.5 9 1.5 9 4.0 mm3.

As SNR measurement using the region of interest(ROI) of the signal intensity (SI) from the object andnoise from the background out of object would notprovide accurate assessment using the PI technique [10,29, 30], we measured the noise via the noise-only scanwith the RF and gradient turned off for the parametersof each of the 3D-T1W-GRE sequences, according torelevant, the previous studies of SNR measurements [31,32]. Both object and noise-only data were reconstructedafter scanning to apply the PI calibration factor and themultichannel data combination to the noise data [31].The ROI for measuring signal and noise was drawn inthe same area as that from three slices in the center areaof the phantom. The SNR was then calculated as follows:SNR = (Rician factor, 1.253)*(SI)/ standard deviationof the noise. The standard deviation of the noise wasestimated from the mean of the noise data, and refer-encing a previous study [32].

Study population

From February 2012 to April 2012, 112 patients under-went liver MRI using a hepatocyte-specific contrastagent (gadoxetic acid, Gd-EOB-DTPA; Primovist� orEovist�; Bayer Healthcare, Berlin, Germany) at 3.0 T(Ingenia, Philips Healthcare) at our institution. Amongthem, 70 patients (M:F = 52:18, median age 61 years,age range 32–80 years) underwent liver MRI includingHR-HBP imaging using AF of four for the followingreasons: (a) hepatocellular carcinoma (HCC) surveillance(n = 49); (b) metastasis surveillance (n = 16; colorectalcancer [n = 7]; pancreas cancer [n = 3]; Klatskin tumor[n = 1]; lung cancer [n = 1]; stomach cancer [n = 1];nasopharyngeal cancer [n = 1]; lymphoma [n = 1];medullary thyroid carcinoma [n = 1]); FLL character-ization (n = 3); and tumor recurrence surveillance afterhemihepatectomy for cholangiocarcinoma (n = 1).

For evaluation of lesion conspicuity, 43 FLLs in23 patients were included: 14 HCCs (1.9 ± 1.1 cm, range

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0.7–4.0 cm); 19 metastases (0.9 ± 0.8 cm, range 0.3–2.8 cm); 6 hemangiomas (1.2 ± 0.7 cm, range 0.5–2.4 cm);3 hepatic cysts (0.8 ± 0.5 cm, range 0.4–1.5 cm,); and 1biopsy-confirmed eosinophilic abscess (4.7 cm). HCCswerediagnosedbasedon the imaging criteria for diagnosingHCCofAssociation for theStudyofLiverDiseasespracticeguideline consisting of arterial enhancement and washoutseen on portal or equilibrium phase images [33]. For met-astatic lesions, the diagnosis was established according tothe characteristicMRI findings, i.e., liver lesionswith lowSIon T1WI and variable, high SI on T2-weighted images(T2WI), irregular or ill-defined borders, rim enhancementseen on MR dynamic images, and exhibiting intervalgrowth of at least 20% in the longest axial diameter as seenon serial cross-sectional imaging inpatientswithunderlyingmalignancy [34–37]. Hemangiomas were defined accordingto the following classical enhancement pattern: strongglobular peripheral enhancement followed by centripetalfilling seen during the portal venous and delayed phases(DPs) on computed tomography (CT) or MR, and nointerval change in size during the follow-up period [37, 38].All hepatic cysts exhibited the following, classical imagingfindings on MR: (a) bright SI on T2WI and low SI onT1WI, and (b) no enhancement after contrast media injec-tion [39].

MR imaging technique

All patients underwent liver MR at on a 3T scanner(Ingenia, Philips Healthcare) equipped with dual-sourceparallel RF excitation technology [24, 26, 40] and directdigital RF receive technology of the same vendor [41],and using a 16-element anterior coil and a built-in pos-terior coil. Routine MR sequences included breath-hold,T2-weighted images, heavily T2-weighted images, diffu-sion-weighted images, and T1-weighted, dual-echo, 3D-GRE images.

A dynamic contrast-enhanced 3D-T1-GRE sequence(enhanced HR isotropic volume excitation sequences:eTHRIVE) was performed during the arterial phase

(AP), portal venous phase (PVP), DP, and HBP, fol-lowing injection of gadoxetic acid (Gd-EOB-DTPA).The standard dose of contrast agent (0.025 mmol/kg)was intravenously administered at a rate of 1.5 mL/s,which was immediately followed by a 20 mL saline flushthrough an antecubital venous catheter using a powerinjector (Spectris Solaris� EP, MEDRAD Inc., War-rendale, PA, USA). After contrast administration,scanning delay times were determined using a real-timeMRI fluoroscopic monitoring technique [28]. AP wasscanned 7 s after contrast media arrival at the distalthoracic aorta, and subsequent PVP and DP were scan-ned 60 s and 3 min, respectively, following contrastinjection. HBP images were also obtained in both theaxial and coronal planes 10 and 20 min after beginningthe contrast medium injection [42]. In order to improvesignal homogeneity of MR images, receive sensitivitycorrection was applied.

In order to determine whether HR T1W-GRE imagescan be obtained within one breath-holding time using ahigh AF, two image sets were obtained using 3D-T1W-GRE sequences in a row during HBP (20 min afterinjection of Gd-EOB-DTPA) in both axial and coronalplanes: conventional image sets, and HR image sets.First, conventional 3D-T1W-GRE set was obtainedusing an AF of 2.6 (2 in the phase-encoding direction(anterior–posterior direction); and 1.3 in the slice-encoding direction). And then, HR 3D-T1W-GRE setusing an AF of four [4 in the phase-encoding direction(right-to-left direction); and zero acceleration in the slice-encoding direction] was achieved. Based on our phantomstudy results, we decided to use an AF of four for HR3D-T1W-GRE sequence. In order to limit the aliasingartifacts arising from objects outside of the FOV, 40%

and 28 % phase oversamplings were used for the con-ventional image set with an AF of 2.6 and for the HRimage set with an AF of 4, respectively. Interpolationwas performed in the slice–select directions for both theconventional 3D-T1W-GRE sequence (6-mm true STacquisition) and HR 3D-T1W-GRE sequence (3-mm

Table 1. Imaging parameters of HBP with the two different parallel acquisition AFs

Conventional 3D-T1W-GRE with AF of 2.6 High-resolution 3D-T1W-GRE with AF of 4

Axial Coronal Axial Coronal

TR/TE (ms) 3.3/1.61 2.9/1.45 3.5/1.71 3.2/1.59FA (�) 10 10 10 10Bandwidth (Hz/pixel) 724 1091.2 715.1 953.6FoV (mm2) 380 9 343 380 9 347 380 9 320 450 9 450Slice thickness (ST/gap, mm)a 6/3 6/3 3/1.5 3/1.5Matrix size 332 9 298 332 9 249 380 9 320 452 9 448Acquired voxel size (mm3) 1.14 9 1.15 9 3.0 1.14 9 1.4 9 3.0 1.0 9 1.0 9 1.5 1.0 9 1.0 9 1.5Reconstructed voxel size (mm3) 0.99 9 0.99 9 3.0 1.08 9 1.07 9 3.0 0.99 9 0.99 9 1.5 0.94 9 0.94 9 1.5NEX 1 1 1 1Acquisition time (s) 16 18.1 18.5 17.6

3D, three dimensional; T1W-GRE, T1-weighted gradient-recalled-echo; AF, acceleration factor; TR, repetition time; TE, echo time; FA, flip angle;FoV, field of view; NEX, number of excitationa Conventional and high-resolution acquisition covered the same slice coverage

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true ST acquisition). Acquired voxel size of each con-ventional and HR axial 3D-GRE image sets were1.14 9 1.15 9 3 mm3 and 1.0 9 1.0 9 1.5 mm3, respec-tively: acquired voxel size and reconstruction voxel sizeare shown in Table 1. The scanning parameters of theconventional 3D-T1W-GRE sequence and HR 3D-T1W-GRE sequence in both the axial and coronal planes aredescribed in Table 1.

When both the coronal and axial HR 3D-T1W-GREimage sets were obtained 20 min after the administrationof gadoxetic acid, patients were requested to place theirarms in a supine position. The ‘‘arms up’’ position wasused to avoid aliasing by the arms along the phase-encoding direction (right to left) and to not to spendmore time doing oversampling for the arms. Therefore,HR T1W-GRE imaging (1 9 1-mm in-plane resolution)was achieved in the same amount of acquisition time asconventional, 3D-T1-GRE imaging (16–18.5 s). This‘‘arms up’’ position was possible because of the largerbore magnet of the 3T scanner used in our study (70 cmin diameter), thus providing enough space to easily applythe ‘‘arms up’’ position, especially in obese patients, andwhich might not have been the case with standard bores(60 cm). PI was performed using a new version of theSENSE reconstruction algorithm (ds-SENSE), which isbased on the coil sensitivity information which can beused to unfold the spatial aliasing and fold-over artifactsin the image space, using an accurate estimation of thecoil sensitivity information [10, 43].

Image analysis

The image quality of the four HBP image sets of eachsession was evaluated by two attending abdominal radi-ologists (reviewer 1, M.H.Y.; reviewer 2, J.H.Y.) with 8and 7 years of clinical experience including 3 years ofbody MR interpretation for each. The radiologists wereblinded to the MR parameters of those image setsincluding the AFs. Four image sets— conventional 3D-T1W-GRE sequences with an AF of 2.6: axial andcoronal; 3D-T1W-GRE sequences with an AF of 4: axialand coronal—were provided. The order of the image setswas randomly distributed for the two radiologists. Allimage reviews were performed using a picture archivingand communication system (Maroview 5.4, Infinitt,Seoul, Korea) and monitors with a spatial resolution of1600 9 1200 (Totoku, Japan). The readers independentlyassessed the degree of the artifact, image noise, and theimage quality using several factors such as the anatomicalorgan conspicuity, bile duct conspicuity, and the overallimage quality. To avoid a learning bias, reviews of theimage sets were performed at a 2-week interval. Aftercomplete initial individual analysis, a comprehensive re-view was also performed in consensus for each image set.

Before the formal evaluation, the image quality andartifact evaluation criteria were established by consensus

among three radiologists (J.H.Y., M.H.Y., and J.M.L.with 21 years of experience in abdominal MR). Allevaluation items were independently assessed by tworeaders (reviewer 1, M.H.Y.; reviewer 2, J.H.Y.). Thedegree of motion artifact was graded on a five-point scaleas follows referencing previous studies [44, 45]: score 1,nondiagnostic images; score 2, severe artifacts causingimpaired diagnostic capability of the readers; score 3,moderate artifacts without diagnostic impairment; score4, mild artifacts; score 5, no or only minimal artifacts.The image noise was defined according to how granularthe images were and was scored using a 1–5 point scale asfollows: score 1, unacceptable noise; score 2, increasednoise at an above average level; score 3, average noise atan acceptable level; score 4, less than average noise; andscore 5, no or minimum noise [46]. The presence ofwraparound artifact at the center of the image resultingfrom the PI was recorded, and the incidences in each AFgroup were compared [47].

Spatial resolution was assessed by evaluating theanatomical organ conspicuity using a five-point scale. Itincluded the following items: liver edge; pancreas ante-rior margin; and hepatic vessels [48]. The five-point scorewas as follows: score 1, very poor; score 2, suboptimal;score 3, acceptable; score 4, above average; and score 5,excellent. Bile duct conspicuity was also assessed using afive-point scale for contrast resolution as follows: score1, a bile duct was not delineated; score 2, a bile duct waspartly delineated and showed a blurry margin; score 3,the entire bile duct was shown although the margin wasblurry; score 4, the whole bile duct including the second-order branch was delineated with a blurry margin or thebile duct including the first-order branch was delineatedwith a clear margin; score 5, common bile duct and thefirst- and second-order branches of the intrahepatic ductwere delineated with a sharp and clear margin [49]. Fi-nally, the overall image quality was graded on a five-point scale: score 1, unreadable; score 2, poor; score 3,acceptable; score 4, good; and score 5, excellent [45].

In 23 patients with FLLs, the readers independentlyscored MR images for lesion conspicuity using a five-point scale as follows: score 1, not delineated; score 2,barely detected; score 3, the lesion was delineated but themargin was blurry; score 4, the lesion was clearly de-picted although the margin was not discrete; and score 5,the lesion had a sharp margin and clear contrast to thesurrounding liver parenchyma [50].

Statistical analysis

The Wilcoxon Signed-rank test was used for evaluatingthe differences in grading for the image quality assess-ment in the conventional 3D-T1W-GRE image sets withan AF of 2.6 vs. the HR 3D-T1W-GRE image sets withan AF of 4 during the HBP. The interobserver agreementof the image quality assessment for various items was

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evaluated using the weighted kappa test. A j value of 0indicated poor; 0.01–0.20, slight; 0.21–0.40, fair; 0.41–0.60, moderate; 0.61–0.80, good; and 0.81–1.00 excellentagreement [51]. All statistical analyses were performedusing commercially available software (IBM SPSS, ver-sion 19, SPSS Inc., IBM Company, Armonk, NY, USA;Medcalc, Medcalc Software, Mariakerke, Belgium), anda p-value less than 0.05 was considered to indicate asignificant difference.

Results

Preliminary phantom study

In the phantom experiment, the SNR was 28% higher on3D-T1W-GRE with an AF value of 2.6 on the scanner

(Ingenia) with the dual RF transmitter and the directdigital receiver than on the scanner (Achieva) withoutthem (219.73 vs. 171.42, respectively). The SNR on 3D-T1W-GRE with an AF of 4 on the scanner with the dualRF transmitter and the direct digital RF receiver was178.36 which was similar to the SNR on 3D-T1W-GREwith an AF of 2.6 on the scanner without them (Fig. 1).Therefore, based on the phantom study results, an AF offour was used for HR 3D-T1W-GRE for this patientsstudy.

Patient study

According to the results of the image quality assessmentperformed by the two independent reviewers, the overall

Fig. 1. Three-dimensional, T1-weighted gradient-echo (3D-T1W-GRE) images of the two L13 phantoms filled with fluid intwo different scanners. Signal (A) and noise (B) maps of thephantom on 3D-T1W-GRE images with an AF of 4 in thescanner equipped with dual RF transmitter and direct digitalreceive technology (Ingenia). Signal (C) and noise (D) maps

of the phantom on 3D-T1W-GRE images (Achieva) with anAF of 2.6 in the scanner without those options. According tothe SNR measurement, both showed similar values, i.e.,178.36 on 3D-T1W-GRE with an AF of 4 in the scanner withthe dual RF transmitter and direct digital receive technology,whereas it was 171.42 in the scanner not equipped with them.

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image quality of both the axial and coronal HR 3D-T1W-GRE image sets using an AF of 4, was significantlybetter compared with the conventional 3D-T1W-GREimages with an AF of 2.6 according to both the reviewers(p < 0.0001): 3.77 ± 0.82 vs. 4.37 ± 0.76 for reviewer 1and 3.79 ± 0.74 vs. 4.43 ± 0.71 for reviewer 2. Theconsensus review also demonstrated the same results,thus demonstrating the better results of the HR 3D-T1W-GRE image sets than of the conventional 3D-T1W-GRE image sets (p < 0.05). For both reviewers 1and 2, the motion artifact was also significantly de-creased, and the conspicuity of the major upperabdominal anatomical structures, including the liveredge, pancreas anterior margin, hepatic vessels, and bileduct, was significantly improved on the HR 3D-T1W-GRE images over that seen on the conventional 3D-T1W-GRE images in both the axial and coronal planes(p < 0.0001) (Tables 2, 3; Figs. 2, 3). Similarly, theconsensus review also demonstrated that HR 3D-T1W-GRE image sets showed better results than conventional3D-T1W-GRE image sets with regard to both thesharpness of the key anatomic structures and the motionartifact (Table 4).

However, according to the consensus review, the im-age noise was significantly greater on HR 3D-T1W-GREimages than on conventional 3D-T1W-GRE images

(p < 0.0001): 4.26 ± 0.63 vs. 3.75 ± 0.54 on the axialimage set and 4.51 ± 0.50 vs. 3.66 ± 0.54 on the coronalimage set (Table 4). For reviewers 1 and 2, the imagenoise was significantly greater on HR image sets than onconventional image sets, and in both the axial and coro-nal planes (p < 0.0001). However, there was no wrap-around artifact on axial and coronal images in both 3D-T1W-GRE images (Table 3).

In addition, the HR 3D-T1W-GRE set showed betterresults regarding the lesion conspicuity than the con-ventional 3D-T1W-GRE set: 3.72–4.42 (p < 0.0001) forreviewer 1 and 3.51–4.63 for reviewer 2 (p < 0.0001).The score of the lesion conspicuity in the consensus re-view was also significantly higher on HR 3D-T1W-GREimages (mean score 3.53 ± 1.03) than on conventional3D-T1W-GRE images (mean score 4.62 ± 0.54)(p < 0.0001) (Fig. 4). Specifically, on consensus review,33–43 lesions (76.7%) showed improved lesion conspi-cuity on the HR 3D-T1W-GRE image set compared tothat of the conventional 3D-T1W-GRE set, and therewere no lesions showing a lesser score for lesion con-spicuity on the HR 3D-T1W-GRE image set.

Overall, the two readers showed good to excellentinterobserver agreement on all of the evaluated items,and with the k values in the range of 0.63–1.0. Regardinglesion conspicuity, the two radiologists showed good

Table 2. Qualitative analysis results of independent review for two axial T1WI sets with AF 2.6 and 4

Reviewer 1 p-Value Reviewer 2 p-Value

Conventional3D-T1W-GRE

High-resolution3D-T1W-GRE

Conventional3D-T1W-GRE

High-resolution3D-T1W-GRE

Motion artifact 3.67 ± 0.60 3.94 ± 0.45 0.0008 3.66 ± 0.56 3.97 ± 0.42 <0.0001Liver edge sharpness 3.37 ± 0.71 4.06 ± 0.68 <0.0001 3.36 ± 0.64 4.16 ± 0.67 <0.0001Pancreas margin 3.71 ± 0.84 4.24 ± 0.82 <0.0001 3.67 ± 1.0 4.26 ± 0.86 <0.0001Hepatic vessel conspicuity 2.96 ± 1.07 3.60 ± 1.12 0.0009 2.97 ± 1.03 3.61 ± 1.17 <0.0001Bile duct conspicuity 4.48 ± 0.76 4.86 ± 0.39 0.0003 4.64 ± 0.70 4.86 ± 0.43 0.0084Image noise (pixel graininess) 4.41 ± 0.55 3.75 ± 0.57 <0.0001 4.26 ± 0.63 3.76 ± 0.52 <0.0001Overall image quality 3.77 ± 0.82 4.37 ± 0.76 <0.0001 3.79 ± 0.74 4.43 ± 0.71 <0.0001Wraparound artifact 0% (0/70) 0% (0/70) 0% (0/70) 0% (0/70)Lesion conspicuity 3.72 ± 1.10 4.42 ± 0.52 <0.0001 3.51 ± 0.95 4.63 ± 0.62 <0.0001

T1WI, T1 weighted image; 3D, three-dimensional, T1W-GRE, T1-weighted gradient-recalled-echo; Conventional T1W-GRE, T1WI using AF of 2.6;HR T1W-GRE, T1WI using AF of 4; p-value was calculated using the Wilcoxon Signed-Rank Test. Values are mean ± standard deviation

Table 3. Qualitative analysis results of independent review for the two coronal T1WI image sets with AF 2.6 and 4

Reviewer 1 p-Value Reviewer 2 p-Value

ConventionalT1W-GRE

High-resolutionT1W-GRE

ConventionalT1W-GRE

High-resolutionT1W-GRE

Motion artifact 3.53 ± 0.63 3.83 ± 0.38 0.0043 3.56 ± 0.63 3.81 ± 0.39 0.0131Liver edge sharpness 3.26 ± 0.63 4.04 ± 0.65 <0.0001 3.26 ± 0.70 4.07 ± 0.62 <0.0001Pancreas margin 3.01 ± 1.01 3.49 ± 1.0 <0.0001 2.99 ± 0.99 3.43 ± 0.97 <0.0001Hepatic vessel conspicuity 2.81 ± 0.98 3.39 ± 1.04 <0.0001 2.89 ± 1.02 3.44 ± 1.07 <0.0001Bile duct conspicuity 4.46 ± 0.81 4.90 ± 0.30 <0.0001 4.47 ± 0.81 4.88 ± 0.32 0.0002Image noise (pixel graininess) 4.51 ± 0.50 3.66 ± 0.54 <0.0001 4.51 ± 0.50 3.66 ± 0.51 <0.0001Overall image quality 3.24 ± 0.77 4.16 ± 0.72 <0.0001 3.26 ± 0.77 4.29 ± 0.64 <0.0001Wraparound artifact 0% (0/70) 0% (0/70) 0% (0/70) 0% (0/70)

T1WI, T1 weighted image; T1W-GRE, T1-weighted gradient-recalled-echo; Conventional T1W-GRE, T1WI using AF of 2.6; HR T1W-GRE, T1WIusing AF of 4; p-value was calculated using the Wilcoxon Signed-Rank Test. Values are mean ± standard deviation

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Fig. 2. MR images in 51-year-old woman who was treated for HCC. Compared with conventional 3D-T1W-GRE image (A), HR3D-T1W-GRE image (B) showed better liver-edge sharpness and hepatic vessel conspicuity.

Fig. 3. MR images in 50-year-old man who underwent liverMR for HCC surveillance. Compared with conventional 3D-T1W-GRE image (A), HR 3D-T1W-GRE image (B) showed

better hepatic vessel conspicuity and liver edge sharpness aswell as SMA and SMV conspicuities in coronal planes.

Table 4. Qualitative analysis results of consensus review for axial, coronal T1WI images with AF of 2.6 and 4

Axial p-Value Coronal p-Value

Conventional3D-T1W-GRE

High-resolution3D-T1W-GRE

Conventional3D-T1W-GRE

High-resolution3D-T1W-GRE

Motion artifact 3.66 ± 0.54 3.94 ± 0.45 0.0012 3.51 ± 0.63 3.81 ± 0.39 0.0053Liver edge sharpness 3.6 ± 0.79 4.14 ± 0.67 <0.0001 3.21 ± 0.66 4.07 ± 0.64 <0.0001Pancreas margin 3.53 ± 0.99 4.23 ± 0.85 <0.0001 3.0 ± 0.99 3.46 ± 0.97 <0.0001Hepatic vessel conspicuity 3.09 ± 1.05 3.64 ± 1.13 <0.0001 2.87 ± 1.03 3.40 ± 1.06 <0.0001Bile duct conspicuity 4.60 ± 0.75 4.86 ± 0.43 0.0027 4.46 ± 0.81 4.90 ± 0.30 0.0001Image noise (pixel graininess) 4.26 ± 0.63 3.75 ± 0.54 <0.0001 4.51 ± 0.50 3.66 ± 0.54 <0.0001Overall image quality 3.83 ± 0.82 4.4 ± 0.71 <0.0001 3.23 ± 0.75 4.16 ± 0.69 <0.0001Lesion conspicuitya 3.53 ± 1.03 4.62 ± 0.54 <0.0001 – – –

T1WI, T1 weighted image; 3D, three dimensional; T1W-GRE, T1-weighted gradient-recalled-echo; Conventional T1W-GRE, T1WI using AF of 2.6;HR T1W-GRE, T1WI using AF of 4; Values are mean ± standard deviationa Lesion conspicuity was assessed on axial images

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agreement regarding both the conventional 3D-T1W-GRE image set (j = 0.654) and the HR 3D-T1W-GREimage set (j = 0.729).

Discussion

HR 3D-T1W-GRE images seem to be clinically feasibleusing 2D, parallel acquisition technique with a high AFat 3T scanner with a multichannel RF transmitter [24,26] and direct digital RF receive technology [41]. Con-sidering that they were achieved during one breath-holdperiod (16–18.5 s), and can provide improve imagequality, it would be more advantageous than conven-tional 3D-T1W-GRE images when it is used for evalu-ation of FLLs. Our study results demonstrate that theHR 3D-T1W-GRE image sets obtained using an AF of 4during the HBP provided significantly better imagequality than the conventional 3D-T1W-GRE image setswith an AF of 2.6 (Table 1). We believe that although wewere not able to assess diagnostic performance of the twoimage sets for detection of FLLs, theoretically, the HR3D-T1W-GRE images should be beneficial for detectingsmall lesions and for delineating small, intrahepatic

anatomic structures. In fact, the HR 3D-T1W-GREimages showed better conspicuity of anatomic structuresincluding the liver edge, pancreas margin, bile duct, andhepatic vessels as well as better lesion conspicuity thandid conventional 3D-T1W-GRE images, because of thehigher spatial resolution. We believe that HR 3D-T1WIwith a high AF could contribute toward achieving inclinical practice high-quality liver MR examinations.

The technical feasibility of using a higher AF up to 4with the SENSE than conventional AFs of 2 forobtaining HR breath-hold T1WI in our study could beattributed to several factors. First, we changed the phase-encoding direction from anterior–posterior to right–leftto use higher AFs, while minimizing motion-relatedresidual aliasing artifact because of a mis-mapping of coilsensitivity. As the SENSE technique requires accurateestimation of the coil sensitivity information, we believethat using a high AF in the phase-encoding directionalong the right to left direction of the patient’s bodywhich has less respiration-related motion, might result infewer artifacts compared to those seen in the traditional,phase-encoding direction in the anteroposterior direction[23]. Second, a new version of SENSE (ds-SENSE) which

Fig. 4. MR images in 52-year-old woman with medullarythyroid carcinoma liver metastasis. On conventional 3D-T1W-GRE image, two metastases (arrowheads) were shown in theliver S7 and S5 (A, B). These metastases were more distinctly

seen on HR 3D-T1W-GRE image (C, D), as clear margins ofthe liver lesions and the hepatic vessel conspicuities wereprovided.

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minimizes artifacts by coil insensitivity also contributedto HR 3D-T1W-GRE images. Theoretically, as theSENSE technique requires accurate estimation of the coilsensitivity maps, a separate calibration scan is requiredwith a previous version SENSE before a real acceleratedscan. However, the reconstructed images may sufferfrom artifacts related to misalignment if patient motionor differences in the depth of respiration developed be-tween the calibration and the accelerated acquisition [48].This problem was partially solved using this new versionof SENSE which incorporates a calibration scan within areal SENSE scan. In addition, coil sensitivity inaccuracy-tolerant-SENSE technique was adapted [43]. Third, thenew phased-array body coils equipped with the newdigitalized RF receive technology also improved theimage quality by increasing the SNR as well as providinglow g-factors with various combinations of accelerationalong phase-encoding direction [52]. Finally, we also re-quested patients to maintain an ‘‘arms up’’ position toremove the aliasing effect caused by the ‘‘arms down’’position, when we selected the right-left direction as thephase-encoding direction. When using the ‘‘arms up’’position, as we could avoid oversampling which is nec-essary to avoid aliasing of the arms into the abdomen, wecould shorten the acquisition time even more by notspending time oversampling (40% for conventional im-age sets vs. 28% for HR image sets). The ‘‘arms up’’position was possible in all of our study patients becausewe used a 3T scanner with a large-bore magnet (70 cm),as it was difficult or uncomfortable to achieve whenusing a 3T scanner with a standard magnet bore (60 cm),especially in obese patients or patients with a large bodyhabitus.

It is interesting to note that although the image noiseincreased on HR 3D-T1W-GRE images with an AF of 4compared to that of conventional 3D-T1W-GRE imageswith an AF of 2.6, it was still in at least the average oreven less than average range (the mean image noisescores: 3.75 for the axial image set and 3.66 for thecoronal image set), and which was suggestive of a clini-cally acceptable level. Indeed, in our study, there was nopatient in whom HR T1WI using an AF of 4 showedeither diagnostically unacceptable image noise or anunacceptable motion artifact. This observation wassupported by our phantom study results which showedsimilar noise levels of two image sets that were acquiredat 3T scanner equipped with the dual RF transmitter anddirect digital receive technology using a high AF or at 3Tscanner not equipped with the dual RF transmitter anddirect digital receive technology using an AF of 2.6. Aswe discussed earlier, several techniques for increasing theSNR, including digitalized RF receive technology anddual-source parallel RF excitation, likely mitigated thehigh image noise resulting from the use of high AFs [26,48]. Enhanced B1 field homogeneity by applying dual-source, parallel RF excitation technology may also help

us obtain consistently stable HR 3D-T1W-GRE images[53]. Several studies demonstrated that dual-source RFexcitation technology could create a more homogenousB1 magnetic field by obtaining detailed RF shimming[24, 25] and therefore could provide contrast uniformityacross the FOV and consequently contribute to betterimage quality, especially on a high-field (3T) MR scan-ner. We believe that in T1W-GRE imaging with a higherAF, the homogenous B1 field might help one to suppressthe aliasing effects arising from sampling density reduc-tion.

According to our results, the HR 3D-T1W-GREimage sets using a high AF were clinically acceptable andeven provided better image quality compared with theconventional 3D-T1W-GRE image sets during the HBPof gadoxetic acid-enhanced MRI. Currently, liver T1WIis most commonly obtained with FS 3D GRE, andtypically, it requires 23 s to cover the liver with an in-plane resolution of 320 9 160, partition thickness of5 mm, and an AF of 2 [23]. Given that PI techniques andpartial Fourier techniques are already used to shorten theacquisition time to enable single breath-hold imaging, itmight realistically not be possible to change the technicalparameters to further improve the spatial resolution.Therefore, our study results demonstrating the technicalfeasibility of HR 3D-T1W-GRE images using a high AFin approximately 18 s, are clinically significant. Fur-thermore, if we use our high-speed imaging acquisitionmethod to further reduce the imaging acquisition time,although at the same spatial resolution as that of con-ventional 3D-T1W-GRE, we could acquire 3D-T1W-GRE images within 12 s. In fact, there is a study ofhighly accelerated T1WI in liver MRI [54]. 2D PIacquisition reduced scan time without deteriorating im-age quality by lowering g-factors [54]. Although themethod to improve SNR and lower g-factors was dif-ferent from that we used in this study, both studiesshowed clinical feasibility of highly accelerated T1WI inabdominal MRI. Based on our observation, we believethat HR T1WI with a high AF could contribute toobtaining a high-quality liver MR examination, not onlyfor HBP imaging but also for a routine dynamic se-quence because its acquisition time is comparable to thatof the currently used 3D GRE sequence [23, 55]. Inaddition, although it might be too early to definitelymake this conclusion, ds-SENSE with high AF might beused for other sequences such as T2WI, diffusion-weighted imaging, and MR angiography to assure betterimage quality and spatial resolution, and the total liverMR examination time might be able to be shortened to15–20 min. Further studies will be required to test thefeasibility of this approach using ds-SENSE with a highAF for whole-liver MR imaging.

Our study has limitations. First, there were only asmall number of patients with FLLs who were includedin the lesion conspicuity evaluation. Therefore, we could

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not evaluate the diagnostic performance of the HR 3D-T1W-GRE image sets compared with the conventional3D-T1W-GRE image sets. Further study regarding thediagnostic performance of HR 3D-T1W-GRE imagingin a larger study population will be required. Second, wedid not use the HR 3D-T1W-GRE sequence for dy-namic-phase imaging which might be a key sequence inliver MRI, for, as the temporal window for the arterial orportal phase lasts only 10–30 s, we could, therefore, notobtain two 3D-T1W-GRE image sets using different AFsin a single phase. However, we believe that, based on ourstudy results, further prospective comparison studies ofthe HR 3D-T1W-GRE sequence versus the conventional3D-T1W-GRE sequence performed in the same individ-uals, will be quite useful. In addition, high flip angle (FA)is known to improve contrast resolution, compared withFA of 10� that we used in this study. Therefore, furtherstudy for clinical feasibility of combining high contrastresolution using high FA and high spatial resolutionusing high AF is warranted.

In conclusion, the 3D-T1W-GRE sequence using ahigh AF of four is a clinically promising and applicablesequence as it improves not only the spatial resolutionbut also the image quality and provides better lesionconspicuity without prolonged acquisition time in gad-oxetic acid-enhanced liver MRI.

Acknowledgment. The authors thank Bonnie Hami, M.A. (USA), forher editorial assistance.

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