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Eur Radiol (2014) 24:320326

DOI 10.1007/s00330-013-3026-4

PEDIATRIC

Free-breathing contrast-enhanced T1-weighted gradient-echo


imaging with radial k-space sampling for paediatric
abdominopelvic MRI
Hersh Chandarana & Kai T. Block & Matthew J. Winfeld &
Shailee V. Lala & Daniel Mazori & Emalyn Giuffrida &
James S. Babb & Sarah S. Milla

Received: 21 June 2013 / Revised: 13 August 2013 / Accepted: 6 September 2013 / Published online: 25 September 2013
# European Society of Radiology 2013

Abstract
Objective To compare the image quality of contrast-enhanced
abdominopelvic 3D fat-suppressed T1-weighted gradientecho imaging with radial and conventional Cartesian k-space
acquisition schemes in paediatric patients.
Methods Seventy-three consecutive paediatric patients were
imaged at 1.5 T with sequential contrast-enhanced T1weighted Cartesian (VIBE) and radial gradient echo (GRE)
acquisition schemes with matching parameters when possible.
Cartesian VIBE was acquired as a breath-hold or as free breathing in patients who could not suspend respiration, followed by
free-breathing radial GRE in all patients. Two paediatric radiologists blinded to the acquisition schemes evaluated multiple
parameters of image quality on a five-point scale, with higher
score indicating a more optimal examination. Lesion presence
or absence, conspicuity and edge sharpness were also evaluated. Mixed-model analysis of variance was performed to compare radial GRE and Cartesian VIBE.
Results Radial GRE had significantly (all P <0.001) higher
scores for overall image quality, hepatic edge sharpness, hepatic
vessel clarity and respiratory motion robustness than Cartesian
VIBE. More lesions were detected on radial GRE by both readers
than on Cartesian VIBE, with significantly higher scores for
lesion conspicuity and edge sharpness (all P <0.001).
Conclusion Radial GRE has better image quality and lesion
conspicuity than conventional Cartesian VIBE in paediatric
patients undergoing contrast-enhanced abdominopelvic MRI.

H. Chandarana (*) : K. T. Block : M. J. Winfeld : S. V. Lala :


D. Mazori : E. Giuffrida : J. S. Babb : S. S. Milla
Department of Radiology, New York University Langone Medical
Center, 660 First Avenue, New York, NY 10016, USA
e-mail: Hersh.Chandarana@nyumc.org

Key Points
Numerous techniques are required to provide optimal MR
images in paediatric patients.
Radial free-breathing contrast-enhanced acquisition demonstrated excellent image quality.
Image quality and lesion conspicuity were better with radial
than Cartesian acquisition.
More lesions were detected on contrast-enhanced radial
than on Cartesian acquisition.
Radial GRE can be used for performing abdominopelvic
MRI in paediatric patients.
Keywords Radial k-space sampling . Radial VIBE .
Paediatric abdominopelvic MRI . Contrast-enhanced
T1-weighted gradient-echo imaging . Free-breathing
abdominal MRI

Introduction
Magnetic resonance imaging is increasingly utilised in the
evaluation of abdominopelvic problems in paediatric patients
because it lacks ionising radiation and provides superior soft
tissue contrast [13]. Nevertheless, there are various challenges
to the widespread acceptance of paediatric MRI in clinical
practice, including long examination times and motion-related
artefacts [4]. Physiological and bulk motion, including respiratory motion, cardiac pulsation and bowel peristalsis, can degrade the image quality of an abdominopelvic MR examination
and can render images non-diagnostic [58].
The three-dimensional T1-weighted gradient echo sequence
with Cartesian k-space sampling (Volume Interpolated Breathhold Examination, or VIBE) performed before and after intravenous injection of gadolinium contrast agent is an important

Eur Radiol (2014) 24:320326

321

component of the paediatric abdominopelvic MR examination


[1]. In routine clinical practice, contrast-enhanced VIBE acquisition is performed either during a breath hold in patients
who understand and follow oral commands, or during free
breathing in paediatric patients who cannot follow commands or suspend respiration. MR imaging in young paediatric patients is often performed with sedation such as general anaesthesia to decrease bulk motion [9, 10]. Because
sedated patients cannot follow commands or suspend respiration if not intubated, conventional Cartesian VIBE is
performed essentially during free breathing, leading to substantial respiratory motion-related artefacts. Even older, nonsedated paediatric patients who understand and follow oral
commands may have difficulty suspending respiration for 10
to 20 s, resulting in suboptimal or non-diagnostic images.
Proposed alternatives to the breath-hold examination include a respiratory-navigated free-breathing 3D T1-weighted
technique [1113]. However, respiratory-navigated sequences can result in unpredictable acquisition times that
may limit the diagnostic utility of contrast-enhanced
abdominopelvic imaging, as acquiring images within a certain time after contrast agent administration may be important for diagnosis. Another alternative is a recently developed, modified fat-suppressed 3D T1-weighted spoiled
gradient-echo sequence that uses the stack-of-stars scheme
to acquire volumetric k-space data [radial gradient echo
(GRE)]. This sequence performs Cartesian sampling along
the slice dimension (kz) and radial sampling in plane (along
ky and kx) [1417]. A recent study suggests that the freebreathing radial GRE sequence might result in images of
comparable quality to the conventional breath-hold VIBE in
adult patients who can adequately suspend respiration [17].
However, there are limited data comparing these acquisition
schemes in paediatric patients, for whom radial freebreathing acquisitions can be more beneficial than the conventional Cartesian sampling scheme.
Therefore, the purpose of our study was to compare the
image quality of contrast-enhanced abdominopelvic 3D fatsuppressed T1-weighted gradient-echo imaging with freebreathing radial and conventional Cartesian k-space acquisition schemes in paediatric patients.

Materials and methods


Patient population
This Health Insurance Portability and Accountability Act
(HIPAA)-compliant retrospective single-centre study was
performed after obtaining waiver for informed consent from
our institutional review board. Patients presenting to our department for clinically indicated paediatric MRI from November 2011 to November 2012 and who underwent imaging on a
single 1.5-T MRI system (MAGNETOM Avanto, Siemens
Healthcare, Erlangen, Germany) on which the radial GRE
sequence is available were enrolled. Seventy-three consecutive patients (44 male and 29 female) with mean age of
7.5 years, range 2 months to 18 years (boys with a mean
age of 7.2 years, range 2 months to 17 years; girls with a
mean age of 8 years, range 6 months to 18 years) constituted our study cohort and underwent imaging for various clinical indications: known or suspected malignancy/
mass workup (n =30), known or suspected IBD/colitis (n =
14), known or suspected tuberous sclerosis (n =10), workup of hydronephrosis/UPJ obstruction or haematuria (n =
6), neurofibromatosis (n =2), known or suspected vascular
pathological condition (n =4), jaundice/pancreatitis (n =3)
and sickle cell disease/iron overload (n =4). Forty-six patients received sedation in the form of deep general anaesthesia and were spontaneously ventilated; thus imaging
was performed with free breathing. Twenty-seven patients
were not sedated and thus were imaged in an attempted
breath-hold for conventional Cartesian acquisition and in
free breathing for radial GRE.
MR Acquisition
Magnetic resonance imaging was performed in all patients on a
1.5-T clinical system using torso phased-array coils. All patients underwent a routine imaging protocol that included conventional axial 3D T1-weighted gradient-echo fat-suppressed
acquisition before and after injection of gadopentetate
dimeglumine (Magnevist, Bayer Healthcare). Dynamic injection of 0.1 mmol of Magnevist per kilogram of body weight

Table 1 Scoring scale for image and lesion quality parameters


Image quality parameter

Score

Scoring system

Overall image quality


Hepatic edge sharpness
Hepatic vessel clarity
Respiratory motion robustness
Lesion conspicuity
Lesion edge sharpness

15
15
15
15
15
15

1, Unacceptable; 2, poor; 3, acceptable; 4, good; 5, excellent


1, Unreadable; 2, extreme blur; 3, moderate blur; 4, mild blur; 5, no blur
1, Unreadable; 2, extreme blur; 3, moderate blur; 4, mild blur; 5, no blur
1, Unreadable; 2, extreme artefact; 3, moderate artefact; 4, mild artefact; 5, none
1, Unreadable; 2, poor; 3, acceptable; 4, good; 5, excellent
1, Unreadable; 2, extreme blur; 3, moderate blur; 4, mild blur; 5, no blur

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Table 2 Image quality scores for
radial GRE and conventional
Cartesian VIBE stratified by
reader

Eur Radiol (2014) 24:320326

Parameter

Overall image quality


Hepatic edge sharpness
Hepatic vessel clarity
Resp. motion robustness

Reader 1
Cartesian
Mean SD

Radial
Mean SD

Cartesian
Mean SD

Radial
Mean SD

2.90.8
3.00.8
2.790.8
3.61.0

4.20.7
4.30.6
4.10.8
5.00.2

<0.001
<0.001
<0.001
<0.001

3.00.9
3.11.0
3.10.9
3.51.0

4.50.6
4.60.6
4.30.7
5.00.0

<0.001
<0.001
<0.001
<0.001

was administered, followed by a 20-ml saline flush at a rate of


2 ml/s using a power injector (Spectris, Medrad, Pittsburgh, PA,
USA). Conventional Cartesian VIBE was acquired during
breath-hold or free breathing in patients who could not suspend
respiration with the following parameters: TR/TE (ms) 3.27
3.98/1.201.99, flip angle 12, slice thickness 22.5 mm, matrix 19225688216, BW 480 Hz/pixel, frequency-selective
fat saturation and parallel imaging factor of 2. Acquisition time
ranged from 10 to 20 s. Immediately after completion of the
conventional post-contrast acquisition, a free-breathing radial
GRE acquisition was performed with matching parameters
where possible: slice thickness 22.5 mm, flip angle 12, TR/
TE (ms) 3.663.94/1.511.97, matrix 256256, BW 480 Hz/
pixel and quick fat saturation mode. Resolution in phase
encoding direction and thus spatial resolution with radial acquisition were higher compared with the conventional VIBE.
Six hundred radial spokes were acquired with the stack-ofstars scheme over 90120 s. Image reconstruction for the
radial GRE was performed inline at the MRI with a standard
gridding procedure that included correction of k-space shifts
caused by gradient timing imperfections.
MR image analysis
All image data sets (radial GRE and conventional Cartesian
post-contrast VIBE) were stripped of patient and acquisition
parameter details and presented in a blinded fashion and random order to two board-certified radiologists with certification
of additional qualification (CAQ) in paediatric radiology with 6
and 3 years of experience (readers 1 and 2, respectively). Both
readers evaluated all images independently on a commercially
Fig. 1 Interval plot of (A) overall
image quality (IQ) and (B) lesion
conspicuity for the two readers for
conventional Cartesian VIBE and
radial gradient echo (GRE)
imaging

Reader 2

available PACS workstation (Philips iSite, Foster City, CA,


USA).
For each data set, each reader independently scored the
following parameters of image quality using a 1-5 scale, with
the highest score indicating the most desirable examination:
overall image quality, hepatic edge sharpness, hepatic vessel
clarity and respiratory motion robustness (Table 1). Lesion
presence or absence, lesion conspicuity and lesion edge sharpness were also evaluated on a five-point scale (Table 1).
Statistical analysis
Mixed model analysis of variance (ANOVA) was used to compare sequences in terms of image quality. The ratings provided
by the two readers for both sequences served as the dependent
variables. Logistic regression for correlated data was used to
assess and compare the sequences in terms of lesion detection.
Specifically, generalised estimating equations (GEE) based on
binary logistic regression were used to model the probability of
lesion detection. Each mixed and logistic model included reader
as a blocking factor and sequence as a fixed classification factor.
To account for statistical dependencies among the ratings derived
for the same patient, subject ID was incorporated into the mixed
and logistic models as a random classification factor. As a result,
the correlation structure was modelled by assuming observations
to be correlated only when acquired from the same subject. For
the ANOVA, the error variance was allowed to vary across
sequences to remove the assumption of variance equality and
the normality assumption underlying the analyses were found
through residual plots and Shapiro-Wilk tests to be reasonably
met. All statistical tests were conducted at the two-sided 5 %

Eur Radiol (2014) 24:320326

323

Fig. 2 A 6-month-old patient with suspected vasculitis underwent postcontrast abdominopelvic MRI with sequential (A) conventional Cartesian
volume interpolated breath-hold examination (VIBE) and (B) radial

GRE. Radial GRE received higher scores for all parameters of image
quality from both readers than conventional Cartesian VIBE

significance level using SAS 9.3 (SAS Institute, Cary, NC,


USA).

reference standard for lesion presence or absence. This radiologist was blinded to the evaluation performed by the two
readers who assessed lesion presence or absence and lesion
image quality.
In total, 31 patients with 31 lesions greater than 0.5 cm
were identified on the reference standard: 10 renal lesions, 6
hepatic lesions, 4 patients with Crohns disease and/or complications of Crohns disease, 3 patients with retroperitoneal
mass/lymphadenopathy, 2 adrenal masses, 2 patients with
peritoneal metastatic lesions, 1 spinal mass, 1 patient with
neurofibroma, 1 patient with pericoeliac soft tissue due to
vasculitis and 1 splenic mass. Reader 1 (with 6 years MRI
experience) identified all of the 31 lesions with radial GRE
(100 % sensitivity) and 28 lesions with Cartesian VIBE
(90.3 % sensitivity). Hence, three lesions were only identified
with radial GRE but had been missed on Cartesian VIBE
(Fig. 3). Reader 2 (with 3 years MRI experience) identified
29 lesions with radial GRE (93.5 % sensitivity) and 23 lesions
with Cartesian VIBE (74.2 % sensitivity). Hence, six lesions
were diagnosed only with radial GRE but had been missed on
the conventional Cartesian VIBE by reader 2. This increased
sensitivity for lesion detection on radial GRE by reader 2 was
statistically significant (P =0.03). There was greater lesion
conspicuity (4.70.6 vs. 3.70.9; P <0.001) and lesion edge
sharpness (4.40.7 vs. 3.30.7; P <0.001) with radial GRE

Results
All 73 patients underwent radial GRE and conventional Cartesian VIBE acquisitions. Thus, a total of 146 data sets were
evaluated by each reader independently.
Image qualitative evaluation
With data provided by the two readers, scores for overall image
quality (4.30.6 vs. 3.00.8), hepatic edge sharpness (4.40.6
vs. 3.00.9), hepatic vessel clarity (4.20.8 vs. 2.90.9) and
respiratory motion robustness (5.00.2 vs. 3.51.0) were significantly higher (all P <0.001) for radial GRE than for conventional Cartesian VIBE. Image quality scores for radial GRE
were significantly higher than for Cartesian VIBE irrespective
of the reader providing the data (Table 2, Figs. 1 and 2).
Lesion evaluation
Review of the entire data set (all sequences) by a third radiologist with 6 years abdominal MRI experience served as a

Fig. 3 A 5-year-old female patient with a suspected liver lesion


underwent post-contrast abdominopelvic MRI with sequential (A) conventional VIBE and (B) radial GRE in the portal venous phase of
enhancement. The liver lesion was not identified by either reader with

conventional VIBE but was detected with radial GRE by both readers
(arrow). On review of the entire data set, this lesion was suspected to be
an atypical focal nodular hyperplasia (FNH)

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Eur Radiol (2014) 24:320326

Fig. 4 A 9-year-old male patient


with tuberous sclerosis underwent
post-contrast abdominopelvic
MRI with sequential (A)
conventional Cartesian VIBE and
(B) radial GRE. Left renal cysts
were more conspicuous with
radial GRE than with the
conventional Cartesian VIBE

(Figs. 4 and 5) than with conventional Cartesian VIBE when


using data from both readers.

Discussion
Our results show that paediatric abdominopelvic T1-weighted
3D examination is feasible with radial k-space sampling during free breathing, with overall image quality that is significantly better than that of the conventional Cartesian acquisition. All parameters of image quality, including hepatic vessel
clarity and hepatic edge sharpness, were scored higher by both
readers for the radial acquisition scheme than for the conventional Cartesian acquisition. Furthermore, spatial resolution
was greater with the radial acquisition scheme than with
Cartesian acquisition owing to the need to acquire Cartesian
data within a breath-hold. Lesion conspicuity and lesion edge
sharpness were rated higher with the radial sampling scheme
than with the Cartesian VIBE. Reader 1 and reader 2 missed
three and six lesions respectively on conventional VIBE that
were identified on the radial GRE.
Degradation of image quality by patient motion is an
important reason for the under-utilisation of paediatric
abdominopelvic MRI in clinical practice, despite its excellent
contrast resolution and lack of ionising radiation. In young
children, breath-holding may be impractical or impossible.
Moreover, while deep sedation or general anaesthesia can help
Fig. 5 A 2-year-old patient with
hepatoblastoma underwent postcontrast abdominopelvic MRI
with sequential (A) conventional
Cartesian VIBE and (B) radial
GRE. A left hepatic lobe
hepatoblastoma lesion had higher
conspicuity and edge sharpness
with radial GRE than Cartesian
VIBE

to control gross body motion artefacts, it cannot control respiratory motion artefacts. To decrease motion-related artefacts,
techniques such as the PROPELLER method, which acquires
k-space data in blades using a radial-type readout scheme,
have been proposed. These PROPELLER techniques have
demonstrated substantial reduction in respiratory motionrelated artefacts and improved image quality for twodimensional (2D) T2-weighted turbo-spin-echo (TSE) as well
as diffusion-weighted imaging (DWI) of the liver [1821]. A
radial acquisition scheme has recently been employed for
performing free-breathing T1-weighted imaging in the abdomen [17, 22]. A recent study by Azevedo et al. suggested that
although free-breathing radial VIBE had lower image quality
scores than conventional VIBE in adults who could breathhold, the technique may be helpful in uncooperative patients
like children who cannot adequately suspend respiration on
command [16].
Decreased sensitivity to motion is the clear advantage of
radial k-space sampling. With conventional Cartesian k-space
sampling, object motion translates into dominant motion artefacts (ghosting) along the phase-encoding direction as well as
overall image blurring. Such a vulnerable phase-encoding axis
does not exist in the radial geometry, and motion artefacts
present as streaks with the stack-of-stars scheme where radial
sampling is performed in plane. Structures that experience
motion can also appear slightly blurry with the radial acquisition scheme. These streak artefacts are easy to identify because

Eur Radiol (2014) 24:320326

of their characteristic aligned appearance. In our study the


occurrence of streak artefacts did not significantly decrease
the image quality or conspicuity of lesions. Thus images
remained of diagnostic quality and received high overall image
quality scores from both readers.
One limitation of radial GRE is the relatively long acquisition time of 90 to 120 s in our study. Acquisition time of
radial GRE was longer than the Cartesian acquisition, which
we routinely perform for multi-phase imaging. Although we
did not match the acquisition times of the Cartesian and radial
sequences, we have previously shown that the image quality
of free-breathing Cartesian post-contrast imaging with multiple averages is significantly lower than the free-breathing
radial GRE despite matched acquisition time [17]. This long
acquisition of radial GRE restricts its utility in dynamic imaging, which requires multi-phase acquisition (arterial, portal
venous and equilibrium phases) with temporal resolution of
about 10 to 20 s. Thus, although portal and equilibrium phase
examinations can easily be replaced with radial GRE acquisitions, arterial phase acquisition will still need to be performed
using a conventional Cartesian approach with a shorter acquisition time. However, note that recent advances in reconstruction techniques including compressed-sensing [23, 24] may
make it feasible to generate images with higher temporal
resolution from continuous radial acquisitions [25]. This will
enable the acquisition of multi-phase data, including during
the arterial and venous phases, with radial acquisition schemes
in the future.
Another disadvantage of radial GRE acquisition is that the
radial sampling scheme is more vulnerable to off-resonance
effects. Because radial GRE uses different readout directions
to perform k-space sampling, strongly off-resonant signals
like fat cause signal blurring instead of a unidirectional chemical shift, as seen with conventional Cartesian acquisition.
Therefore, it is essential to perform radial GRE acquisitions
with spectral fat saturation. Incomplete or poor fat saturation
may result in streak artefacts, degrading image quality. These
artefacts, although mild, were seen in some cases because of
residual fat signal around areas of strong inhomogeneity away
from the isocentre. These artefacts did not significantly degrade image quality as evident by high overall image quality
scores by both readers. This limitation may be overcome with
the development of a Dixon-based fat/water separation technique for radial sampling.
The limitations of our study also include the relatively small
number of patients, especially those with lesions. Nevertheless,
our data suggest that radial GRE might have higher image
quality and resolution than conventional VIBE, and this may
explain its higher sensitivity for abdominopelvic lesion detection compared with the conventional sampling scheme. The
clinical significance of this observation needs to be evaluated in
a larger prospective study. Some groups have also advocated a
2D fast low-angle shot GRE or turbo FLASH sequence for non-

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breath-hold imaging. We chose not to incorporate this sequence


in our study because of its substantially lower spatial resolution,
inability to perform good quality multi-planar reformation and
the inability to perform high-quality fat suppression with this
sequence.
In conclusion, many paediatric patients cannot adequately
suspend respiration, decreasing the image quality of the conventional contrast-enhanced T1-weighted examination. Here,
we have shown improved image quality and higher lesion
conspicuity with free-breathing radial GRE acquisition in paediatric patients undergoing contrast-enhanced abdominopelvic
MRI, albeit at the cost of longer but clinically acceptable
acquisition times.
Acknowledgments Research support in the form of hardware and
software from Siemens Healthcare.

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