Synchronisation strategies in T2-weighted MR imaging for detection of liver lesions: Application on a nude mouse model
1 CREATIS-LRMN, CNRS UMR 5220, Inserm U630,
INSA-Lyon, Universit� de Lyon, Universit� Lyon 1, Villeurbanne, France.
2 Hospices Civils de Lyon, D�partement
d�Imagerie Digestive, CHU Edouard Herriot, Lyon, France.
3 Inserm U865, Facult� de m�decine RTH Laennec, Lyon, France.
Aim: The objective of this work was to propose
original synchronisation strategies based on T2-weighted sequence performed on
a small animal MRI spectrometer in order to improve the image contrast and
detect mouse liver lesions at high magnetic field.
Materials and Methods: The experiments were
performed in vivo at 7T using a 32 mm inner diameter cylindrical volumetric coil for both RF emission and reception. A sensitive pressure sensor was used
to detect external movements due to both respiration and heart beats. The
pressure sensor was interfaced with a commercial ECG Trigger Unit to use
dedicated functionalities (trigger levels, delays and window). To enable
T2-weighted imaging with minimised T1 effects, an acquisition strategy with
controlled TR spanning over several respiratory cycles was developed. With this
strategy, the slices were acquired over several respiratory periods.
Results: The acquisition, performed over several
respiratory periods, enables a longer TR than the typical mouse respiratory
period. The image contrast is controllable and independent of the respiratory
period. The heavily T2-weighted images obtained with the developed strategy
allow better visualisation of lesions at high magnetic field. Moreover, double
respiratory and cardiac synchronisation, based on a unique sensitive pressure
sensor, improves image quality with less motion artifacts, especially in the
ventral liver region. The total slice number is independent of respiratory
period and thin slices can be acquired to cover the whole liver.
Conclusion: The developed strategy enables high
quality pure T2-weighted imaging with minimal motion artifacts. This strategy
improves T2-weighted image contrast and quality, especially at high magnetic
field, on animals with short respiratory periods. The strategy was demonstrated
using a mouse model of liver lesions at 7T. This protocol could be used to
carry out a longitudinal follow-up. � 2007 Biomedical Imaging and
Intervention Journal. All rights reserved.
Keywords: mice liver, high-field MRI, synchronisation, motion
artifacts, T2-weighted contrast image
Magnetic resonance imaging is an established imaging
method for the evaluation of liver diseases. In clinical practice, MR imaging
examination of the liver uses a combination of breath-hold T1-weighted gradient
images and T2-weighted images, including gadolinium enhancement with
acquisition of multiple phases. In order to avoid blurring and ghost artifacts
due to respiratory motions, several techniques for T2-weighted imaging have
been proposed . Breath-hold T2-weighted imaging is feasible with a long echo train to reduce breath-hold times. This technique is associated with a short inter-echo spacing to minimise artifacts due to T2-dependent signal decay occurring with a long echo train. The technique has been proven to be superior to a free-breathing conventional spin-echo (SE) sequences in the detection of hepatic tumours at 1.5 T [2, 3]. The benefits of breath-hold T2-weighted imaging include better lesion conspicuity and reduced blurring by an order of magnitude in image acquisition [2, 4]. An alternative to the breath-hold approach is the respiratory-triggered fat-suppressed (FS) fast SE imaging. This technique is more accurate than the free-breathing with SE sequence or breath-hold with fast SE sequences, with improved small lesion conspicuity [5, 6]. In small animal models, liver study on MR imaging requires specific adaptation including strong constraints in the conditioning of the animals and the spatial resolution . It is mandatory to control the anaesthesia and the temperature by measuring the physiological signals. Conventional SE T2-weighted sequence has the potential to provide high image contrast and spatial
resolution if motion artifacts are suppressed. Conventional procedure for small
animals consisted of synchronisation of T2-weighted imaging with the
respiratory cycle [8-11]. However, slices are acquired on each respiratory cycle, and the number of acquisition slices is limited by the short respiratory period Tresp (typically in the range of 0.5 s to 1.5 s), leading to insufficient liver coverage. Moreover, the image contrast is not freely controllable because TR is given by Tresp and is usually unsuitable for T2-weighted image contrast, especially at high magnetic field .
In this study, we performed a prospective qualitative
comparison between conventional acquisition T2-weighted imaging and three
increased evolutions of T2-weighted images to improve detection of liver
lesions and to determine which acquisition strategy is best for repeated
examinations during a longitudinal study.
Materials and Methods
Female athymic nu/nu CD-1 nude mice between 7 and 11 weeks
old, obtained from Charles River Laboratories (L'Arbresle, France), were used.
The animals were bred and maintained in a filtered environment. Cages, food and
bedding were sterilised in the autoclave. The experimental protocol was
approved by the Animal Care and Use Committees of the University Claude Bernard
Lyon 1. The intestinal STC-1 cell line, a gift from D. Hanahan through the
courtesy of A. Leiter (New England Medical Center, Boston, MA), was
derived from an endocrine tumour developed in the small intestine of a double
transgenic mouse obtained by crossing two lineages expressing the rat insulin
promoter linked, respectively, to the simian virus 40 large-T antigen and to
the polyomavirus small-t antigen . STC-1 cells were maintained in DMEM supplemented with 5% foetal calf serum (FCS), 2 mmol.L-1 glutamine and antibiotics (100 UI.mL-1 penicillin plus 50 mmol.L-1 streptomycin). Animals were anaesthetised with pentobarbital prior to all surgical procedures. A 50 �l solution, containing STC-1 cells adjusted to a final concentration of 5.107 cells.mL-1, was injected into the spleen of adult female mice after abdominal sterilisation with iodine and alcohol swabs .
The anaesthesia protocol was conducted with an approved
system (Minerve, Esternay, France). First, mice were placed in an anaesthesia
induction box with 2 - 2.5 % isoflurane gas (Laboratoire
Belamont, Boulogne Billancourt, France) administered at 1 L/min rate. Then
the animals were placed in a supine position on a dedicated plastic bed . To maintain the anaesthesia during the acquisition, the mouse�s nose was introduced into a face cone mask delivering anaesthetic gases (1 - 2 % isoflurane with a mixture of 70% oxygen and 30% air at 0.6 to 1 L/min).
Pressure sensor and triggering device
The cardiac and respiratory movements were detected using
a home-made air pillow placed next to the thorax and upper abdomen. The air pillow was connected with a plastic tube to a
sensitive pressure sensor (reference DCXL01DN, Honeywell, Freeport, IL, USA) and detected movement due to respiration and heart beats. The pressure range of
this ultra low pressure sensor was within 1 inch height of H2O. Pressure sensor was interfaced (connection and power supply)
with an ECG Trigger Unit HSB-T (Rapid Biomedical, W�rzburg, Germany), in order to use the adapted functionalities of this trigger unit (amplification,
filtering, trigger level, trigger delay and trigger window). Because the
trigger unit used had no screen display, signals were displayed using a digital
oscilloscope (Tektronix TDS 2014, Beaverton, OR, USA).
To generate multiple trigger pulses to the MR console
using a single output trigger pulse from the ECG Trigger Unit, or to control
the minimum delay between two trigger pulses, we used a waveform generator
33220A (Agilent Technologies, Palo Alto, CA, USA). A burst of one or more
square pulses was generated with adapted number of cycles, depending on the
respiratory period. The connection scheme between devices is shown in Figure 1.
The experiments were performed in vivo at 7 T
on a Biospec system (Bruker, Ettlingen, Germany) equipped with a shielded
gradient system (400 mT/m gradient strength and 120 mm diameter). For
both RF emission and reception, a cylindrical volumetric coil with 32 mm
internal diameter (Rapid Biomedical, W�rzburg, Germany) was used. A FS multiple
SE sequence with three echoes (TE=20, 40, 60 ms) was used with the
following parameters: 30 x 30 mm2 FOV, 256 x 256
matrix, 0.5 mm slice thickness and 17 kHz receiver bandwidth. Images
were acquired in the axial plane, using two axial saturation bands placed on
both sides of the acquisition box to reduce flow artifacts. The minimum delay between
two consecutive slices with these sequence parameters was 90 ms. The delay
between two consecutive slices was defined as the inter-slice time (Tis).
Method I: Conventional triggering strategy
The conventional triggering procedure consists of
synchronising all slices, starting from one single trigger pulse. The trigger
time point is adjusted manually for each mouse by setting the trigger level and
delay on respiration signal to occur between the end of the expiration and the
beginning of inspiration. Using this basic technique, all slices should be
acquired within the expiration period from one cycle. TR is determined by the
respiratory period with TR = Tresp. For every trigger
pulse, a single line of k-space is acquired for all slices . The trigger signal and the acquisition period over the respiratory waveforms are shown in Figure 2a.
Method ІІ: Uncoupling TR from Tresp
To perform heavily T2-weighted contrast images with
minimal T1 effects, TR has to be increased to be longer than the respiratory
period. This was carried out by decoupling the respiratory period Tresp
from the repetition time TR by introducing a minimum delay between two trigger
pulses (Figure b). As in the previous method, all the slices are acquired
within one respiratory cycle but not withevery single cycle. With a minimum
delay between two trigger pulses of 3 s, signal acquisition is performed
every two to six respiratory cycles depending on mouse Tresp value.
Method ІІІ: Balanced acquisitions over several
Similar TR imposed with previous evolution can be obtained
by spanning multiple slice acquisitions over several respiratory cycles (Nresp).
While TR = Nresp x Tresp, the
effective TR is almost independent of Tresp and relatively constant
between animals by choosing an adapted number of respiratory cycles. For this
method, an independent trigger pulse is generated for every single slice and
all the slices are acquired within several respiratory cycles corresponding to
desired repetition time TR.
At the end of every expiration cycle, a burst of trigger
pulses is generated using the waveform generator. The burst of trigger pulses
consists of a series of square pulses with 105 ms delay between each pulse
sent to the MRI console. The �low� level of the square pulses is in the range
of zero to 0.8 volts, and the �high� level is in the range of 2 to 5 volts
according to TTL (transistor-transistor logic) requirements for trigger console
input. The delay between two pulses was set slightly longer than the minimum
delay needed to acquire one slice (90 ms). The number of square pulses
generated within one burst was chosen based on the respiratory period in order
to fully use the expiration period. For each trigger pulse, a unique slice with
a single k-space line was acquired. Figure 2c is a schematic diagram showing
the principle of this triggering and acquisition strategy over the respiratory
waveforms. For instance, in a sequence with 9 slices, the slices can be divided
into 3 groups. Each slice group is acquired within one respiratory cycle:
the slices ordered (interleave case) and numbered as 1, 3, 5 are acquired in
the first cycle, the slices numbered 7, 9, 2 in the second cycle and the slices numbered 4, 6, 8 in the third cycle. For a mouse with a respiratory period of 1.5 s,
36 slices can be successfully acquired by exciting 12 slices (with a burst
of 12 trigger pulses) per respiratory cycle, which means that 3 respiratory
cycles are needed to cover the entire liver, leading to an effective TR of 4.5 s.
This synchronisation and acquisition scheme allows an increasing total number
of slices, by increasing the effective TR, depending on what is required. Thus
in our specific case, 36 slices were acquired to cover the whole mouse liver
with thin slices of 0.5 mm thickness.
Method ІV: Dual cardiac-respiratory triggering with balanced
Due to the close proximity of the heart, heartbeats can
generate motion artifacts in the upper part of the liver. To avoid liver
contamination by heart motion artifacts, a dual cardiac-respiratory triggering
was used. In this strategy, the variability of the respiratory rate was
determined prior to MR acquisition and the scanning period was chosen to be
shorter than the shortest respiratory period. Thus, a safe number of cardiac cycles that were likely to occur for
all respiratory cycles during MR acquisition was used. The synchronisation
and acquisition scheme is shown in Figure 2d. An example of real signals and setup
(trigger level, acquisition window) for dual cardiac-respiratory triggering is
shown in Figure 3.
Qualitative and quantitative evaluation
Image quality obtained with the four different triggering
methods was assessed, taking into account the presence of artifacts and overall
image quality as well as the contrast between smaller hepatic lesions and liver
tissue. Additionally, the signal-to-noise ratio (SNR) was measured in hepatic
parenchyma and in large (> 1 mm in diameter) lesions. The
contrast-to-noise ratio (CNR) between lesions and parenchyma was also
calculated. Both parameters were assessed and corrected to the square root of
the total scan time for comparisons between the conventional triggering
technique and the dual cardiac-respiratory triggering with balanced
The analysis of the nude mice hepatic lesion images
obtained from the various synchronisation schemes enabled us to qualitatively
characterise each proposed strategy. Efficient respiratory synchronisation is
mandatory to obtain reasonable image quality that allows the detection of small
lesions. An illustration of image degradation due to motion artifacts with and
without synchronisation on respiratory motion is shown in Figure 4. Representative
images of the inferior epigastric area, acquired with three out of four
investigated strategies, are shown in Figure 5 on normal specimen. On
T2-weighted images, the gall bladder appears in hyperintensity signal. In the
presence of motion, this high intensity signal will propagate along the phase
encoding direction. Without respiratory triggering, the motion artifacts are
present (Figure 5a). In the conventional respiratory strategy with a long
controlled effective TR, a good T2-weighted contrast image is achieved, but
with motion artifacts at the gall bladder due to cardiac movements (Figure
5b). All the slices (limited to about 12 slices) are acquired within one
respiratory cycle but not with every single respiratory cycle. This strategy is
clearly not efficient since scanning is performed only during the expiration
delay of one cycle over three. Using the respiratory triggering strategy with
balanced acquisitions over several respiratory periods, the artifacts and the
image contrast are equivalent to the previous strategy but it has the advantage
that the number of acquirable slices increases three fold (up to 36 slices).
The additional cardiac synchronisation significantly reduces the remaining
motion artifacts at the cost of an increase in scan time.
For the detection and the characterisation of liver
lesions, multi-echo imaging with dual cardiac and respiratory triggering is
very useful, especially in the ventral liver region where motion artifacts are
generated by the heartbeat (Figure 6).
With an average Tresp of 1.5 s and a variable
effective TR depending on Tis, the total acquisition time was in the
range of 20 to 38 min. The main parameters and characteristics of different
strategies evaluated in this work are summarised in Table 1.
The ratio of the SNR corrected for acquisition time using
the dual cardiac-respiratory triggering to balanced acquisitions with the
conventional triggering technique was constant with a mean value of 1.01 � 0.02.
However, CNR corrected for acquisition time using the dual cardiac-respiratory
triggering with balanced acquisitions increased by 41 � 11%, 12 � 2%,
and 15 � 4% for 20, 40 and 60 ms TE respectively, compared to
the conventional triggering technique.
An MRI protocol adapted to the study of liver tumours of
nude mice, including �strong� constraints on the conditioning of the animals,
was established. In a magnetic environment and with restricted space, we
administered anaesthesia, controlled the animal body temperature and measured
the cardiac and respiratory signals. Conventional triggering and different
synchronisation strategies not available in commercial high field small animal
MRI spectrometers were assessed.
The regular protocol consists of T2-weighted imaging
synchronised with the respiratory motion. In order to significantly reduce
motion artifacts, images within the late expiration period were acquired. This
conventional method has several limitations: limited number of slices (the
number of slices that can be acquired is restricted in between the trigger
pulse and the next inspiration event), significant cross-talking due to the
time reduction between two slices, and poor T2-weighted contrast. The limited
number of slices allowed to cover the liver volume can be circumvented with
larger slice thickness but this leads to partial volume effects. Finally, the
choice of the image contrast is limited by the fact that TR is controlled by Tresp.
Thus, image contrast is not freely controllable and TR is unsuitable for the
required T2-weighted image contrast [17-19] especially at high magnetic field (4.7 T and more) due to the longitudinal relaxation time T1 increase with magnetic field.
With the second method, suitable T2-weighted image
contrast was obtained by uncoupling TR and Tresp. Despite the
improved contrast, the slice number was still limited and not optimal in terms
of effectiveness, since scanning is performed only during the expiration delay
of one cycle over three (Figure 2b).
With the third method, the number of slices was increased
due to the fact that the slices were divided into a few groups. Thus the entire
liver was covered with thinner slices, resulting in reduced partial volume
effect. Another advantage of this slice repartition is the reduction of the
possible cross-talking due to the increased time separation between two
adjacent slices. Furthermore, the decoupling between Tresp and the
effective TR is preserved and thus the T2-weighted contrast is almost as freely
controllable as with the second method.
The dual cardiac-respiratory triggering strategy with
balanced acquisitions leads to equivalent T2-weighted image contrast and
quality far from the heart but significantly improves image quality and
detection of the hepatic lesions in the liver dome region at close proximity to
the heart. To our knowledge, no papers have reported improved T2-weighted
contrast images with dual respiratory and cardiac synchronisation performed on
a small animal MRI system at high magnetic field.
The various synchronisation techniques described in this
paper do not depend on the imaging sequence used and could be applied to other
sequences such as RARE (Rapid Acquisition Relaxation Enhancement) for
T2-weighted contrast imaging.
On most commercial synchronisation units, heart
synchronisation is usually performed based on Electrocardiogram (ECG)
signals [7, 20]. During a scan, RF pulses and gradient switching induce eddy currents disturbing the ECG signal . For small flip angles, the ECG signal can be easily filtered to recover a usable signal for triggering and to perform, for example, FLASH acquisitions in a CINE mode. ECG filtering is much more challenging using SE or RARE sequence with additional FS pulse or saturation bands. The pressure sensor used for respiratory and cardiac triggering was deported outside the RF coil, the gradient coil and the magnet bore. Pressure signal is uncorrupted by the eddy currents induced by RF pulses or gradient switching and thus it can be used with EPI sequence and large flip angles with good reproducibility for in vivo experiments.
At this time, the acquisition speed for dual
cardiac-respiratory triggering with balanced acquisitions is limited by Tis
that is given by the cardiac cycle period in the 200 ms range. In order to
increase acquisition speed without deteriorating image contrast and quality, we
are currently modifying a sequence in order to excite two slices within one
single heartbeat. The first slice located close to the heart will be then synchronised
with it and the second one located far from the heart will be selected about
100 ms after the first one. With this ultimate evolution, we anticipate an
image quality similar to full dual triggering with a drastic reduction of the
Finally, another way to increase acquisition speed would
be to use parallel imaging techniques, using array coil with multiple elements.
An original acquisition strategy for T2-weighted MR
imaging of small animals at high magnetic field was developed. The method
proposed allows acquisition of heavily T2-weighted liver images with
respiratory and cardiac synchronisation. Dual cardiac and respiratory
synchronization, using a unique sensitive pressure sensor, improved the image
quality and detection of hepatic lesions especially in the liver dome region.
The contrast was easily controllable due to the relative independence of the
effective TR with the respiratory period. Moreover, this strategy allowed an
important increase in the number of slices required for full liver coverage.
The protocol will be used to carry out a longitudinal follow-up of hepatic
lesions and to characterise the nude mouse model used before therapeutic
This work was supported by the Programme �Imagerie du Petit
Animal CNRS-CEA 2005�. The authors would like to thank Lee Shoo Ming for
the English language edition. The experiments were performed by authors on the
Figure 1 Schematic of connection for sensor and devices used for triggering. An air pillow was connected to a pressure sensor for both respiration and heart motion detection. The pressure sensor was interfaced with the ECG Trigger Unit HSB-T. This device ensures the amplification and filtering of input signal as well as the adjustment of the trigger level, trigger delay and trigger window. The trigger pulse generated by the ECG unit is used by the waveform generator to send a burst of trigger pulses to the MRI console.
Figure 2 Diagrams of different synchronisation and slice acquisition strategies used to obtain T2-weighted contrast images. The trigger pulses sent by the trigger unit to the MRI console as well as the excitation timing of each slice is indicated and illustrated for 9�slices: (a)�Conventional triggering strategy for T2-weighted contrast images. The repetition time is equal to the respiratory period with TR�=�Tresp. All slices are acquired within one respiratory cycle (non interleaved case); (b)�Heavier T2-weighted image contrast is obtained with minimum controlled TR imposed between two slice packages; (c)�New acquisition strategy with balanced slice acquisitions. A trigger pulse is generated for every single slice and acquisition of slices is spanned over several respiratory cycles; (d)�Dual cardiac and respiratory triggering with balanced acquisition over several respiratory cycles. The time between two consecutive slices is called inter-slice time (Tis).
Figure 3 Example of the setup for dual cardiac-respiratory triggering: (a)�Signal from the pressure sensor with acquisition window enabled between two respiratory cycles; (b)�Trigger pulses sent to MRI console based on cardiac cycle.
Figure 4 Images of mice liver obtained at D21: (a)�without any synchronisation with TR���1.5�s; (b)�with respiratory triggering and slice excitation spanned over three respiratory cycles (TR���3�נTresp���4.5�s).
Figure 5 Images of mice liver (Tresp�=�1.5�s; 12 slices; slice thickness 1.5�mm) obtained on normal specimen: (a) without synchronisation (TR�=�1.5�s; TA�=�5�min�20�s); (b)�with conventional respiratory strategy and a long controlled TR (TR���3�s; Tis�=�90�ms; TA�=�9�min); (c) with respiratory triggering strategy with balanced acquisitions over several respiratory periods (TR���3�נTresp�=�4.5�s; Tis�=�105�ms; TA�=�9�min); (d) with dual cardiac and respiratory triggering with balanced slice acquisitions (TR�=�4.5�s; Tis���200�ms; TA�=�17�min).
Figure 6 Multi-echo images (Tresp���2�s; 36 slices; 0.5�mm slice thickness) and slice excitation spanned over several respiratory cycles obtained at D21: (a, c, e) with respiratory triggering (TR���3�נTresp; Tis�=�105�ms; TA�=�21�min) for TE�=�20, 40, 60�ms; (b, d, f) with cardiac and respiratory triggering (TR���6�נTresp; Tis�=�155�ms; TA�=�35�min) for TE�=�20, 40, 60�ms.
Table 1 Summary of different synchronisation strategies with associated parameters of interest given for an average respiratory period Tresp���1.5�s
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|Received 31 August 2007; received in revised form 23
December 2007, accepted 25 December 2007
Correspondence: Creatis-LRMN, CNRS UMR 5220, Inserm U630, Universit� Lyon 1, b�t. 308., 43 Boulevard du 11 Novembre 1918, 69616 Villeurbanne, France. Tel.: +33 (0) 472431597; Fax: +33 (0) 472448199; E-mail: firstname.lastname@example.org (Olivier Beuf).
Please cite as: Baboi L, Milot L, Lartizien C, Roche C, Scoazec J-Y, Pilleul F, Beuf O,
Synchronisation strategies in T2-weighted MR imaging for detection of liver lesions: Application on a nude mouse model, Biomed Imaging Interv J 2007; 3(4):e53
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