Received: 27 April 2023 Revised: 18 August 2023 Accepted: 19 August 2023
DOI: 10.1002/mrm.29859
RESEARCH ARTICLE
Rapid MR elastography of the liver for subsecond
stiffness sampling
Matthias Anders1Tom Meyer1Carsten Warmuth1Josef Pfeuffer2
Heiko Tzschaetzsch1Helge Herthum3Mehrgan Shahryari1
Katja Degenhardt4Oliver Wieben5,6 Sebastian Schmitter4
Jeanette Schulz-Menger7,8,9,10 Tobias Schaeffter4,11 Juergen Braun12
Ingolf Sack1
Correspondence
Ingolf Sack, Department of Radiology,
Charité–Universitätsmedizin Berlin,
Corporate Member of Freie Universität
Berlin and Humboldt-Universität zu
Berlin, Charitéplatz 1, 10117 Berlin,
Germany.
Email: [email protected]
Funding information
BIOQIC, Grant/Award Numbers:
CRC1340, RTG2260; German research
foundation (DFG)
Abstract
Purpose:Depictingthestiffnessofbiologicalsofttissues,MRelastography(MRE)
has a wide range of diagnostic applications. The purpose of this study was to
improvethetemporalresolutionof2DhepaticMREinordertoprovidemorerapid
feedback on the quality of the wavefield and ensure better temporal sampling of
respiration-induced stiffness changes.
Methods: We developed a rapid MRE sequence that uses 2D segmented
gradient-echo spiral readout to encode 40Hz harmonic vibrations and generate
stiffness maps within 625ms. We demonstrate the use of thistechnique as a rapid
test for shear wave amplitudes and overall MRE image quality and as a method
formonitoringrespiration-inducedstiffnesschangesin theliverin comparisonto
3D MRE and ultrasound-based time-harmonic elastography.
Results: Subsecond MRE allowed monitoring of increasing shear wave ampli-
tudes in the liver with increasing levels of external stimulation within a single
breath-hold. Furthermore, the technique detected respiration-induced changes
in liver stiffness with peak values (1.83±0.22m/s) at end-inspiration, fol-
lowed by softer values during forced abdominal pressure (1.60±0.22m/s) and
end-expiration (1.49±0.22m/s). The effects of inspiration and expiration were
confirmed by time-harmonic elastography.
Conclusion: Our results suggest that subsecond MRE of the liver is useful for
checkingMRE driversettingsand monitoringbreathing-induced changesin liver
stiffness in near real time.
KEYWORDS
breathing, hepatic perfusion, liver, MRE scout, rapid MR elastography, stiffness
For affiliations refer to page 321
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© 2023 The Authors. Magnetic Resonance in Medicine published by Wiley Periodicals LLC on behalf of International Society for Magnetic Resonance in Medicine.
312 wileyonlinelibrary.com/journal/mrm Magn Reson Med. 2024;91:312–324.
ANDERS et al. 313
1INTRODUCTION
MR elastography (MRE) is a versatile technique that uses
changes in tissue stiffness to detect pathologies.1Most
abdominal applications of MRE focus on the liver because
changes in liver tissue can silently progress to a fibrotic
state, which is associated with a variety of clinical compli-
cations,butarerelativelyeasytodetectbyincreasedtissue
stiffness.2,3
MRE involves the mechanical generation of
shear waves, which are encoded by motion-sensitive
phase-contrast MRI sequences.4Shear wave excitation
requires external hardware and crucially relies on correct
driversettingsandconnectionstoacousticenergysources.
Direct feedback to the operator is crucial to rule out fail-
ure. Furthermore, measured liver stiffness varies during
the respiratory cycle5,6 and with blood perfusion.7,8 For
example,itisrecommendedtoperformMREinexpiration
and in a controlled state of fasting,9–11 and to ask patients
to abstain from fluid intake before the examination.12,13
Today, MRE is considered the most precise method for
measuring liver stiffness, outperforming ultrasound elas-
tography.14 However, unlike elastography by ultrasound,
MRE allows only little interaction between the operator
and the patient, resulting in limited feedback regarding
compliancewithbreathinginstructionsortechnicalissues
such as suboptimal wave excitation.10,15
Consequently, we identified two major limitations of
current abdominal MRE that can potentially be addressed
by a rapid MRE technique capable of sampling stiffness
maps in the subsecond range: (i) Scout MRE scans for
patient-specific adjustment of driver positions and excita-
tion amplitudes prior to more time-consuming MRE pro-
tocolsinvolvingbreath-holds.UsingMREscouts,theoper-
ator could easily check shear wave amplitudes—the criti-
calcontrastmechanism inMRE—withina regionof inter-
est(ROI).(ii)Studiesoftheeffectofbreathingonliverstiff-
ness,16 includingassessmentofliverphysiologyandhemo-
dynamics based on stiffness changes, would be greatly
facilitated without the need for resynchronizing MRE
acquisition to physiological maneuvers. Published studies
found liver stiffness measured by rapid ultrasound elas-
tography to be sensitive to the increase in intra-abdominal
pressure induced by forced breathing during the Valsalva
maneuver.7,8,17 Previous MRE studies reported significant
differences in liver stiffness between inspiration and expi-
rationwithhighervaluesduringinspiration18 andincreas-
ing differences in patients with fibrosis,19 motivating the
development and use of subsecond MRE for measuring
stiffness during free-breathing stiffness measurement.
Here we introduce subsecond rapid MRE of the liver
tonavigateMRE driver settingsand monitor physiological
stiffness variations from breathing in near real time.
Single-breath-hold MRE of the liver using simultaneous
multislice acquisition20 has been proposed for 3D MRE,
allowing acquisition within 14 to 17s when combined
with fractional encoding21 and the use of gradient-echo
(GRE) sequences.22 Real-time MRE has been developed
using 2D single-shot GRE MRE and stroboscopic wave
sampling.23,24 Instroboscopicwaveencoding,a slight mis-
match between the TR of the pulse sequence and the
oscillationperiod ensurescontinuousaccumulationof the
wave phase, resulting in stiffness mapping at high frame
rates on the order of 5 to 6Hz. However, larger FOV and
shorterT∗
2signaldecaytimesrequiremultishot,segmented
acquisitions,precludingstroboscopicsamplingintheliver.
Therefore, we present a novel MRE concept that sacrifices
some of the high temporal resolution of real-time MRE in
favor of segmented k-space acquisition for coverage of a
largebodyregion,includingtheliverandadjacentabdom-
inal organs, in arbitrary views in less than a second. We
hypothesize that subsecond liver MRE is feasible when
performedemployingsegmented2Dwavefieldacquisition
with only a few k-space segments and a small number of
time steps over a wave period, synchronization of TR to
continuous oscillations, and postprocessing that is opti-
mized to reduced wavefield information.
The proposed rapid MRE sequence may offer a useful
compromise that, while lacking the volumetric coverage
of full 3D MRE, combines the precision of MRE with the
rapid feedback on liver stiffness available in ultrasound
elastography.To verifyour hypothesis,wecompareresults
of our novel MRE sequence with state-of-the-art 3D MRE
and ultrasound-based time-harmonic elastography (THE)
of the liver.
2METHODS
Elevenvolunteers(8men;meanage,36±9years)without
symptoms or a history of liver disease were examined by
MREafterwritteninformedconsentwasobtained.Allpar-
ticipants additionally underwent THE on a different day
to further investigate breathing-induced stiffness changes
observed in MRE.
Allsubjectswereexaminedina3TMRIscanner(Mag-
netom Lumina, Siemens Healthineers, Germany) with a
12-channel receiver coil. The abdomen was exposed to
vibrationsatafrequencyof40Hzusingfourcustom-made
compressed-air drivers attached to the upper trunk with
Velcro strips, two on the chest and two on the back. The
vibrations were generated with solenoid valves that con-
trolled the airflow by switching them on and off at the
desiredexcitationfrequency.Toavoidanylatencybetween
mechanical stimulation and the time of motion-encoding,
the clocks of the vibration generator and the MRI scanner
314 ANDERS et al.
were synchronized. The resulting modulations in the air-
flow were then translated into mechanical deflections by
the plastic actuators.25
2.1 Sequences
Figure 1presents the timing diagram of the rapid MRE
sequence developed in this study. The sequence had a
multishot GRE spiral design sensitized to motion by bipo-
lar motion-encoding gradients (MEGs) with nulled first
moments. Each wave image was obtained by interleaving
three spiral k-space segments. The spiral trajectory was
based on a dual-density design with full sampling in the
k-space center and twofold undersampling in the outer
area.26 The repetition time was set to 50ms, which corre-
sponds to two vibration periods, in order to avoid phase
incoherences between the vibration and imaging gradi-
ents in different k-space segments. The following imaging
parameters were used: FOV=360×360mm2; voxel size =
2.5×2.5×5.0mm3; single slice; TR=50ms; TE=14ms;
6/3(designed/played-out)spiralinterleaves;parallelimag-
ing factor of 2 (using iterative self-consistent parallel
imaging reconstruction27 and deblurring based on B0
field maps28); MEG duration=12.48ms (nearest possible
approximation of 12.5ms), yielding 28.7μm/rad encod-
ing efficiency; MEG amplitude=34mT/m in thru-plane
direction because this component is typically encoded in
MRE of the liver.29 A single stiffness map was gener-
ated from four wave images acquired at evenly spaced
intervals over a vibration period of 25ms. For this, after
acquisition of a full image, the subsequent acquisition
was shifted by 25ms/4=6.25ms relative to the vibra-
tion waveform, resulting in a total acquisition time of
625ms for a full elastogram ([3k-space segmentsx50ms
TR+6.25ms wave-phase shift]x4 instances over a vibra-
tion cycle). Other possible parameter combinations are
discussed below.
For comparison, 3D MRE was performed using a
Cartesian,single-shot,spin-echo,EPIMRE(SE-EPI-MRE)
sequence comprising an asymmetric MEG prior to the
refocusing pulse as described in Ref. 30 Image acquisition
was performed within a breath-hold using the following
parameters: FOV=360×260mm2; 11 slices each of 5mm
thickness; phase partial Fourier=7/8; 2.5×2.5×5.0mm3
voxel size; 11 slices; TR=855ms; TE=40ms; parallel
imaging factor of 2 (GRAPPA); MEG duration=12.88ms
(nearest possible approximation of 12.5ms); MEG ampli-
tude=34mT/m; consecutively deployed along all three
Cartesian axes, eight instances over a vibration cycle,
resulting in a total acquisition time of approximately 21s
for a full 3D elastogram.
2.2 Acquisition protocols
Two MRE experiments were performed in each partic-
ipant in a single session. First, rapid MRE was per-
formed to check at which air-pressure sufficient wave
amplitudes were induced in the liver. Therefore, trans-
verse wave images were acquired to consecutively gener-
ate six stiffness maps at different amplitude levels. The
input air pressure to the actuators was automatically
increased from 0mbar to 1000mbar in 200mbar incre-
ments with 2s forerun time to reach a mechanical steady
state. Overall, this scout experiment took a total scan time
of 6x(2+0.625)=15.75s, during which each participant
was asked to hold their breath in end-expiration, which
is the recommended breathing state in liver MRE.10 For
comparison with established 3D MRE, the SE-EPI-MRE
sequence was applied in the same transverse orientation
as the rapid MRE 2D-slice. SE-EPI-MRE acquisition was
performedduringbothend-expiratoryandend-inspiratory
breath-holds without moving the position of the 3D slice
block to test possible effects of different breath-hold states
on liver stiffness. Because the position of the liver varied
significantly between the two breath-hold positions, we
selected different slices from the 3D blocks that matched
the anatomy of the liver depicted by the 2D rapid MRE
sequence. In a second experiment, we used the optimized
pressure settings from the first experiment and studied
the respiration-induced shift in liver position along the
feet–head direction using a coronal view. Here, a series
of 100 MRE maps were acquired continuously over 62.5s
to capture the dynamic changes in liver stiffness induced
by different breathing patterns and maneuvers. The coro-
nal view allowed us to correct for feet–head motion of the
liver using image registration for improved comparison.
Each participant performed a sequence of five different
breathing maneuvers following the instructions given by
the operator via the MRI communication system. The
sequenceofbreathingmaneuversisillustratedinFigure1.
First, the participants were asked to exhale and maintain
the state of end-expiratory breath-hold for 10s, followed
by fast inhalation and an end-inspiration breath-hold for
another 10s. The acquisition was then continued without
breathing but increased abdominal pressure through the
Valsalva maneuver for 15s, followed by a short phase of
expiration for 5s and free breathing during the remain-
ing 22.5s. Prior to the experiments, the participants were
trained in this respiratory protocol, including the Valsalva
maneuver, by ventilating against a manometer to ensure
that an abdominal pressure corresponding to approxi-
mately 50mbar expiration pressure was maintained dur-
ing the scan.
ANDERS et al. 315
FIGURE 1 Rapid MRE sequence and timing relative to external vibration of 40Hz and respiration. Each elastogram was generated
from wave data encoded at four different time points over a vibration period (T1–T4) using a segmented spiral gradient-echo sequence with
three interleaved spiral readouts as demarcated by green, yellow, and red circles (S1–S3). After acquisition of these three k-space segments,
each of which had a TR of 50ms corresponding to two vibration cycles, the start of the subsequent image acquisition was shifted by
𝜏=6.25ms, indicated by the displacement of the gray points toward the green points. Consequently, after four images, a full vibration cycle
was encoded, resulting in a total acquisition time of 625ms for a full elastogram. In a second experiment with time-resolved rapid MRE
sequence, 100 elastograms were continuously acquired over 62.5s in order to capture breathing-induced changes in stiffness. The breathing
paradigm consisted of five consecutive maneuvers of expiration breath-hold (10s), inspiration breath-hold (10s), Valsalva maneuver (15s),
expiration breath-hold (5s), and free breathing for the remaining acquisition. ADC, analog-to-digital converter; MRE, MR elastography.
2.3 Time-harmonic elastography
THEoftheliverwasperformed,asdescribedinRef.8,once
during an end-inspiratory breath-hold and once during
an end-expiratory breath-hold. In brief, the subjects were
positioned supine on a bed with an integrated vibration
generator. A multifrequency waveform of six frequencies
(27,33,39,44,50,56Hz)wasusedforcontinuousmechan-
ical excitation. Anatomy and motion were detected by a
commercial elastography system (GAMPT mbH, Merse-
burg, Germany) using a curved-array C5-H2 transducer at
2MHz. For acquisition, the transducer was positioned in
theleftintercostalspace toimage the right liver lobe. Data
were acquired at a depth of 120mm and an 80Hz frame
rateover1s.Stiffnessmapsweregeneratedusingthesame
algorithmasforMRE.31 Notethat,becausethelivermoves
out of the imaging during respiration, continuous acquisi-
tion of hepatic elastograms by THE is not possible.
316 ANDERS et al.
2.4 Data postprocessing
Stiffness maps in terms of shear wave speed (SWS, in m/s)
were reconstructed by wavenumber (k)-based multifre-
quencydualelasto-viscoinversionmethod,asproposedin
2016 by Tzschäetzsch et al.31 and recently made available
on a publicly accessible server by Meyer et al.32 Because
our novel MRE technique acquires less information than
standard multicomponent and multifrequency MRE, the
smoothing capacity of the pipeline was slightly increased
by using a third-order Butterworth high-pass filter with
a 94rad/m threshold instead of the conventional linear
high-pass filter.32 Furthermore, the directional filters with
Gaussian kernels (eight spatial directions) were replaced
by cosine-squared kernels (four directions). Motion cor-
rection was performed in all coronal images based on
spatial normalization33 to align the liver position in the
2D image slice with the ROI of the entire liver manu-
ally selected from the image acquired at the first time
point. This image was used as reference for registration
of the liver in serial coronal images. Therefore, in-plane
rigid body motion correction was applied to the complex
MRI data prior to MRE postprocessing as described in
Shahryari et al.6
2.5 Statistics
Mean values were obtained from manually selected ROIs
covering the full liver visible within the 2D slices.
Bonferroni-corrected paired Wilcoxon tests with a level of
significanceof0.05 wereusedforall comparisonsofgroup
mean SWS values. Wave amplitudes and SNRs were com-
puted from the magnitudes of complex-valued shear wave
fields and wavelet-based noise analysis of the displace-
ment fields, respectively.34 A one-way repeated measures
analysis of variance test with Bonferroni correction was
performed to investigate the effect of different pressure
levels on the SD of SWS and SNR. Optimal thresholds
for wave amplitude and displacement SNR to exclude too
noisy shear waves were derived by histogram analysis of
pixel values in the livers of all subjects.
3RESULTS
SWS maps in a transverse view of a representative vol-
unteer are shown in Figure 2A, demonstrating that
rapid MRE can be used to quickly assess whether
generated waves fully penetrate the liver before more
(A) (B)
(C)
FIGURE 2 Shear wave fields and shear wave speed maps in a transverse view through the abdomen acquired with the rapid MRE
sequence within 625ms. (A) Real part of the complex-valued shear wave field, amplitude of the shear wave field, and shear wave speed
shown in the left, middle, and right column, respectively, at different pressure levels of the actuators. White dashed lines demarcate the liver
region; green lines indicate the regions inside the liver which were automatically detected as being reliable for stiffness measurement based
on wave amplitude thresholds (>3.6μm). (B) Shear wave amplitudes and displacement SNR within the liver at increasing drive pressure from
0 to 1000mbar. (C) SD of shear wave speed within the liver at increasing drive pressure from 0 to 1000mbar.
ANDERS et al. 317
(A) (B)
FIGURE 3 SWS obtained by rapid MRE and SE-EPI-MRE. (A) Representative anatomical images (MRE magnitude signal) and SWS
maps obtained with the two sequences. Whereas SE-EPI-MRE covered a full volume in which similar slices were identified in end-expiration
and end-inspiration, the rapid MRE sequence captured only a single slice in end-expiration to avoid tissue displacement due to respiration.
Despite notable differences in image position and organ morphology due to respiration, both sequences provide similar detail resolution. (B)
Group statistical plots of mean SWS of liver tissue visible in the slices shown in (A). SE-EPI-MRE, spin-echo, echo-planar-imaging MRE;
SWS, shear wave speed.
time-consuming examinations are performed. Figure 2B
shows the increase in wave amplitudes in the liv-
ers of all subjects as the air pressure applied to the
actuators increased. Shear wave amplitudes increased
from 1.16±0.48μm at 0mbar (indicating noise) to
7.82±3.06μm at 1000mbar (full deflection amplitudes,
p<0.0001), whereas there was no notable change for
drive pressures exceeding 600mbar (p>0.05). For wave
amplitudes between 0mbar (noise) and 200mbar (sig-
nificant amplitudes), we found an optimal threshold of
3.6μm (indicated by green lines in Figure 2A). Similar
to wave amplitudes, displacement SNR increased from
22.12±10.75 to 93.56±31.45 (p<0.001), with an optimal
SNR threshold of 38.18 to exclude noisy wave amplitudes
in all livers from analysis. SD of liver SWS is shown in
Figure 2C. Note the steep decrease from 0.77±0.17m/s to
0.31±0.09m/s at 0 and 200mbar, respectively (p<0.001).
Again, an optimal threshold, namely an SWS SD of 0.55,
ensured sufficient wave amplitudes already at 200mbar
vibration pressure. Eight of 11 subjects found the vibra-
tion amplitudes at 1000mbar still acceptable, whereas
three described them to be slightly uncomfortable. All
subjects reported the vibration amplitudes at 200mbar to
be negligible. Therefore, 200mbar was the drive pressure
recommended for the experiments described below.
Figure 3compares the results and quality of the SWS
maps obtained by 2D rapid MRE and 3D SE-EPI-MRE for
the same volunteer. Similar transverse slices are shown
for end-inspiration and end-expiration selected from the
same 3D MRE scan and corresponding to the 2D MRE
slice that was acquired during end-expiration. It should
be noted that the transverse 2D rapid MRE scan was only
acquired during end-expiratory breath-hold to avoid read-
justment of the slice position that would have been nec-
essary due to liver movement. Grayscale and color maps
are displayed because quantitative values are better cap-
tured by color maps, whereas details are better seen in
grayscale maps. Overall, image quality and detail reso-
lution of SWS maps were similar for the two methods.
Note that our novel MRE sequence acquired only four
wave dynamics and one wave component, whereas 3D
MRE maps were reconstructed from eight wave dynam-
ics and three field components. Quantitative SWS values
of the liver were similar in all three images as demon-
strated in Figure3B, with slightly higher percentileranges
in rapid MRE than 3D MRE. Mean liver SWS values
were 1.48±0.12m/s, 1.46±0.10m/s, and 1.43±0.09m/s
for rapid MRE, 3D MRE (end-inspiration), and 3D
MRE (end-expiration), respectively, without significant
differences.
318 ANDERS et al.
(A)
(B) (C)
FIGURE 4 Use of rapid MRE for time-resolved measurement of liver stiffness during breathing in a coronal view. (A) Representative
SWS maps corresponding to the defined breathing states after motion correction using image registration. Color-coded frames indicate
precise breathing states (green: end-expiration breath-hold; purple: end-inspiration breath-hold; red: Valsalva; blue: free breathing). All 100
SWS maps acquired within 62.5s are provided as supplemental Figure S1. (B) SWS and displacement data obtained from image registration
averaged within the liver for three volunteers (the upper row corresponds to the subject shown in (A)). The colors demarcate the phases of
breathing within which SWS was averaged for group analysis. The gray phase (2s) represents the transition period before tissue oscillation
reaches equilibrium. (C) Group statistical plot of means and 95% confidence intervals for SWS and liver displacement during different
breathing maneuvers. *p<0.05, **p<0.01.
The use of our novel MRE sequence to study the
influence of breathing on SWS is illustrated in Figure 4.
Representative SWS maps after image registration for
breathing motion correction show the pixel-wise changes
in SWS during different breathing maneuvers. The
full series of 100 coronal SWS maps is available as
Supporting Information (see Figure S1). Overall liver stiff-
ness in the volunteer shown was apparently higher at
end-inspiration compared to both the Valsalva maneu-
ver (p<0.01) and end-expiration (p<0.01). Movies of
SWS maps covering all breathing maneuvers investigated
in one of the volunteers, with and without image regis-
tration, are provided as Video S1. The time courses of
spatial means shown in Figure 4B for three volunteers
corroborate our visual interpretation of the SWS maps
presented in Figure 4A. Moreover, displacement curves
obtained from image registration are plotted, indicating
the breathing-induced physiological displacement of the
liver along the feet–head direction. Remarkably stable
SWS values were obtained despite pronounced motion
patterns during the free-breathing phase following the
Valsalva maneuver. Shear wave amplitudes also did not
significantlyvarywithbreathing.GroupmeanSWSvalues
and liver displacements for the phases in all 11 subjects
are shown in Figure 4C for the four color-coded phases in
Figure 4A,B. The lowest SWS values were observed dur-
ing end-expiration (1.49±0.22m/s), but the values were
not significantly different from those obtained during the
Valsalva maneuver (1.60±0.22m/s) and free breathing
(1.62±0.25m/s), again suggesting that end-expiration
is the best controlled breathing state for liver MRE.
However, a significant difference was observed between
SWS at end-expiration and peak SWS at end-inspiration
(1.83±0.22m/s,p<0.01).THEreproducedthemainfind-
ingofhigherSWSvaluesafterinspiration(1.36±0.06m/s)
than expiration (1.30±0.06m/s, p<0.05) while providing
lower values than MRE (p<0.01), as discussed below. No
change in wave amplitudes was induced by the different
ANDERS et al. 319
breathing maneuvers (all p>0.05). All SWS values are
summarized in Table 1. Our results for liver displace-
ment, shear wave amplitudes, and SWS values for the four
respiratorystatesinvestigatedaresummarizedinTableS1.
4DISCUSSION
Here, we present a novel MRE sequence based on a
multishot, GRE sequence with spiral readout. With an
acquisition time of 625ms for obtaining 2D SWS maps of
the abdomen, this, to our knowledge, is the fastest MRE
method available for liver studies to date. As shown by
the two experiments we conducted, the method can be
used to optimize parameter settings and to assess elas-
togramqualitybeforeacquiringhigher-dimensionalMRE.
It can also be used to study potential changes in stiffness
related to physiological changes in geometry, blood flow,
or abdominal pressures that can be induced in the liver by
breathing.
Our sequence provides a technical solution for short
T∗
2relaxation times in larger FOVs, where organs, such as
the liver, can move and deform moderately during the res-
piratory cycle. The key innovation is based on 2D k-space
sampling with only a few segments (three), time steps
(four), and wave components (one), and TR adaptation to
multiple integer periods (2 of 40Hz) of externally induced
continuous oscillations (requiring clock synchronization
between wave generator and MRI scanner). These specific
parameters that we used here could be further optimized
for higher frequencies, shorter TR, and fewer time points
inthevibrationcycle.Forexample,retaining3k-spaceseg-
mentsandshorteningtheMEGto11.5mswouldallowTR
to be reduced to 40ms, which could be matched to two
oscillation periods of 50Hz. Furthermore, reducing the
number of time steps to three would result in even shorter
sampling times of 9*40+20ms=380ms,providedthat
imagequalityissufficientforMREinversion.Thisdemon-
strates the generalizability of our technique to further
optimize rapid MRE sequences.
The potential benefit of rapid MRE scout scans to
obtain information on whether shear waves penetrate the
ROI has been discussed in the literature.4Involving exter-
nal hardware, MRE is susceptible to technical failure if
adequate feedback on the operational status of the equip-
ment is not available. For example, inadequate placement
of actuators or failure of acoustic power transmission
coulddiminishwaveamplitudes,degradingstiffnessmaps
or even corrupting the entire examination. A rapid MRE
scan can quickly provide feedback, so the operator can
check for potential deficiency of shear waves or adjust
driver positions and wave amplitudes prior to the actual
clinicalMREscanofinterest.Moreover,patientawareness
of MRE actuator vibrations, combined with the feedback
receivedbytheoperator,couldfurtherincreasethesuccess
rate of clinical MRE35–37 and minimize technical failures
related to mechanical excitation at low costs.
In our experiments, we demonstrated the con-
sistency of SWS values obtained by our novel MRE
sequence in comparison with SE-EPI-MRE, which has
become an established MRE technique for the liver.25,38,39
SE-EPI-MRE is more susceptible to off-resonance-related
distortion artifact than segmented spiral readout
sequences,40,41 whereas the latter are more susceptible to
blurringartifacts.Otherk-spacesamplingschemesforfast
GREMRE,suchasradialreadout,havebeenproposedand
are currently being tested.42 ThefactthatSE-EPI-MRE
could not resolve a difference in stiffness between the end
of inspiration and end of expiration may be attributable
to the long scan time and breath-hold phases (21s vs. 10s
in our breathing experiment) (Figure 4), which averages
out temporal effects. Because THE is a rapid method for
stiffness measurement (1s acquisition time), it has been
used as a robust tool to test physiologic effects in elas-
tography.43 However, in this study, THE identified only
a slight difference in stiffness between end-inspiration
and end-expiration (5%), whereas rapid MRE detected a
much larger effect of nearly 24%. We believe that rapid
MRE in the coronal view captures the instantaneous
response of liver stiffness to respiration better than THE
because, during an ultrasound examination, the operator
must readjust the probe position and acoustic window
after each breathing command. This also indicates that
the timing of the maneuver is more important than the
net duration of data acquisition. It is worthwhile to men-
tion that THE provided slightly lower values than MRE
(approximately 1.3m/s vs. 1.5m/s). This is possibly due
to the high SWS dispersion of healthy liver, which may
shift the effective center frequency of the multifrequency
shear waves from 41.5Hz to lower values, thus reducing
the measured effective SWS.44
ArichbodyofliteraturereportsMREoftheliverunder
various conditions of blood perfusion, fasting, and breath-
ing. A marked postprandial increase in liver stiffness has
beenobservedinbothpatientswithchronicliverdisease45
and healthy volunteers11 and has been shown to corre-
late with portal venous flow.46 These findings have led
to the recommendation that MRE should be performed
in a controlled fasted state.9Furthermore, MRE is typi-
cally performed at end-expiration10 because the state of
breathing during the MRE scan was identified as a con-
founder of liver stiffness.18,19 Both breathing and eating
affect hepatic perfusion, suggesting that enhanced hemo-
dynamic activity of the liver and the resulting higher
intravascular pressure are associated with increased tis-
suestiffness.Thisnotionwassupportedbytheobservation
320 ANDERS et al.
TABLE 1 Mean values and SDs of shear wave speed within the liver for each subject and group values acquired in different experiments of this study
Rapid MRE study Breathing study Ultrasound elastography
Sequence
SE-EPI-MRE SE-EPI-MRE Rapid MRE Rapid MRE Rapid MRE Rapid MRE Rapid MRE THE THE
Breath hold state
End-
Expiration End-
Inspiration End-
Expiration End-
Expiration End-
Inspiration Valsalva Free
breathing End-
Expiration End-
Inspiration
No. Mean and SD of SWS Values in m/s
11.45±0.38 1.51±0.18 1.37±0.18 1.22±0.06 1.89±0.30 1.67±0.07 1.34±0.02 1.25±0.02 1.30±0.02
21.52±0.17 1.39±0.17 1.38±0.22 1.90±0.17 2.27±0.22 1.86±0.21 2.05±0.26 1.23±0.02 1.33±0.07
31.60±0.31 1.60±0.22 1.52±0.19 1.31±0.03 1.54±0.22 1.33±0.10 1.41±0.10 1.37±0.04 1.52±0.05
41.61±0.38 1.38±0.24 1.42±0.18 1.39±0.07 1.58±0.09 1.37±0.09 1.46±0.06 1.26±0.03 1.30±0.03
51.51±0.13 1.46±0.22 1.44±0.18 1.51±0.08 1.80±0.22 1.54±0.11 1.45±0.06 1.35±0.04 1.38±0.06
61.29±0.18 1.33±0.16 1.32±0.15 1.22±0.06 1.68±0.06 1.55±0.04 1.65±0.08 1.38±0.04 1.37±0.02
71.32±0.43 1.41±0.18 1.38±0.19 1.59±0.21 1.68±0.06 1.32±0.06 1.68±0.24 1.23±0.03 1.29±0.03
81.50±0.32 1.52±0.25 1.50±0.22 1.45±0.04 1.86±0.31 1.56±0.10 1.61±0.04 1.39±0.03 1.35±0.04
91.64±0.38 1.65±0.23 1.62±0.27 1.84±0.25 2.14±0.23 1.92±0.27 2.14±0.24 1.28±0.06 1.40±0.04
10 1.37±0.24 1.42±0.19 1.42±0.18 1.48±0.06 1.94±0.34 1.87±0.08 1.40±0.05 1.25±0.04 1.33±0.02
11 1.52±0.36 1.40±0.19 1.38±0.18 1.45±0.04 1.78±0.14 1.66±0.08 1.52±0.04 1.36±0.04 1.36±0.07
Group 1.48±0.12 1.46±0.10 1.43±0.09 1.49±0.22 1.83±0.22 1.60±0.22 1.62±0.25 1.30±0.06 1.36±0.06
Abbreviations: MRE, MR elastography; SE-EPI-MRE, spin-echo, echo-planar-imaging MRE; SWS, shear wave speed; THE, time-harmonic elastography.
ANDERS et al. 321
that liver stiffness was higher after ingestion of water,12,13
whereas relief of high portal pressure by shunting was
reported to cause a decrease in stiffness.47,48 Furthermore,
ahigherintra-abdominalpressureasgeneratedbytheVal-
salva maneuver can lead to a collapse of hepatic veins
and overall reduction of liver perfusion, resulting in hep-
atic softening.7,8 Conversely and in agreement with pre-
vious studies,18,19 our results at end-inspiration suggest
that preserved hepatic flow in the presence of elevated
intra-abdominal pressure leads to higher stiffness values.
Although these results provide strong evidence for hep-
atohemodynamic effects on tissue stiffness, they are cor-
relative and not causal. Beyond blood perfusion, other
factors such as geometric deformation with compression
stiffening49 or changes in the metabolic state of hepa-
tocytes might dynamically alter liver stiffness.50 In any
case, by measuring dynamic changes in tissue stiffness,
the proposed rapid MRE sequence could open a window
into the study of relationships between biomechanics and
function/perfusion properties of abdominal tissues, simi-
lartowhathasrecentlybeenreportedforothertissuesand
organs such as the lower extremities23 or the brain.24
Our study has limitations. First, by nature of the
design as an exploratory, technical feasibility study, only
healthy participants were investigated. It would be inter-
esting to test a short clinical protocol in patients with
chronic liver diseases and detect possible stiffness differ-
ences between inspiration and expiration within approx-
imately two breathing cycles. Such dynamic property
changes might reveal the alteration of the dynamic com-
ponent of liver stiffness better than two static measure-
ments.19 A technical limitation is the restriction of our
novel MRE technique to 2D, whereas shear waves in the
abdomen are 3D vector fields. Therefore, a geometric bias
may occur if the slices are not optimally aligned with
respect to the wave propagation direction. However, the
k-based multi-inversion method that we used mitigates
the geometric bias by incorporating spatiotemporal filters
that favor in-plane propagating waves while suppressing
waves that cross the image plane obliquely. In addition,
the cosine dependence of the geometric bias, as discussed
in Ref. 51 minimizes the effect of oblique waves on the
resulting 2D SWS maps. A further technical limitation is
thatwe didnotimplementthe data processingpipelineon
ourMRI scanner;thus, rapidMREimageswerecomputed
offline, and the wave amplitude information and stiffness
maps were not available to us until after the examina-
tions.However,asmentionedearlier,thegoalofthisstudy
was to demonstrate the technical feasibility of our novel
MRE technique and its use for rapid measurement of liver
stiffness during the respiratory cycle. After this successful
pilot study, we plan to fully implement the postprocess-
ingpipeline ofrapidMRE onourMRI system.Once phase
images have been received from the MRI system’s com-
puter, MRE inversion can be performed within a fraction
of a second.
5CONCLUSION
This study shows the feasibility of rapid MRE for subsec-
ond sampling of abdominal stiffness. The viable method
can be used for navigating the setup of MRE driver
hardware and postprocessing pipelines as well as for
detecting stiffness variations due to breathing-induced
changes in abdominal pressure and blood flow to the
liver. Using rapid MRE for quantification of liver stiffness
changes attributable to breathing, we observed a decrease
in stiffness from end-inspiration, to Valsalva maneuver, to
end-expiration. Overall, with the findings presented here,
this approach has opened the door to instantaneous mea-
surement of tissue stiffness in abdominal organs using
MRE,withquasireal-timeresolutionsimilartoultrasound
elastographybutlesslimitedintermsofimagepositioning
and data quality, and the possibility of using the scan as a
scout for externally induced shear waves.
AFFILIATIONS
1Department of Radiology, Charité—Universitätsmedizin Berlin,
Corporate Member of Freie Universität Berlin and
Humboldt-Universität zu Berlin, Berlin, Germany
2Application Development, Siemens Healthcare GmbH, Erlangen,
Germany
3Berlin Center for Advanced Neuroimaging (BCAN), Berlin, Germany,
Corporate Member of Freie Universität Berlin, Berlin Institute of Health
and Humboldt-Universität zu Berlin, Berlin, Germany
4Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and
Berlin, Berlin, Germany
5Department of Medical Physics, University of Wisconsin, Madison,
Wisconsin USA
6Department of Radiology, University of Wisconsin, Madison,
Wisconsin USA
7Charité—Universitätsmedizin Berlin, Corporate Member of Freie
UniversitätBerlinandHumboldt-Universität zuBerlin,Berlin, Germany
8Working Group On CMR, Experimental and Clinical Research Center,
a cooperation between the Max Delbrück Center for Molecular
Medicine in the Helmholtz Association and the
Charité—Universitätsmedizin Berlin, Berlin, Germany
9DZHK (German Centre for Cardiovascular Research), partner site
Berlin, Berlin, Germany
10Department of Cardiology and Nephrology, HELIOS Hospital
Berlin-Buch, Berlin, Germany
11Department of Medical Engineering, Technische Universität Berlin,
Einstein Centre Digital Future, Berlin, Germany
12Institute of Medical Informatics, Charité—Universitätsmedizin Berlin,
CorporateMemberofFreieUniversitätBerlinandHumboldt-Universität
zu Berlin, Berlin, Germany
322 ANDERS et al.
ACKNOWLEDGMENTS
We thank the German Research Foundation (DFG) for
funding (RTG2260 BIOQIC, CRC1340 Matrix-in-vision).
Open Access funding enabled and organized by Projekt
DEAL.
ORCID
Matthias Anders https://orcid.org/0000-0002-6447-
2029
Tom Meyer https://orcid.org/0000-0002-2171-6791
Carsten Warmuth https://orcid.org/0000-0001-8785-
1999
Josef Pfeuffer https://orcid.org/0000-0001-9887-0458
Heiko Tzschaetzsch https://orcid.org/0000-0001-9458-
2221
Helge Herthum https://orcid.org/0000-0001-6494-0833
Mehrgan Shahryari https://orcid.org/0000-0002-3981-
1711
Katja Degenhardt https://orcid.org/0000-0002-0482-
9698
Oliver Wieben https://orcid.org/0000-0002-7931-1930
Sebastian Schmitter https://orcid.org/0000-0003-4410-
6790
Jeanette Schulz-Menger https://orcid.org/0000-0003-
3100-1092
Tobias Schaeffter https://orcid.org/0000-0003-1310-
2631
Juergen Braun https://orcid.org/0000-0001-5183-7546
Ingolf Sack https://orcid.org/0000-0003-2460-1444
TWITTER
Ingolf Sack bioqic@twitter.de
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SUPPORTING INFORMATION
Additional supporting information may be found in the
online version of the article at the publisher’s website.
VIDEO S1: Animations of 100 coronal shear wave speed
maps acquired at a frame rate of 62.5Hz during breath-
ing maneuvers corresponding to Figure 4A of the main
manuscript. The left side of the animation shows shear
wave speed maps without image registration, while the
right side shows maps with image registration. The pur-
ple region of interest delineates the liver in the registered
images.
FIGURES1:Full set of coronalmaps showing shearwave
speed during the respiratory study, corresponding to the
subset featured in Figure 4A of the main manuscript.
100 liver shear wave speed maps acquired in one sub-
ject over 62.5s were corrected for respiratory motion
using image registration. Breathing states are delineated
by color-coded frames (green:end-expiration breath-hold;
324 ANDERS et al.
purple: end-inspiration breath-hold; red: Valsalva; blue:
free breathing).
TABLE S1: Spatially averaged values of shear wave speed
(SWS in m/s) and shear wave amplitude (SWA in μm)
as well as liver displacement (LD in mm) for different
breathing states in the breathing study.
How to cite this article: Anders M, Meyer T,
Warmuth C, et al. Rapid MR elastography of the
liver for subsecond stiffness sampling. Magn Reson
Med. 2024;91:312-324. doi: 10.1002/mrm.29859
