Nienke P.M. Wassenaar1, Anne-Sophie van Schelt1, Eric M. Schrauben1, Rémi van der Woude2, Jamila E. de Jong2, Jules L. Nelissen1, Hanneke W.M. van Laarhoven3, Jing Guo4, Ingolf Sack4, Jurgen H. Runge1, Aart J. Nederveen1, and Jaap Stoker1
1Radiology and Nuclear Medicine, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, Netherlands, 2University of Twente, Enschede, Netherlands, 3Department of Medical Oncology, Cancer Center Amsterdam, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, Netherlands, 4Department of Radiology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Synopsis
Free-breathing acquisition of
pancreatic MR elastography can potentially introduce errors in stiffness
reconstruction. In this study, breathing tasks are introduced during interleaved
and reversed slice order MRE acquisition to determine if the quality of MRE
increases. The shear-wave speed and octahedral shear strain
signal-to-noise-ratio in the pancreas did not significantly change when using
breathing tasks. However, the stability of the pancreas location over time
increases when using breathing tasks combined with reversed slice ordering as
well as the octahedral shear strain signal-to-noise-ratio in the whole abdomen.
Future research should focus on comparing shear-wave speed reproducibility of
both MRE methods.
Introduction
Pancreatic MR
Elastography (MRE) can detect viscoelastic changes in the course of
pancreatitis or pancreatic cancer1,2. Both breath-hold and free-breathing (FB) MRE is possible,
the latter preferable in sick patients unable to suspend their breath multiple
times. However, FB-MRE acquisition can lead to a mismatch in pancreatic location
over multiple phase-offsets, potentially introducing errors in stiffness reconstruction.
Using a breathing task (BT) paradigm timed such
that MRE acquisition for a given slice occurs during the same respiratory phase
could potentially increase MRE quality without limiting the temporal and
spatial resolution. We investigated the impact of BTs on pancreatic MRE by evaluating
the pancreatic location over multiple phase-offsets. Furthermore, the influence
of BTs on the octahedral shear strain signal-to-noise-ratio (OSS-SNR) and
shear-wave speed (SWS) was determined.Methods
Study
protocol:
Nine healthy
volunteers (♂=3,♀=6, mean
age 27±2 years) were
included. Subjects fasted four hours prior to MRI examination. BTs were created
in ePrime (version 3.0,PST Inc.,Sharpsburg,PA,USA) and followed a natural
breathing pattern(Figure 1). The breathing period was equal to TR and phase-offset
delay, and instructions were synchronized with the sequence using a TTL pulse.
This way, each slice with varying phase-offset is acquired at the same
respiratory phase.
MRI
measurements:
Multi-slice
multi-frequency spin-echo echoplanar imaging (SE-EPI) MRE images were acquired with a 3.0T MRI scanner
(R.5.7.1.1,Ingenia,Philips,Best,the Netherlands). Mechanical vibrations were
introduced using four compressed-air driven MRE transducers at four vibrational
frequencies (MREfreq=30,40,50,60Hz)2. Motion encoding
gradients (MEG) were applied along three orthogonal directions. Three different
MRE acquisitions were recorded(Table 1). In FB-MRE scans, no BTs were displayed
and standard interleaved slice ordering was used. For the two MRE scans using synchronized
BTs, interleaved (BT-Int) and reversed central slice ordering (BT-Rev) were
performed(Figure 1). BT-Rev was used to test if central slices containing the
pancreas within the multi-slice acquisition were scanned during end-expiration.
Analysis
and statistics:
To
determine the stability of the pancreas location over phase-offsets for the
three MRE scans, the pancreas was manually delineated in three slices aimed at
head, body and tail on the magnitude MRE images for eight phase-offsets at 30
and 50 Hz. The mean dice similarity coefficient (DSC) of all combinations of the
regions of interest (ROI) of all three slices was calculated. To test for
differences between BT-Int and BT-Rev, the DSC for each slice was compared. Magnitude
images of BT-Int and BT-Rev were visually compared to investigate the influence
of slice order on image quality.
The whole
pancreas was delineated on mean magnitude MRE images (mean over phase-offsets,
MEG directions, frequencies). These ROIs were used to determine the pancreatic
OSS-SNR and pancreatic SWS which was calculated with kMDEV inversion3.
The OSS-SNR was also calculated over the whole abdomen. Repeated measures ANOVA
with pairwise comparison and Bonferroni correction was used for statistical
analysis. Image analysis and statistical analysis were performed in Matlab
(R2021a,Mathworks,Natick,MA,USA) and SPSS (version 26,IBM,Armonk,NY,USA).Results
Mean values of DSC, SWS and
OSS-SNR are shown in Table 2. Compared with FB, DSC was significantly higher
for BT-Rev (p=0.026), while no significant difference was found for DSC between
BT-Int and BT-Rev or FB and BT-Int. No significant differences were found
between the MRE scans for pancreatic SWS and OSS-SNR. However, OSS-SNR in the
whole abdomen significantly increased for BT-Rev compared to FB and BT-Int (p-value=0.010
and 0.014 respectively).
Magnitude images over eight phase-offsets can be
found in Figure 2. Comparing the magnitude image quality between BT-Int and BT-Rev,
signal loss in various slices was present more pronounced in BT-Rev. Overlap
images of phase-offset ROIs and corresponding elastograms are shown in Figure 3. Discussion
Introduction of BT-Rev
paradigm during pancreatic MRE significantly increases DSC compared to FB-MRE.
This may be an important finding for pancreatic tumors where stromal tissue is
of great interest. Pancreatic tumors can be small and a consistent location
over multiple phase-offsets is needed to be able to perform sub-region analysis.
Previous research showed that 2D motion correction in coronal direction
improves sharpness of FB-MRE images4. Nevertheless, this is more difficult
in an axial orientation and eddy current artifacts lead to distortions when
acquiring pancreatic MRE in coronal orientation on a 3T MRI system.
BT-Rev MRE significantly improves
OSS-SNR in the whole abdomen compared to FB and BT-Int, while pancreatic OSS-SNR
did not significantly differ between scans. Higher abdominal OSS-SNR suggests
that measurements may be more reproducible when BT-Rev is used. The pancreatic
SWS did not significantly differ, and values were comparable to literature1,2,4,5.
Magnitude image quality of BT-Int
was visually higher than BT-Rev. This could be explained by signal leakage into
adjacent slices typical of EPI acquisitions. Despite this finding, the increase
in whole-abdomen OSS-SNR and DSC warrant future research on using BT-Rev to compare
the reproducibility of SWS measurements with FB-MRE. The scan time increased
two times when using BTs, giving the opportunity to acquire more/thinner slices
or a higher in-plane resolution. Furthermore, future research could focus on performing
motion correction in axial orientation or applying respiratory binning.
Conclusion
Although, pancreatic OSS-SNR
did not improve and SWS did not significantly change, using BTs during
pancreatic MRE acquisition causes a more stable pancreatic location over
multiple phase-offsets leading to a higher OSS-SNR in the whole abdomen. Acknowledgements
No acknowledgement found.References
- Zhu
L, Guo J, Jin Z et al. Distinguishing pancreatic
cancer and autoimmune pancreatitis with in vivo tomoelastography. Eur Radiol.
2021 May;31(5):3366-3374. doi: 10.1007/s00330-020-07420-5. Epub 2020 Oct 30.
PMID: 33125553.
- Marticorena
Garcia SR, Zhu L, Gültekin E et al. Tomoelastography for Measurement of Tumor
Volume Related to Tissue Stiffness in Pancreatic Ductal Adenocarcinomas. Invest
Radiol. 2020 Dec;55(12):769-774. doi: 10.1097/RLI.0000000000000704. PMID:
32796197.
-
Tzschätzsch
H, Guo J, Dittmann F et al. Tomoelastography by
multifrequency wave number recovery from time-harmonic propagating shear waves.
Med Image Anal. 2016 May;30:1-10. doi: 10.1016/j.media.2016.01.001. Epub 2016
Jan 13. PMID: 26845371.
-
Shahryari M, Meyer T, Warmuth C et al. Reduction of
breathing artifacts in multifrequency magnetic resonance elastography of the
abdomen. Magn Reson Med. 2021 Apr;85(4):1962-1973. doi: 10.1002/mrm.28558. Epub
2020 Oct 26. PMID: 33104294.
-
Gültekin E, Wetz C, Braun J et al. Added Value of Tomoelastography for Characterization of Pancreatic
Neuroendocrine Tumor Aggressiveness Based on Stiffness. Cancers (Basel). 2021
Oct 15;13(20):5185. doi: 10.3390/cancers13205185. PMID: 34680334.