A comparison of M012 compensated spin-echo and STEAM cardiac DTI at multiple cardiac phases
Andrew David Scott1,2, Sonia Nielles-Vallespin1,3, Pedro Ferreira1,2, Peter Gatehouse1,2, Zohya Khalique1, Philip Kilner1,2, Dudley Pennell1,2, and David Firmin1,2

1Cardiovascular Biomedical Research Unit, Royal Brompton and Harefield Foundation NHS Trust, London, United Kingdom, 2National Heart and Lung Institute, Imperial College London, London, United Kingdom, 3National Heart Lung and Blood Institute, National Institutes of Health, Bethesda, MD, United States

Synopsis

In-vivo cardiac diffusion tensor imaging (cDTI) performed with a stimulated echo (STEAM) sequence is considered strain sensitive and low SNR. Alternatively, motion compensated spin-echo (M012-SE) sequences are thought to be strain insensitive and high SNR, but suffer from long echo times and short mixing times. In this work we compare the reliability of and the cDTI parameters derived from STEAM and M012-SE data in 20 volunteers at mutliple points in the cardiac cycle on a standard clinical scanner. We show systematic differences between the sequences and show that there are few correlations between these differences and strain and/or T1/T2.

Purpose

In this work, we implement a velocity and acceleration compensated spin-echo (SE) cardiac diffusion tensor imaging (cDTI) sequence1,2,3 on a clinical 3T scanner with standard gradients and show initial comparisons with a stimulated echo (STEAM)4,5 sequence at multiple points in the cardiac cycle. We also correlate parameter differences between sequences with strain, T1 and T2.

Methods - cDTI acquisition

A SE EPI cDTI sequence was implemented with 0th, 1st and 2nd order motion-compensated diffusion gradients (M012)1,2. Mid-ventricular short-axis cDTI was performed in 20 healthy volunteers on a 3T Siemens Skyra (gradients 45mT/m@200T/m/s per axis) with M012-SE and STEAM5. Acquisitions were performed at end-systole, end-diastole and the sweet-spot. The sweet-spot is the trigger-time at which strain effects in STEAM should be eliminated6 and DENSE analysis from 13 subjects found an average of 150ms from the R-wave. Time from R-wave to diffusion-encoding was matched between sequences. Optimal parameters were used for both sequences2,7. M012 acquisitions used bmain=450smm-2, TE=73ms and water-selective excitation. STEAM acquisitions used bmain=800smm-2, TE=23ms and fat saturation. Both acquisitions used 6 diffusion directions, bref=150smm-2, 6 averages, TR=2RR-intervals, reduced phase field-of-view, 360x135x8mm3 at 2.8x2.8mm2 resolution, SENSE x2 and an identical EPI echo train. Each breath-hold was 20RR for both sequences. Since STEAM requires 2RR for diffusion-encoding, M012-SE was triggered to alternate R-waves.

Methods - Strain and T1/T2-mapping

Strain information was obtained from a breath-hold 2D spiral cine DENSE acquisition8 in the same plane as cDTI. T1 and T2 maps were acquired in the same plane using a 5(3)3 modified Look-Locker sequence9 and a T2-prep based 3-point method10 respectively.

Methods - Processing

cDTI data were processed using in-house software to produce pixel-wise maps of mean diffusivity (MD), fractional anisotropy (FA), helix angle (HA), tensor mode (mode), signal to noise ratio (SNR)5 and absolute second eigenvector angle (E2A)11. Circumferential and radial strain data was obtained from the DENSE data using the University of Virginia DENSE analysis software. Mean T1 and T2 values were calculated from a septal region of interest.

Methods - Statistical analysis

Global left ventricular cDTI parameters were compared between sequences using a Wilcoxon signed-rank test (p<0.01). To test the influence of strain, Pearson’s correlation coefficient was calculated between systolic – diastolic cDTI parameters and peak radial and circumferential strain. The influence of T1 and T2 weighting was investigated by correlating differences in cDTI parameters between sequences with T1 and T2 values.

Results

cDTI was performed successfully in all subjects and time points using STEAM. Processed M012-SE data was considered insufficient quality for further analysis in 2/20 systolic, 5/20 sweet-spot and 6/20 diastolic acquisitions due to bulk-motion related signal loss. Figure 1 shows examples of good cDTI parameter maps from one subject at all time points acquired using both sequences. Figure 2 shows examples of sweet-spot parameter maps in one subject where the M012-SE maps are poor. Global cDTI parameters are plotted in figure 3. There were significant differences between M012-SE and STEAM in MD, FA, E2A and Helical Angle gradient (HAg, °/mm) at all time points and SNR in diastole. Few of the correlations were significant (see table for all p<0.05) and only systolic FA (STEAM – M012-SE) vs. T1 reached p<0.01.

Discussion and conclusions

Previous studies using M012-SE have used high performance gradient systems1,2,3, but we have demonstrated the feasibility of M012-SE cDTI using standard clinical gradients with a similar TE. While M012-SE can be performed at points throughout the cardiac cycle in most subjects, STEAM was successful in all subjects. This is due to the short diffusion gradients used with STEAM and despite the motion compensated design of M012-SE, failure was likely due to uncompensated cardiac motion during the long diffusion-encoding gradients. This also results in a long TE when using M012-SE and hence an increased T2 sensitivity. Differences between sequences in systolic SNR and FA, and diastolic MD were found to significantly correlate with T2.

STEAM cDTI is usually considered to have poor SNR efficiency and to be affected by strain4. However, few differences in cDTI parameters between systole and diastole demonstrated a significant correlation with peak strains and we did not observe increased SNR when using M012-SE, but did find higher STEAM SNR in diastole.

These preliminary results demonstrate that there are systematic differences between cDTI parameters derived from M012-SE and STEAM. While strain, T1 and T2 partially account for some differences, the factor 50 difference in mixing-time between sequences (~20ms M012-SE vs. ~1s STEAM) is likely to be responsible for the majority (figure 4). This is consistent with the higher FA and lower MD found using STEAM.

Future work will focus on a comprehensive analysis of these techniques, their relative advantages and suitable applications.

Acknowledgements

This work was performed at the National Institute for Health Research funded Cardiovascular Biomedical Research Unit at the Royal Brompton Hospital and Imperial College London.

References

1. Welsh CL, DiBella EV, Hsu EW. Higher-Order Motion-Compensation for In Vivo Cardiac Diffusion Tensor Imaging in Rats. IEEE Trans Med Imaging. 2015;34(9):1843-53.

2. Stoeck CT, von Deuster C, Genet M, et al. Second-order motion-compensated spin echo diffusion tensor imaging of the human heart. Magn Reson Med. 2015 May 28. doi: 10.1002/mrm.25784. [Epub ahead of print].

3. von Deuster C, Stoeck CT, Genet M, et al. Spin echo versus stimulated echo diffusion tensor imaging of the in vivo human heart. Magn Reson Med. 2015 Oct 7. doi: 10.1002/mrm.25998. [Epub ahead of print].

4. Reese TG, Weisskoff RM, Smith RN et al. Imaging myocardial fiber architecture in vivo with magnetic resonance. Magn Reson Med. 1995;34(6):786-91.

5. Nielles-Vallespin S, Mekkaoui C, Gatehouse P, et al. In vivo diffusion tensor MRI of the human heart: reproducibility of breath-hold and navigator-based approaches. Magn Reson Med. 2013;70(2):454-65.

6. Tseng WY, Reese TG, Weisskoff RM, Wedeen VJ. Cardiac diffusion tensor MRI in vivo without strain correction. Magn Reson Med. 1999;42(2):393-403.

7. Scott AD, Ferreira PF, Nielles-Vallespin S et al. Optimal diffusion weighting for in vivo cardiac diffusion tensor imaging. Magn Reson Med. 2015;74(2):420-30. doi: 10.1002/mrm.25418. Epub 2014 Aug 22.

8. Zhong X, Spottiswoode BS, Meyer CH et al. Imaging three-dimensional myocardial mechanics using navigator-gated volumetric spiral cine DENSE MRI. Magn Reson Med. 2010;64(4):1089-97.

9. Kellman P, Wilson JR, Xue H et al. Extracellular volume fraction mapping in the myocardium, Part 1: Evaluation of an automated method. J Cardiovasc Magn Reson. 2012;14(63).

10. Giri S, Chung YC, Merchant A et al. T2 quantification for improved detection of myocardial edema. J Cardiovasc Magn Reson. 2009;11(56).

11. Ferreira PF, Kilner PJ, McGill LA et al. In vivo cardiovascular magnetic resonance diffusion tensor imaging shows evidence of abnormal myocardial laminar orientations and mobility in hypertrophic cardiomyopathy. J Cardiovasc Magn Reson. 2014;16(87).

Figures

Figure 1: High-quality cDTI parameter maps from one example subject acquired using STEAM and M012-SE at 3 points in the cardiac cycle.

Figure 2: Despite the relatively similar SNR between sequences and the good quality reference images, in this subject the M012-SE data at the sweet-spot did not demonstrate the normal transmural progression of HA.

Figure 3: cDTI parameters compared between STEAM and M012-SE. Individual subjects are plotted as coloured crosses and the median and interquartile range are shown in black (STEAM) or grey (M012-SE). As might be expected, given the much shorter mixing time, the MD is higher and FA is lower in the M012-SE sequence than for STEAM. SS – sweet-spot.

Figure 4: Root mean squared distances diffused during the mixing time. Pig heart histology in a plane perpendicular to the myocyte long-axis. Based on a diffusivity of 3x10-3mm2s-1 (free water at 37oC), during the mixing time (Δ) free-water molecules would diffuse around 75μm in the STEAM acquisition, but only around 10μm in the M012-SE acquisition, which is less than the diameter of a typical myocyte.

Table: Significant correlations (p<0.05). Pearson's correlation coefficient was calculated between differences in cDTI parameters across the cardiac cycle (systole - diastole) and both radial and circumferential global strain. Then cDTI parameter differences between sequence (STEAM - M012-SE) were correlated with both T1 and T2. T1 and T2 were measured in ms, MD in x10-3 mm2s-1 and transmural helix angle gradient (HAg) in o/mm.



Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
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