Free-breathing Diffusion Tensor Imaging of the In Vivo Human Heart - Stimulated Echo vs. Spin Echo Acquisition
Constantin von Deuster1,2, Christian T. Stoeck1,2, Martin Genet2, David Atkinson3, and Sebastian Kozerke1,2

1Division of Imaging Sciences and Biomedical Engineering, King's College London, London, United Kingdom, 2Institute for Biomedical Engineering, University and ETH Zurich, Zurich, Switzerland, 3Centre for Medical Imaging, University College London, London, United Kingdom

Synopsis

In vivo cardiac Diffusion Tensor Imaging (DTI) using the Stimulated Echo Acquisition Mode (STEAM) is particularly challenging during free breathing acquisition. To address this limitation, spin echo (SE) sequences employing motion-compensated diffusion gradients may be used. In this work, scan time, SNR efficiency and diffusion tensor metrics are compared between the STEAM method and a second-order motion compensated SE approach. For SE, SNR and gating efficiency were increased by 2.65 and 29% relative to STEAM, respectively. It is concluded that the SE method is an attractive alternative to STEAM based approaches for in vivo free-breathing cardiac DTI.

Introduction

The Stimulated Echo Acquisition Mode (STEAM) has been the primary method for in vivo cardiac Diffusion Tensor Imaging (DTI)1. STEAM, however, requires two consecutive heartbeats to encode the signal, hence requiring breath holding or narrow-window respiratory gating for consistent signal formation2. Additionally, the inherent signal loss of STEAM relative to Spin Echo (SE) and the impact of cardiac strain during STEAM encoding render STEAM DTI acquisition of the beating heart particularly challenging3,4. To address these limitations, single shot SE sequences may be used in combination with respiratory navigator gating and motion compensated diffusion gradient waveforms5. It is the objective of the present work to compare respiratory gating and SNR efficiency along with diffusion tensor metrics between STEAM DTI and second-order motion compensated SE DTI of the in vivo human heart6,7.

Methods

Cardiac-triggered diffusion-weighed STEAM and second-order motion compensated SE sequences (Figure 1) were implemented on a 1.5T Philips Achieva system (Philips Healthcare, Best, The Netherlands) equipped with a 5-channel cardiac receiver array and a gradient system delivering 80mT/m @ 100mT/m/ms. Data were acquired in 7 healthy subjects (5 female, weight 62±9kg, age 24±2years, heart rate 66±10beats/min). Written informed consent according to institutional guidelines was obtained prior to imaging. STEAM was implemented as described previously2. For second-order motion compensated SE7, fat suppression was performed using a 1-3-3-1 binomial spatial-spectral excitation pulse8. A variable rate selective excitation (VERSE)9 echo pulse was employed to reduce echo times. Both STEAM and SE used reduced field-of-view excitation. Data acquisition was performed during free-breathing using navigator gating (NAV1 gating window: 5mm). For STEAM, data were accepted if the relative displacement between NAV1 and NAV2 was within ± 0.5mm (Figure 1a). Diffusion encoding was along 3 (b=100s/mm2) and 9 (b=450s/mm2) directions10. Imaging parameters were: in-plane resolution 2.8×2.8mm2, slice thickness 8mm, FOV: 230×98mm2, TE/TR(STEAM): 31ms/2-R-R, TE/TR(SE): 70ms/1-R-R, number of signal averages STEAM/SE: 8/16 to obtain identical nominal scan times. Imaging was triggered to the systolic strain “sweet spot” to avoid strain effects in STEAM3. Myocardial SNR of STEAM vs. SE was assessed per single average in a separate scan using b=100s/mm2 and 450s/mm2 encoded along 6 diffusion directions (16mm slice thickness, 4 signal averages). SNR was normalized to unit time yielding SNR efficiency SNRt. DTI analysis was performed on mean diffusivity (MD), fractional anisotropy (FA), the local helix elevation (helix angle) and the deviation of the helix from circumferential contour (transverse angle). For all scans, navigator gating efficiency was recorded.

Results

Navigator efficiency of STEAM was 29% lower on average compared to SE resulting in effective scan times across all volunteers of 8:28±2:56 min:sec vs. 5:59±2:43 min:sec for STEAM vs. SE. The ratio of SNR efficiency SNRt(SE/STEAM) = SNRt(SE)/SNRt(STEAM) for SE versus STEAM was 2.9±0.7 and 2.4±0.6 for b=100 and 450s/mm2, respectively. A comparison of helix and transverse angle maps acquired in the same subject is given in Figure 2. The linear transmural change of helix angles is noted for both techniques in Figure 2b. In the STEAM case, however, endo- and epicardial helix angles were found to be less steep with increased angle variation relative to SE. Transverse angles were close to zero degrees with significantly increased standard deviation in the STEAM case compared to SE (-1.6±20.7° vs. -2.6±16.5°, p<0.01) (Figure 2c). The root-mean-square error (RMSE) of linear regression of transmural helix angles was significantly higher for STEAM vs. SE (19.8±4.2° vs. 15.9±3.7°, p<0.01). While 3.5±1.4% of the diffusion tensors derived from STEAM had negative eigenvalues, no negative eigenvalue was detected for SE. FA values obtained with STEAM were significantly higher relative to SE (0.60±0.03 vs. 0.37±0.03, p<0.001) while MD values were lower for STEAM vs. SE (1.01±0.06x10-3mm2/s vs. 1.49±0.15x10-3mm2/s, p<0.001).

Discussion

Free-breathing cardiac diffusion tensor imaging using second-order motion-compensated SE DTI allows for significantly shorter scan times (29%) while yielding a 2.65-fold increase in SNR when compared to STEAM DTI of the in vivo heart. The higher SNR of SE DTI translates into improved diffusion tensor accuracy as evidenced by helix and transverse angle distributions. Of note, systematic differences for MD and FA between STEAM and SE were found. These differences may be explained by the long diffusion time ΔT of STEAM (ΔTSTEAM = 1000ms vs. ΔTSE = 25ms) and associated motional narrowing effects during STEAM encoding11.

Conclusion

Navigated, second-order motion compensated SE DTI presents an attractive alternative to STEAM DTI for free-breathing mapping diffusion tensors of the in vivo heart on modern MR systems with high-performance gradients.

Acknowledgements

This work is supported by UK EPSRC (EP/I018700/1).

References

1. Edelman R, Gaa J, Wedeen VJ, et al. In vivo measurement of water diffusion in the human heart. Magn Reson Med 1994;32:423–428.

2. 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;70:454–465.

3. Tseng WI, Reese TG, Weisskoff RM, et al. Cardiac diffusion tensor MRI in vivo without strain correction. Magn Reson Med 1999;42:393–403.

4. Stoeck CT, Kalinowska A, von Deuster C, et al. Dual-phase cardiac diffusion tensor imaging with strain correction. PLoS One 2014;9: e107159.

5. Gamper U, Boesiger P, Kozerke S. Diffusion imaging of the in vivo heart using spin echoes - considerations on bulk motion sensitivity. Magn Reson Med 2007;57:331–337.

6. Welsh C, Di Bella E, Hsu E. Higher-order motion-compensation for in vivo cardiac diffusion tensor imaging in rats. IEEE Trans Med Imaging 2015;34:1843–1853.

7. 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. doi: 10.1002/ mrm.25784.

8. Meyer CH, Pauly JM, Macovski A, et al. Simultaneous spatial and spectral selective excitation. Magn Reson Med 1990;15:287–304.

9. Hargreaves BA, Cunningham CH, Nishimura DG, et al. Variable rate selective excitation for rapid MRI sequences. Magn Reson Med 2004; 52:590–597.

10. 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.

11. Noehren B, Andersen A, Feiweier T, et al. Comparison of twice refocused spin echo versus stimulated echo diffusion tensor imaging for tracking muscle fibers. J Magn Reson Imaging 2015;41:624–632.

Figures

Diffusion weighted STEAM (a) and second-order motion compensated SE (b) sequence.

Helix and transverse angle maps for SE and STEAM acquisition (a). Summary of helix angle distributions for endo-, mid- and epicardial myocardium (b). The solid boxes and error bars correspond to the 50% and 90% percentile of the helix angle distribution along the circumferential dimension. Histogram of transverse angle distributions (c).



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