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Fetal whole-heart 4D blood flow visualisation using motion-corrected multi-planar real-time PC-bSSFP MRI
Thomas A Roberts1, Joshua F.P. van Amerom1, Anthony N Price1, Maria Deprez1, David F. A. Lloyd1,2, Laurence H Jackson1, Milou P.M van Poppel1, Kuberan Pushparajah2, Mary A Rutherford1, Reza Rezavi1,2, and Joseph V Hajnal1

1School of Biomedical Engineering & Imaging Sciences, King's College London, London, United Kingdom, 2Department of Congenital Heart Disease, Evelina Children's Hospital, London, United Kingdom

Synopsis

Measurement of blood flow in the fetal heart and the great vessels is challenging due to fetal motion and small vessel sizes. 2D methods for fetal flow imaging require significant slice piloting to locate the vessels, and small changes in fetal position can often necessitate reacquisition. In this work, we demonstrate the potential for motion-corrected whole-heart 4D flow imaging in the fetus using stacks of highly accelerated 2D bSSFP slices, which are inherently sensitive to velocity. Real-time acquired images were aligned in space and cardiac phase, and vectorially combined to yield time-resolved flow information.

Introduction

Measuring blood flow in the fetal heart and great vessels is challenging because the heart beats very rapidly, the vessels are small and the fetus is prone to spontaneous movement. Recently, we have developed a framework for retrospective motion-corrected 4D reconstruction of the fetal heart and great vessels from 2D real-time balanced steady state free precession (bSSFP) [1]. The framework was initially designed for cine imaging and disregarded the phase in the 2D bSSFP images, however, the bSSFP sequence is intrinsically velocity-sensitive because the first-moment is non-zero along the read and slice directions [2]. In this work, we use motion-corrected volumetric reconstruction of the velocity-sensitive phase of 2D bSSFP images to allow for 4D visualisation of blood flow in the fetal heart.

2D phase contrast gradient echo (PC-GRE) methods for measuring fetal blood flow [3] are susceptible to both in- and through-plane motion, often requiring repeated slice-planning and reacquisition. PC-GRE also uses a segmented acquisition that causes temporal mixing of acquired data. Mapping the blood velocity in the entire heart using motion-corrected methods may address these shortcomings.

Methods

All imaging was performed on a 1.5T Philips Ingenia scanner. To demonstrate proof of principle, stacks of parallel 2D bSSFP slices were acquired in a flow phantom (3 stacks orthogonal to scanner axes, 3 oblique), and in a single pregnant volunteer (5 stacks) using the following parrameters: TR/TE 3.8/1.9ms, flip angle 60°, 8x k-t SENSE [4] acceleration, field of view 400×304mm, voxel size 2.0×2.0x6.0mm, slice overlap 3-4mm, 96 images per slice in 7s, 37 slices. In the phantom study, images were acquired with voxel size 1.5x1.5x3.0mm, slice overlap 1.5mm and without acceleration.

4D Reconstruction Framework: 4D velocity-sensitive volumetric reconstructions were performed using a processing pipeline, shown in Fig1, modified from work described for image-domain volume reconstruction of the fetal brain [5] and fetal heart [1]. Magnitude and phase volumes were reconstructed separately, using motion-correction, cardiac synchronisation and outlier rejection parameters estimated from magnitude-valued data. Velocity-sensitive phase was separated from background phase in the the acquired bSSFP images by subtracting a third-order 3D polynomial fit to the phase in static amniotic fluid and tissue in each acquired stack isolated [6]. The velocity-sensitive directions in scanner space of each image were calculated from the first moments of gradients, the stack orientation and motion correction parameters, before being vectorially combined.

Flow Phantom: Water was passed through plastic tubing at a constant flow rate using a water pump. Two types of tubing with different internal diameters were formed into a continuous loop, which returned water to the pump. To minimise bSSFP artefacts, the tubing was housed inside a water-filled spherical flask (Fig2a). The phantom was imaged using PC-GRE for comparison with the volumetric PC-bSSFP reconstruction.

Results

Phase maps from the PC-bSSFP volumetric reconstruction were similar to PC-GRE phase maps in the superior-inferior direction (Fig2). In the 4D fetal heart reconstruction (Fig3) strong blood flow was observed in all great vessels. The 4D reconstructed phase was most sensitive to blood flow in the fetal superior-inferior direction, with the phase of the blood in the aorta and pulmonary artery directed towards the fetal head, while the phase in the superior vena cava showed blood returning to the heart. The pulsatility of arterial blood flows could also be observed.

Discussion

The presented framework allowed for 4D visualisation of blood flow in the fetal heart and great vessels. Motion-correction and outlier rejection to compensate for fetal motion and maternal respiration. This approach is especially advantageous for fetal cardiac imaging, since data can be acquired without highly-specific scan plane prescriptions, and referenceless PC-bSSFP allows for velocity estimation from a single image. In the future, the magnitude and phase data will be combined into a single reconstruction pipeline, which we anticipate will improve motion correction and outlier rejection while simultaneously generating 4D image-domain and 4D flow data.

Acknowledgements

Thomas A. Roberts and Joshua F.P. van Amerom are joint first authors of this work.

This work was supported by the Wellcome EPSRC Centre for Medical Engineering at King’s College London (WT 203148/Z/16/Z) and by the National Institute for Health Research (NIHR) Biomedical Research Centre based at Guy’s and St Thomas’ NHS Foundation Trust and King’s College London. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health.

References

[1] van Amerom JFP, Lloyd DFA, Murgasova MK, Price AN, Malik SJ, van Poppel MPM, Pushparajah K, Rutherford MA, Razavi R, Hajnal JV. Fetal whole-heart 3D cine reconstruction using motion-corrected multi-slice dynamic imaging. ISMRM 2018, p.1052.

[2] Markl M, Alley MT, Pelc NJ. Balanced phase‐contrast steady‐state free precession (PC‐SSFP): a novel technique for velocity encoding by gradient inversion. Magn. Reson. Med. 2003;49(5):945-52.

[3] Jansz MS, Seed M, van Amerom JFP, Wong D, Grosse‐Wortmann L, Yoo SJ, Macgowan CK. Metric optimized gating for fetal cardiac MRI. Magn. Reson. Med. 2010;64(5):1304-14.

[4] Tsao J, Boesiger P, Pruessmann KP. k-t BLAST and k-t SENSE: dynamic MRI with high frame rate exploiting spatiotemporal correlations. Magn. Reson. Med. 2003;50:1031–42.

[5] Kuklisova-Murgasova M, Quaghebeur G, Rutherford MA, Hajnal J V., Schnabel JA. Reconstruction of fetal brain MRI with intensity matching and complete outlier removal. Med. Image Anal. 2012;16:1550–64.

[6] Nielsen JF, Nayak KS. Referenceless phase velocity mapping using balanced SSFP. Magn. Reson. Med. 2009;61(5):1096-102.

Figures

Figure 1: Framework for velocity-sensitive 4D reconstruction of the fetal heart from multi-planar real-time 2D bSSFP. 4D reconstruction is first performed using magnitude images [1], consisting of an initial motion correction stage static (temporal mean) images; cardiac synchronisation, including including heart rate estimation and slice-slice cardiac cycle alignment; and further motion-correction using real-time images interleaved with 4D reconstruction; followed by a final final 4D reconstruction, including outlier rejection. Phase images are corrected and then used in a 4D reconstruction with previously-estimated parameters.

Figure 2: Comparison of superior-inferior encoded PC-GRE sequence and velocity-sensitive 3D PC-bSSFP volumetric reconstruction. (a) Coronal and (b) transverse magnitude images. Dashed-yellow box shows region in phase maps. There was good agreement in the flow in (c) the PC-GRE map and (d) the 3D PC-bSSFP volume reconstruction created from 6 stacks.

Figure 3: Velocity-sensitive 4D cardiac reconstruction of healthy 30 week fetus. Magnitude and velocity-sensitive phase are shown in (a) sagittal aortic arch plane, (b) three vessel view and (c) coronal plane perpendicular to three vessel view. The phase was most sensitive to velocities in the fetal superior-inferior direction. Flow in the inferior direction (blue), is seen in the descending aorta (DAo) and superior vena cava (SVC), while flow in the superior direction (red) is seen in the ascending aorta (Ao) and pulmonary artery (PA). Peak flows can be seen in systole with reduced flow during diastole. The right atrium (RA) is also labelled for reference.

Proc. Intl. Soc. Mag. Reson. Med. 27 (2019)
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