Three-dimensional visualisation of the fetal heart using prenatal MRI with motion-corrected slice-volume registration: a prospective, single-centre cohort study

Abstract

Background: Two-dimensional (2D) ultrasound echocardiography is the primary technique used to diagnose congenital heart disease before birth. There is, however, a longstanding need for a reliable form of secondary imaging, particularly in cases when more detailed three-dimensional (3D) vascular imaging is required, or when ultrasound windows are of poor diagnostic quality. Fetal MRI, which is well established for other organ systems, is highly susceptible to fetal movement, particularly for 3D imaging. The objective of this study was to investigate the combination of prenatal MRI with novel, motion-corrected 3D image registration software, as an adjunct to fetal echocardiography in the diagnosis of congenital heart disease.

Methods: Pregnant women carrying a fetus with known or suspected congenital heart disease were recruited via a tertiary fetal cardiology unit. After initial validation experiments to assess the general reliability of the approach, MRI data were acquired in 85 consecutive fetuses, as overlapping stacks of 2D images. These images were then processed with a bespoke open-source reconstruction algorithm to produce a super-resolution 3D volume of the fetal thorax. These datasets were assessed with measurement comparison with paired 2D ultrasound, structured anatomical assessment of the 2D and 3D data, and contemporaneous, archived clinical fetal MRI reports, which were compared with postnatal findings after delivery.

Findings: Between Oct 8, 2015, and June 30, 2017, 101 patients were referred for MRI, of whom 85 were eligible and had fetal MRI. The mean gestational age at the time of MRI was 32 weeks (range 24-36). High-resolution (0·50-0·75 mm isotropic) 3D datasets of the fetal thorax were generated in all 85 cases. Vascular measurements showed good overall agreement with 2D echocardiography in 51 cases with paired data (intra-class correlation coefficient 0·78, 95% CI 0·68-0·84), with fetal vascular structures more effectively visualised with 3D MRI than with uncorrected 2D MRI (657 [97%] of 680 anatomical areas identified vs 358 [53%] of 680 areas; p<0·0001). When a structure of interest was visualised in both 2D and 3D data (n=358), observers gave a higher diagnostic quality score for 3D data in 321 (90%) of cases, with 37 (10%) scores tied with 2D data, and no lower scores than for 2D data (Wilcoxon signed rank test p<0·0001). Additional anatomical features were described in ten cases, of which all were confirmed postnatally.

Interpretation: Standard fetal MRI with open-source image processing software is a reliable method of generating high-resolution 3D imaging of the fetal vasculature. The 3D volumes produced show good spatial agreement with ultrasound, and significantly improved visualisation and diagnostic quality compared with source 2D MRI data. This freely available combination requires minimal infrastructure, and provides safe, powerful, and highly complementary imaging of the fetal cardiovascular system.

Funding: Wellcome Trust/EPSRC Centre for Medical Engineering, National Institute for Health Research.

Figure 1

Scatter plots comparing measurements from two independent observers for echocardiography (A) and MRI (B) The blue line represents the line of equality in both panels. The distribution of errors is shown in panel C, with the Bland-Altman plot in panel D. There was a small but significant mean bias of −0·33 mm (95% CI −0·46 mm to −0·20 mm; p<0·0001) in favour of larger echocardiography measurements of the same structure when compared with MRI.

Figure 2

Results of structured anatomical assessment from two independent observers, shown by anatomical category (A) Proportion of all cases in which structures of interest could be identified. (B) Diagnostic quality assessment. 2DMRI=two-dimensional MRI data. 3DVOL=three-dimensional motion-corrected MRI volume. *p<0·0001.

Figure 3

Motion-corrected MRI data from a fetus with double aortic arch at 32 weeks Shown are the descending aorta (DAo), arterial duct (D), and left (L) and right (R) aortic arches. At 2 months postnatal age, contrast-enhanced MRI could show a right-sided arch (middle panel); however, a ligamentous remnant of the left arch was predicted on the basis of the fetal MRI findings (asterisk); this finding was confirmed at surgery (right panel). The distal remnant of the arterial duct—analogous to the diverticulum of Kommerell—is also seen (K). See video 3 for more detail.

Figure 4

Example segmentation from motion-corrected 3D data, in a 33-week fetus referred because of abnormal right pulmonary veins on echocardiography (A) In this anterior projection of the lungs and major blood vessels, a single right pulmonary vein (RPV) can be seen draining anomalously to the inferior vena cava (IVC) in the circled area. A single left pulmonary vein (LPV) was also noted. Inset: minimum-intensity projection of the 0·7mm isotropic volume used to generate segmentation (RPV=yellow, IVC=blue). (B) All findings were confirmed postnatally by contrast-enhanced CT, with the anomalous vein indicated with an arrow. See video 4 for more detail.

Figure 5

Segmentation of a fetal heart from 3D data at 32 weeks in a fetus with pulmonary atresia and ventricular septal defect, right aortic arch, and disconnected pulmonary arteries Fetal MRI showed two large collateral arteries (asterisks): the left pulmonary artery (LPA) was supplied by a large collateral vessel originating close to the origin of the left common carotid artery, with the right pulmonary artery (RPA) supplied by a tortuous collateral or arterial duct from the underside of the aortic arch. The left subclavian artery (LSCA) was also noted to be aberrant. All findings were confirmed with postnatal CT at 2 months (right panel). The bottom panel shows three coronal planes of the original 3D motion-corrected fetal data. These images were used for pre-birth surgical planning and parental counselling. DAo=descending aorta. RColl=right collateral.

Figure 6

Segmentation of motion-corrected MRI data of a fetus with suspected coarctation of the aorta at 33 weeks' gestation Posterior projection (top left) and left lateral projection (top right) are shown. The aorta (Ao), arterial duct (AD), descending aorta (DAo), aortic isthmus (i), and superior vena cava (SVC) are labelled. Coarctation was confirmed after birth and treated surgically. The bottom panel shows planes from the reconstructed 3D dataset in a transverse (Tra), coronal (Cor), and sagittal (Sag) orientation. See video 2 for more detail. TA=transverse arch. PA=pulmonary artery.