Measuring human placental blood flow with multidelay 3D GRASE pseudocontinuous arterial spin labeling at 3T

Abstract

Background: Placenta influences the health of both a woman and her fetus during pregnancy. Maternal blood supply to placenta can be measured noninvasively using arterial spin labeling (ASL).

Purpose: To present a multidelay pseudocontinuous arterial spin labeling (pCASL) combined with a fast 3D inner-volume gradient- and spin-echo (GRASE) imaging technique to simultaneously measure placental blood flow (PBF) and arterial transit time (ATT), and to study PBF and ATT evolution with gestational age during the second trimester. The PBF values were compared with uterine arterial Doppler ultrasound to assess its potential clinical utility.

Study type: This was a prospective study.

Subjects: Thirty-four pregnant women.

Field strength/sequence: Multidelay 3D inner-volume GRASE pCASL sequence on 3T MR scanners.

Assessment: Subjects underwent two longitudinal MRI scans within the second trimester, conducted between 14-16 and 19-22 weeks of gestational age, respectively. Placental perfusion was measured using the free-breathing pCASL sequence at three postlabeling delays (PLDs), followed by offline motion correction and model fitting for estimation of PBF and ATT.

Statistical tests: A paired t-test was conducted to evaluate the significance of PBF/ATT variations with placental development. A two-sample t-test was conducted to evaluate the significance of PBF difference in subjects with and without early diastolic notch.

Results: The mean PBF and ATT for the second trimester were 111.4 ± 26.7 ml/100g/min and 1387.5 ± 88.0 msec, respectively. The average PBF increased by 10.4% (P < 0.05), while no significant change in ATT (P = 0.72) was found along gestational ages during the second trimester. PBF decreased 20.3% (P < 0.01) in subjects with early diastolic notches in ultrasound flow waveform patterns.

Data conclusion: Multidelay pCASL with inner-volume 3D GRASE is promising for noninvasive assessment of PBF during pregnancy. Its clinical use for the detection of aberrations in placental function and prediction of fetal developmental disorders awaits evaluation.

Level of evidence: 1 Technical Efficacy: Stage 2 J. Magn. Reson. Imaging 2018;47:1667-1676.

Keywords: arterial spin labeling (ASL); gestational age; human placenta; magnetic resonance imaging (MRI); placental blood flow (PBF).

Figure 1

(a) Scheme of inner-volume GRASE pCASL sequence. Background suppression was achieved by two inversion pulses following a whole volume pre-saturation. Switching the slice selective gradient to Y-axis for re-focusing pulses preserved the signal only within the targeting imaging volume to avoid wrapping around artifacts along Y-axis. (b) Demonstration of spatial position of imaging volume and ASL labeling plane. Labeling place was placed at aortic bifurcation and highlighted by the yellow dashed line.

Figure 2

Simulated time courses of longitudinal magnetization of spins moving across the labeling plane (t=0 ms) under: (a) label and (b) control conditions. Velocities of spins are 11.5 cm/s and 40.3 cm/s, which represent the vessel center velocity at aortic bifurcation and carotid arteries, respectively.

Figure 3

(a) Perfusion signal at PLD 1000/1500/2000 ms of a representative slice. (b) Calculated PBF maps. One of focal hyper-perfusion regions was indicated by a blue arrow. (c) Calculated ATT maps. Images are overlaid on the T2-weighted structural image measured by GRASE sequence.

Figure 4

3D views of PBF (a) and ATT (b) map. Three pairs of coronal/sagittal slices were displayed adjacent to the transverse plane, and their spatial positions were specified by color arrows around the transverse image.

Figure 5

Comparison of PBF (left plot) and ATT (right plot) acquired from two scans within the second trimester. Each dot in the plot represents PBF or ATT of a single subject while horizontal and vertical axes represent the data from the first (14–16 weeks) and second (19–22 weeks) scans respectively. Slope of the solid blue line was estimated from 34 subjects’ data using the least square method. Red dashed line was plotted for reference with a slope of 1 indicating no change between two scans.

Figure 6

(a) Histogram of PBF values, which was divided into nine consecutive bins with a width of 50 ml/100g/min except the last bin is open ended, at repeated scans. Fraction of PBF values in each bin was averaged across 34 subjects with error bars indicating the inter-subject standard deviation. (b) Mean ATT in nine regions corresponding to PBF bins at repeated scans. Each bar represented the ATT averaged across 34 subjects with error bars indicating the inter-subject standard deviation.

Figure 7

Scatter plot of resistance index (RI) and pulsatility index (PI) versus PBF values. Left and right column showed RI/PI from left and right uterine artery, respectively. Top and bottom row showed results acquired after the first and second MRI scans, respectively. Linear regression between RI/PI and PBF was illustrated by dashed lines, and no significant correlation was found (P values were listed next to each dashed line). Subjects with the early diastolic notch were labeled by red filled marks. Bilateral/unilateral notches presented in three/one subjects’ Doppler ultrasound waveform pattern acquired after the first MRI scan. Two subjects (subject #5 and #26) with persistent notches at two scans were identified by blue and green arrows. Bilateral/unilateral notches presented in subject #26/#5 Doppler ultrasound waveform pattern acquired after the second MRI scan.