Comparison of readout-segmented echo-planar imaging and single-shot echo-planar imaging in the fetal brain

Introduction

Magnetic resonance imaging (MRI) is helpful in assessing suspected anomalies in the fetal central nervous system (CNS) and visualizing complementary cases that routine ultrasonography (US) cannot display clearly (1). Its superior spatial and contrast resolution can provide anatomic information for patient counseling and decision-making, help improve pregnancy outcomes, and optimize perinatal management (2-5).

Diffusion-weighted imaging (DWI), which can assess water molecular movement within a tissue at a microscopic level, allows for the estimation of the organisation and structure of white matter tracts as myelinated white matter fibres restrict the free diffusion of water (6). The diagnostic value of DWI in fetal brain imaging has been established for various brain lesions, such as ischemia, cortical malformations, infections (7). Single-shot echo-planar imaging (SS-EPI) is routinely the most current technique used for clinical studies in the fetal brain as it is less susceptible to errors caused by motion that occur during diffusion sensitization of the magnetic resonance (MR) signal (8). The ability to capture data from a two-dimensional (2D) slice or a three-dimensional (3D) volume in less than 100 ms is the primary advantage of the echo-planar imaging (EPI) sequence. This feature makes EPI the preferred sequence of choice when multiple region of interest (ROI) measurements are required under different conditions or when subject movement is uncontrolled (9,10). This approach has been extensively used to investigate the normal brain’s structural connectivity and microstructure and various brain disorders (11-13). However, k-space fills slowly in the phase-encoding direction, then SS-EPI sequences are hampered by high sensitivity to geometric distortion, signal loss, and T2* blurring (14).

Readout Segmentation of Long Variable Echo-trains (RESOLVE) is an advanced DWI technology. RESOLVE samples a subset of contiguous points in the readout direction with a sinusoidal EPI readout. K-space is divided into segments along the readout direction by multiple shots. Data are captured by each shot from a series of consecutive k-space sample points, leading to prominent shorter echo spacing than with SS-EPI (8). RESOLVE has previously been applied in pediatric brain imaging (14-16). The findings of these studies showed that RESOLVE was capable of motion correction and image production with less susceptibility-related changes, distortion, and blurring, and to improve spatial resolution, compared with SS-EPI, with the application of shortened echo spacing in each segment, acceleration of k-space filling in the readout direction, and parallel imaging (14-16).

However, the application of RESOLVE has not been previously described in the fetal brain, for which DWI plays an important role in the evaluation of normal brain development. Therefore, this study aimed to determine the clinical feasibility of RESOLVE in the fetal brain and to compare SS-EPI and RESOLVE image quality on a 1.5T MRI scanner. We present this article in accordance with the STROBE reporting checklist (available at https://tp.amegroups.com/article/view/10.21037/tp-2025-77/rc).

Methods

Study population

This retrospective study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by institutional ethics board of Sichuan Provincial People’s Hospital (No. 2021288) and informed consent was signed by the patients’ legal guardians.

From December 2019 to December 2021, fetal MRI, including DWI with RESOLVE and SS-EPI, was conducted on a 1.5T MRI scanner.

Patients with gestational age >22 weeks were included. Exclusion criteria were (I) fetuses with congenital brain abnormalities or (II) images with artifacts that precluded evaluation (Figure 1).

Figure 1 Flow diagram of participants. DWI, diffusion-weighted imaging; SS-EPI, single-shot echo-planar imaging; RESOLVE, Readout Segmentation of Long Variable Echo-trains.

MR examinations

RESOLVE and SS-EPI images were performed with a 1.5T MR scanner (Aera, Siemens Healthineers, Erlangen, Germany) using a body matrix coil with 16-channel. All patients underwent DWI, half-Fourier acquisition single-shot turbo spin-echo (HASTE), and true fast imaging with steady-state precession (TRUFSIP). DWI was performed using conventional single excitation EPI and RESOLVE sequences, with a b-value =800 s/mm² (Table 1).

HASTE parameters: repetition time (TR) 1,300 ms, echo time (TE) 93 ms, slice thickness 4 mm, slice distance 0 mm, matrix 320×320, field of view (FOV) 400 mm × 400 mm, echo spacing 4.22 ms, and acquisition time 34 s. TRUFSIP parameters: TR 4.2 ms, TE 1.67 ms, slice thickness 4 mm, slice distance 0 mm, matrix 384×384, FOV 384 mm × 384 mm, and acquisition time 31 s. T1-weighted parameters: TR 3.8 ms, TE 1.4 ms, slice thickness 4 mm, slice distance 0 mm, matrix 128×128, FOV 320 mm × 320 mm, and acquisition time 15 s.

Qualitative analysis

Evaluation of the SS-EPI and RESOLVE images for the 190 patients was performed by two radiologists. All readers were blinded to the 2 types of DWI sequence, but they had access to clinical patient information and other MRI sequences (T1-weighted imaging, HASTE, and TRUFSIP). The overall image quality, lesion conspicuity, susceptibility-related changes, and image distortion were evaluated using a 5-point Likert scale (1, nondiagnostic; 2, poor; 3, standard; 4, good; and 5, outstanding). Image distortion referred to an alteration in size, profile, or orientation. Susceptibility-related signal referred to signal changes resulting from local B0 inhomogeneity. Lesion conspicuity referred to the contrast between background tissue and the lesion. The overall quality of the image was scored using the general evaluation of the images. The scores from the 2 readers for each sequence in each measure were averaged for further statistical analysis.

Quantitative analysis

The apparent diffusion coefficient (ADC) was calculated using the following formula:

Sb/S0=exp(−b×ADC)[1]

where Sb and S0 are the signal intensities in the diffusion gradient factors of b and 0. ROI of the ADC measurement was placed at the centrum semiovale (Figure 2). In addition, the ADC values in the bilateral centrum semiovale were measured twice and averaged for further statistical analysis.

Figure 2 Measurement of SNR and ADC on RESOLVE and SS-EPI. (A) ADC map of RESOLVE, and (B) ADC map of SS-EPI. ROIs were marked at the bilateral centrum semiovales (black circles). (C) Image (b=800 s/mm²) of RESOLVE and (D) image (b=800 s/mm²) of SS-EPI. ROI of SI_Brain was placed at bilateral centrum semiovales (black circles) and ROI of SI_Background was situated in the air (white circles). ADC, apparent diffusion coefficient; RESOLVE, Readout Segmentation of Long Variable Echo-trains; ROI, region of interest; SI, signal intensities; SNR, signal-to-noise ratio; SS-EPI, single-shot echo-planar imaging.

The signal-to-noise ratio (SNR) was calculated using the following formula:

SNR=(SIBrain−SIBackground)/SDBackground[2]

where SI_Brain and SI_Background are the mean signal intensities (SI) of the brain and air, and SD_Background is the standard deviation of air. The ROI of SI_Brain was placed at the centrum semiovale (Figure 2). SNR was repeatedly measured three times by each reader and was averaged for further statistical analysis.

For the SNR and ADC measurements, ROIs in the two DWI sequences were generally the same size and location to avoid any bias.

Statistical analysis

Inter-observer agreement between the two readers was evaluated using the weighted Cohen kappa test with 95% confidence intervals (≤0.20 indicated poor consistency; 0.21–0.40 average consistency; 0.41–0.60 moderate consistency; 0.61–0.80 good consistency; and 0.81–1.00 almost perfect agreement).

The SNR and ADC did not follow the normal distribution and were expressed as medians (range). The Mann-Whitney U test was adopted in the comparisons of the SNR and ADC between the two groups. The correlation of ADC values between ss-EPI and RESOLVE was determined by Spearman’s correlation analysis. Last, SPSS 21.0 (IBM Inc) was used in the statistical analysis of the obtained data. Statistical significance was assumed to be P<0.05.

Results

Participants

One hundred and twenty-three patients were excluded for significant motion artifacts in DWI images, and 199 patients were excluded for structure or signal abnormalities in the fetal brain. Ultimately, 190 pregnant women were included (mean age 27.5 years; range, 18–41 years), mean gestational age 31.5 weeks (range, 23–38 weeks); 24 patients were in their second trimester and 166 patients were in their third trimester.

Qualitative

The weighted Cohen kappa analysis showed a good-to almost perfect agreement between the two readers for all categories (Table 2). The two radiologists’ mean scores for overall image quality, lesion conspicuity, susceptibility-related change, and image distortion in the 190 patients are shown in Figure 3 and Table 3.

Figure 3 Bar graph shows average scores for four imaging parameters of RESOLVE and SS-EPI studies in 190 patients. Susceptibility-related changes, image distortion, lesion conspicuity, and overall quality for visualizing the brain were considered: image distortion was defined as an alteration in size, profile, or orientation; the susceptibility-related signal was defined as signal changes due to local B0 inhomogeneity; lesion conspicuity was defined as a contrast between the lesion and background tissue; and the overall image quality was scored with the general evaluation of the images. Observers used a 5-point Likert scale where 1 was nondiagnostic; 2, poor; 3, standard; 4, good; and 5, outstanding. RESOLVE was better than SS-EPI in every aspect (bar graph). RESOLVE, Readout Segmentation of Long Variable Echo-trains; SS-EPI, single-shot echo-planar imaging.

According to the two radiologists’ subjective evaluation, RESOLVE was better than SS-EPI in distortion reduction (P<0.001) and susceptibility-related change (P<0.001), lesion conspicuity (P<0.001), and overall image quality (P=0.003) (Figure 4).

Figure 4 Images of fetal brains in different gestational age for comparison of RESOLVE and SS-EPI. (A,B) RESOLVE images of a 25-week-old fetus, and (C,D) SS-EPI images of the same fetus. (E,F) RESOLVE images of a 30-week-old fetus and (G-H) SS-EPI images of the same fetus. Compared with SS-EPI, RESOLVE had better overall image quality without apparent artifacts (A,B,E,F). (G) Showed slight image distortion in the left cerebellar hemisphere (arrows), and (H) showed susceptibility artifacts in the right occipital lobe on SS-EPI (arrows). RESOLVE, Readout Segmentation of Long Variable Echo-trains; SS-EPI, single-shot echo-planar imaging.

Quantitative

The ADC values were 1.74 (range, 1.64–1.84) ×10⁻³ s/mm² for SS-EPI and 1.73 (range, 1.63–1.83) ×10⁻³ s/mm² for RESOLVE. ADC values in the centrum semiovale did not show significant difference between the two sequences (P=0.64). A significant positive association was noted between ADC values of the two sequences (P=0.003, R=0.229). The correlation of ADC values between RESOLVE and SS-EPI is shown in Figure 5. The SNR was 45.53 (range, 43.82–47.54) for SS-EPI and 35.57 (range, 33.76–37.55) for RESOLVE. Last, the SNR of SS-EPI was significantly higher than that of RESOLVE (P<0.001) (Figure 6).

Figure 5 Scatter plot of ADC values showing a correlation between RESOLVE and SS-EPI. The plot showed a positive correlation of ADC values between the two sequences (P=0.003, R=0.229). ADC, apparent diffusion coefficient; RESOLVE, Readout Segmentation of Long Variable Echo-trains; SS-EPI, single-shot echo-planar imaging.

Figure 6 Boxplot of SNR on SS-EPI and RESOLVE at the centrum semiovale showing that the SNR of SS-EPI was significantly higher than that of RESOLVE. RESOLVE, Readout Segmentation of Long Variable Echo-trains; SS-EPI, single-shot echo-planar imaging; SNR, signal-to-noise ratio.

Discussion

In our study, RESOLVE and SS-EPI were performed using 1.5T MRI in 190 fetal brains and reviewed by two radiologists. The results showed that RESOLVE had better image quality than SS-EPI, similar to the results of previous studies in pediatric brains (14-16).

SS-EPI is the preferred modality for DWI due to its rapid scanning speed and ability to withstand patient motion (8). Despite its advantages, SS-EPI slowly fills the k-space in the phase-encoded direction and is susceptible to geometric distortion, signal loss, and T2* blurring during scanning, which can give rise to limited spatial resolution and artifacts (17). The long duration between SS-EPI echoes results in distortions at the air-tissue interface, and the long echo trains cause T2* blurring, particularly at high field strengths (18,19). By dividing the k-space into multiple segments, the acquisition time of each echo is significantly shortened, with the reduction of susceptibility and T2* decay (8). RESOLVE incorporates various characteristics to expedite k-space traversal, minimizing the distortion typically associated with SS-EPI (20).

RESOLVE had better image quality due to several reasons. The distortions presented with EPI were primarily influenced by the slow traversal through the k-space in the phase-encoded direction (21). RESOLVE divided k-space into consecutive adjacent and sectionally overlapping segments, reducing the spacing between echoes in the echo train and leading to diminishing distortion (18,22). The echo spacing of the EPI train, which was segmented and shortened by RESOLVE, impacted the inter-echo acquisition time, reducing T2* blurring and geometric distortions. Geometric distortion, T2* blurring, and susceptibility-related changes were further reduced by the shorter spacing between echoes in the echo train (14). In our study, RESOLVE expedited k-space traversal, and the inter-echo acquisition time (0.38 ms) was shorter than SS-EPI (0.91 ms), thereby reducing these distortions.

Holdsworth et al. integrated RESOLVE and generalized autocalibrating partial parallel acquisition (GRAPPA) in pediatric patients. GRAPPA achieved a higher acceleration factor, and RESOLVE could be acquired at a higher resolution due to the decreased distortions (14). Sampling a consecutive series of k-space points at each shot adhered to the Nyquist condition, which allowed RESOLVE to gain a 2D navigator echo to correct nonlinear phase errors. Using a 2D navigator-based reacquisition scheme, the RESOLVE sequence was corrected for motion-induced phase errors before reconstruction. In addition, the 2D navigator used much shorter echo-spacing than SS-EPI, leading to reduced effects of susceptibility and T2* blurring. RESOLVE adopted a Cartesian k-space sampling strategy, leading to a shorter scanning time than a relevant Periodically Rotated Overlapping Parallel Lines with Enhanced Reconstruction (PROPELLER) sequence (8). Due to reduced susceptibility-related change and image distortion and improved lesion clarity, the overall image quality was therefore improved.

In our study, ADC values of RESOLVE and SS-EPI in quantitative comparisons had no statistical differences. This finding confirmed that ADC values acquired by RESOLVE could serve as a credible basis for observing the fetal brain compared to SS-EPI. It also indicated that RESOLVE has the potential to be used for further clinical applications in fetal brains with abnormalities. Our study results showed that the SNR of SS-EPI was better than that of RESOLVE, similar to previous reports (14,15). The SNR was affected by several factors, including the matrix sizes, point diffusion function (PSF), and T2 of the tested tissue (23). With more efficient k-space coverage and the absence of an additional navigator, SS-EPI had higher scanning time efficiency, contributing to the higher SNR due to the unstandardized scanning time of both RESOLVE and SS-EPI sequences, instead of other factors such as TE (14,15). Higher spatial resolution, and less blurring and distortion artifacts achieved by RESOLVE improved anatomic details and interfaces but lost SNR. The SNR varies across different scanning regions and field strengths, and is influenced by the exact imaging protocol (23). Fetal motion constitutes a major factor affecting SNR, so shorter-duration SS-EPI exhibits higher SNR. Despite the lower SNR of RESOLVE, its benefits were more useful in clinical practice. Increased field strength (3T), advanced denoising algorithms may also be employed to improve SNR in RESOLVE in future studies.

We found another disadvantage of the RESOLVE sequence besides the lower SNR. Although fetal movement would affect the scan, the pregnant woman or fetus could not be sedated. The scanning time of the RESOLVE sequence (2 m 30 s) was longer than that of SS-EPI (41 s) in this study. The increased scanning time heightened the possibility of fetal movement affecting the process, and motion artifacts would significantly reduce image quality. The navigator would fail to correct phase errors when the k-space center shifted out of the navigator acquisition window, due to serious subject movement during the diffusion preparation caused by the increasing time. Furthermore, the motion information resulted in corrupted data. These corrupted data could seriously decrease image quality and aggravate the effect of motion artifacts (24). This finding might account for the better image quality of SS-EPI in a few cases in our study.

Innovative techniques have also shown promise in reducing motion artifacts. Hutter et al. introduced a system allowing alternative decision of diffusion encoding on the slice level, and a longer time sampling of slices with low b-value was subsequently realized. This new encoding technology enabled more robust motion correction (25). In their studies of eight fetal subjects, the novel approach proved robust and effective, and it demonstrated benefit in reducing distortion and motion correction in all subjects. The diffusion encoding can be incorporated into any acquisition parameters, including multiband imaging, and may be applied to DWI with RESOLVE in general (25).

The utilization of optimized MRI coils is anticipated to reduce the transfer of vibration and motion artifacts. We employed a body matrix coil with 16-channel, which is routinely implemented for abdominopelvic imaging protocols. Dedicated scanning coils specifically designed for pregnant women represents another method for reducing motion artifacts (26). Besides, the motion correction algorithms showed in focused ultrasound surgery (FUS) in moving organs can also achieve motion-compensation by deriving motion information from MR monitoring images (27,28).

As radiologists often prioritize faster protocols due to time constraints and patient comfort, the routine clinical application of RESOLVE in fetal brain is limited due to its long scanning time with the current protocol. A survey of radiologists from Department of Radiology of Sichuan Provincial People’s Hospital suggested the main clinical adoption barrier of RESOLVE was the long scanning time and consequent motion artifacts during the scan which potentially influence the image quality. To address clinical workflow demands and radiologists’ requirements, future work will need to prioritize minimizing the scan time of the RESOLVE sequence while maintaining its diagnostic utility. Many studies have proposed improved schemes for the RESOLVE sequence to shorten longer scanning times. Scanning times could be shortened by utilizing partial Fourier reconstruction and omitting readout segments on one side of the k-space (29). Simultaneous multislice (SMS) is an acceleration technique, which has been introduced to shorten scanning times by slicing the acceleration factor and be competent for compatible acquisition of multiple slices (30). Frost et al. successfully applied the SMS technique to RESOLVE (SMS-RESOLVE), resulting in a 50% reduction of the scanning time in adult brain imaging (18). Future research may be needed to investigate the implementation of these methodologies in fetal brain MRI to optimize scan duration.

There are several limitations in this study. First, our study did not involve any fetuses with congenital brain anomalies, and we did not explore the superiority of the RESOLVE sequence in pathological situations. MRI is particularly beneficial in diagnosing callosal, cerebral cortical, and posterior fossa anomalies and destructive pathologies of the brain parenchyma. According to the recommendations of the American College of Radiology (ACR), fetal MRI is primarily indicated for congenital anomalies and vascular abnormalities (31). Therefore, further research including the cohort of fetal brain anomalies are required to validate the application of RESOLVE in these abnormalities in fetal brains. Second, RESOLVE’s longer scan time compared to SS-EPI currently limits its routine clinical use. Although acceleration techniques (GRAPPA, SMS) were not applied in this study, we plan to incorporate them in future research. We are also collaborating to develop advanced motion-correction strategies to further improve RESOLVE’s clinical feasibility. Third, our analysis of image quality was primarily based on the technical characteristics of the two imaging sequences. However, gestational age was identified as an additional influencing factor. According to prior study, with advancing gestational age, the frequency of fetal movements decreases, which is attributed to the reduction in intrauterine space (32). As most of the patients were examined in their third trimester, fetal movement was less prominent. Therefore, the results from qualitative evaluation of the 2 sequences was also influenced. Fourth, the study was conducted at a single institution and lacked longitudinal follow-up to assess the reproducibility of results across different MRI scanners and operators. A multicenter study utilizing MRI systems from different manufacturers will help rigorously validate the reproducibility of the results.

Conclusions

The RESOLVE image quality was better than that of SS-EPI in visualizing the fetal brain without a significant difference in ADC values between the two sequences. Although RESOLVE had lower SNR than SS-EPI, better image quality made this acceptable. RESOLVE images are more conducive to the clinical diagnosis of fetal craniocerebral lesions. As RESOLVE is affected by fetal movement due to long scanning times, further parameter optimization is still needed.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tp.amegroups.com/article/view/10.21037/tp-2025-77/rc

Data Sharing Statement: Available at https://tp.amegroups.com/article/view/10.21037/tp-2025-77/dss

Peer Review File: Available at https://tp.amegroups.com/article/view/10.21037/tp-2025-77/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tp.amegroups.com/article/view/10.21037/tp-2025-77/coif). M.C. is currently an employee of Siemens Healthineers Ltd. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by institutional ethics board of Sichuan Provincial People’s Hospital (No. 2021288) and informed consent was signed by the patients’ legal guardians.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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