Combining optimized three-dimensional ZOOMit real inversion recovery with T2-preparation to shorten the delay interval and scan time for endolymphatic hydrops evaluation in patients with Ménière’s disease

Introduction

Endolymphatic hydrops (EH) of the membranous labyrinth is present in various inner ear disorders (1), such as Ménière’s disease (MD), low-frequency sudden sensorineural hearing loss (SSNHL), vestibular migraine, vestibular schwannoma, and delayed EH. EH and perilymphatic enhancement (PE) have been found to be correlated with the clinical features of MD (2). Previously, in the absence of surgery, the presence or absence of EH in patients with the above-mentioned inner ear disorders could not be objectively demonstrated. It was not until 2007 that Nakashima et al. (3) first successfully visualized EH in living patients with MD using a three-dimensional (3D) fluid-attenuated inversion recovery (FLAIR) sequence following the intratympanic administration of gadolinium (Gd). Since then, 3D real inversion recovery (IR) after the intratympanic administration of Gd (IT-Gd) has been employed to evaluate EH (4,5). However, IT-Gd is not a common route for the contrast enhancement of magnetic resonance imaging (MRI), is an invasive technique, and requires a 24-hour-delay interval before MRI. These limitations have hindered the widespread use of this method. Thus, a less invasive method, such as the intravenous administration of Gd (IV-Gd), is needed. Nakashima et al. (6) successfully used 3D-FLAIR and 3D-real IR after administering a double-dose IV-Gd to visualize EH in patients with MD.

Studies have shown that 3D-real IR has a more precise grading of EH than does 3D-FLAIR (7-9), as the former differentiates the endolymphatic space, perilymphatic space, and the surrounding bone (5). Currently, the scan time of 3D-real IR is long, ranging from 559 to 920 seconds (5,7,10-12), which makes it difficult for some individuals, especially those with vertigo, to remain still. Furthermore, the noise produced by MRI can induce or aggravate vertigo and hearing loss (13). Additionally, the delay interval between IV-Gd and MRI acquisition ranges from 3.5 to 6 hours (6,11,14), which increases the wait times and complicates the patient workflow.

A recent study showed that the 3D-zoomed imaging technique with parallel-transmission (ZOOMit) sampling perfection with application-optimized contrasts using different flip-angle evolutions (SPACE) real IR had a shorter scanning time compared to that of 3D turbo spin-echo (TSE) real IR (12). However, the scan time and delay interval of this sequence were still long. Combining a specific T2 preparation (T2Prep) and inversion time (TI) was shown to be useful in separating the perilymphatic space from the endolymphatic space in noncontrast 3D-FLAIR (15). Moreover, Barlet et al. (16) demonstrated that using a 3D-FLAIR sequence with a longer repetition time (TR) can shorten the delay interval from 4 hours to 2 hours. However, Chen et al. (17) reported that a 3-hour time interval for 3D-real IR was not feasible for clinical practice. This is because the signal intensity (SI) of the perilymphatic space is too low to show EH. Using ZOOMit and T2Prep can improve the SI (12,15), yet no study has examined whether 3D-ZOOMit real IR with T2Prep can clearly visualize EH and shorten the delay interval.

Thus, we hypothesized that combining optimized 3D-ZOOMit SPACE real IR with a specific T2Prep (otz-3D real IR) and long TR would shorten the delay interval and scan time with sufficient and homogenous PE while providing high reliability for the grading of EH and assessing blood-labyrinth barrier (BLB) impairment. We compared the signal intensity ratio (SIR), contrast-to-noise ratio (CNR), signal-to-noise ratio (SNR), scores of the overall image quality, the separation of endolymph and perilymph, and EH grade across three different delay intervals. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-179/rc).

Methods

Patients

The Institutional Review Board of Shandong Second Provincial General Hospital approved this single-center prospective imaging study (No. 20220240) and was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. Written informed consent was obtained from all participants. This study included 43 consecutive participants with unilateral SSNHL (18) or MD (19) who visited the Outpatient Department of Shandong Second Provincial General Hospital from September 2022 to December 2022. Patients were excluded from the study if they met any of the following exclusion criteria: (I) trauma, neoplasm, or inflammation of the temporal bone; (II) previous temporal bone surgery, chemotherapy, or treatment with other immunosuppressive drugs; (III) MR-related contraindications; and/or (IV) significant image artifacts (e.g., motion artifacts or susceptibility artifacts affecting >50% of inner ear structures or obscuring the relative contrast of the endolymph and perilymph).

MRI examinations

MRI examinations were carried out with the MAGNETOM Prisma 3-T scanner (Siemens Healthineers, Erlangen, Germany) with a 64-channel array head and neck coil. To acquire a strong and homogenous PE in postcontrast otz-3D real IR, all the participants underwent IV injections of a double dose (0.4 mL/kg body weight) of gadoteridol (ProHance, Bracco, Milan, Italy) according to previous research (6,12,20). Subsequently, all participants underwent otz-3D real IR 2 hours, 4 hours, and 6 hours after IV-Gd (12). The optimal scanning parameters of the otz-3D real IR were as follows: TI, 2,100 ms; TR, 9,500 ms; echo time, 547 ms; T2Prep, 200; turbo factor, 192; matrix size, 320×160; bandwidth, 306 Hz; field of view, 18 cm × 169 cm; voxel, 0.3×0.3×1.0 mm³; and reconstruction, real. The scan time was 7 minutes and 17 seconds. The T2Prep duration (200 ms) was selected after comparative testing of 100, 150, and 200 ms durations, with 200 ms demonstrating optimal separation between the endolymphatic and perilymphatic spaces (15). Additionally, a TI of 2,100 ms was determined to be optimal for distinguishing these compartments (15). The TR (9,500 ms) was optimized through parametric comparisons (TR range, 8,000–10,000 ms), with 9,500 ms providing maximal perilymph-to-endolymph contrast and Gd sensitivity, respectively (16).

Qualitative analyses

All MRI scans were independently and blindly assessed by two radiologists with 12 and 17 years of experience in inner ear imaging, respectively. Images, patient identifiers, and scan timing data were anonymized, with image presentation order randomized, and all sequences were presented individually and randomized to both readers and not per patient in pairs. The time interval between the two readings was at least 1 week. The radiologists assessed the overall image quality and the separation of endolymph and perilymph in terms of score and graded the cochlear EH (C-EH) and vestibular EH (V-EH) in the same session.

Poor, sufficient, good, and excellent overall image quality for diagnosis were scored as 1, 2, 3, and 4, respectively, based on a 4-grade subjective quality rating score (21): a score of 1 indicated that less than a quarter of the inner margin was visible, a score of 2 indicated that a quarter to half of the inner margin was visible, a score of 3 indicated that half to three-quarters of the inner margin was visible, and a score of 4 indicated that more than three-quarters of the inner margin was visible. None, some, most, and all separation of endolymph and perilymph in the inner ear were scored as 1, 2, 3, and 4, respectively (12,22).

To grade EH, the method proposed by Li et al. (12) based on the classification system of Bernaert et al. (23) was used. The C-EH was graded as none, I, or II, while the V-EH was graded as none, I, II, or III. Visually increased PE, suggesting BLB impairment, was defined as a higher SI of the cochlear basal turns compared with that of the contralateral ear (23,24).

Quantitative analyses

According to previously published methods (12,22,24), two radiologists each measured all participants’ SI. In brief, a 1-mm² circular region of interest (ROI) was set on the scala tympani of the cochlear basal turn’s center (SI_peri) and utricle (SI_endo), respectively; moreover, a 10-mm² circular ROI was set in the left middle cerebellar peduncle (SI_lmcp). The standard deviation (SD) of a 6-mm² circular ROI in the ipsilateral external auditory canal was defined as noise (SD_noise).

The average SIs or SDs were calculated from two measurements by two radiologists and used to calculate the SIRs (serving as quantitative indicators of PE and BLB impairment), CNRs, and SNRs via the following equations (12):

SIR=SIperi/SIlmcp[1]

CNR=(SIperi−SIendo)/SDnoise[2]

SNR=SIperi/SDnoise[3]

Statistical analyses

Statistical analyses were performed with SPSS version 25.0 (IBM Corp., Armonk, NY, USA), MedCalc version 18.2 (MedCalc Software, Ostend, Belgium), and GraphPad Prism version 8.0.2 (Dotmatics, Boston, MA, USA) software. A repeated-measures analysis of variance or the Friedman test was used for the qualitative and quantitative analyses. Normality was assessed via Shapiro-Wilk tests; repeated-measures analysis of variance was applied for parametric data that satisfied a normal distribution, while the Friedman test was used for nonparametric ordinal scores or for parametric data that did not satisfy the normal distribution. For qualitative and quantitative analyses, interobserver agreement was tested with weighted kappa (κ) statistics, interclass correlation coefficients (ICC), or Bland-Altman plots. The statistical significance level was set at P<0.05.

Results

Demographic characteristics of the participants

In total, 43 consecutive participants with unilateral SSNHL or MD were initially recruited for the study; however, 12 participants were excluded due to image artifacts (n=4), an internal auditory canal tumor (n=1), or incomplete scans at 6 hours after IV-Gd (n=7) (Figure 1). Thus, 31 consecutive participants were included in the analysis and underwent otz-3D real IR scanning at three postinjection intervals, respectively (Table 1).

Figure 1 Flowchart of participant enrollment in this study. 3D-real IR, three-dimensional real inversion recovery; MD, Ménière’s disease; SSNHL, sudden sensorineural hearing loss.

Qualitative analysis

The scores and EH grades between the two radiologists showed good agreement (all kappa values >0.75). Significant differences were observed among the three postinjection intervals for the scoring of overall image quality and the separation of the endolymph and perilymph (all P values <0.001; Tables 2,3). The post hoc analyses revealed that for otz-3D real IR, the overall image quality at 4 hours after IV-Gd was superior to that at 2 hours (pairwise comparison P<0.001), as was the separation of asymptomatic cochlear endolymph and perilymph (pairwise comparison P=0.04). Superior results were also observed 6 hours after IV-Gd (compared with those at 2 hours) in terms of overall image quality (pairwise comparison P<0.001) and the separation of affected and asymptomatic cochlear endolymph and perilymph (both pairwise comparison P values <0.001). No significant differences in these scores were observed between 4 and 6 hours after IV-Gd on otz-3D real IR images (pairwise comparison P>0.99 for overall image quality; pairwise comparison P=0.30 and P=0.38 for the separation of affected and asymptomatic cochlear endolymph and perilymph, respectively; and pairwise comparison P>0.99 and P=0.90 for the separation of affected and asymptomatic vestibular endolymph and perilymph, respectively), and the evaluations of the affected C-EH and V-EH did not differ significantly across the three postinjection intervals (P=0.37 and P>0.99, respectively) (Table 4 and Figure 2).

Figure 2 Axial optimized 3D-ZOOMit SPACE real inversion recovery with T2 preparation images at (A) 2 h, (B) 4 h, and (C) 6 h after the IV-Gd from a patient with definite unilateral right-sided Ménière’s disease. Visually increased perilymphatic enhancement of the cochlear basal turn was observed on the right side (arrowheads) after IV-Gd with a higher signal intensity than that on the left side (large arrow); the images were comparable at delay intervals of 2, 4, and 6 h. Grade II cochlear endolymphatic hydrops (small arrows) was easily diagnosed at delay intervals of 2, 4, and 6 h, with equal scores for the separate visualization of the endolymphatic and perilymphatic space. Note that the signal intensity of the cochlear basal turn on the left side (large arrow) increased gradually at 2, 4, and 6 h. 3D-ZOOMit, three-dimensional zoomed imaging technique with parallel transmission; IV-Gd, intravenous administration of gadolinium; SPACE, sampling perfection with application-optimized contrasts using different flip-angle evolutions.

Quantitative analysis

The SIs between the two radiologists showed good agreement (all ICCs >0.75; Figure 3). The CNR, SNR, and SIR of the affected side were 56.51±17.05, 38.08±10.61, and 15.05±4.52 at 2 hours, respectively; 65.26±23.66, 46.05±15.30, and 17.26±5.33 at 4 hours, respectively; and 75.31±19.71, 53.71±14.01, and 18.27±4.73 at 6 hours, respectively. The CNR, SNR, and SIR of asymptomatic side were 42.72±11.41, 30.69±8.88, and 12.26±4.19 at 2 hours, respectively; 46.59±12.01, 36.69±10.98, and 14.29±4.73 at 4 hours, respectively; and 60.10±14.01, 46.25±13.20, and 15.20±3.90 at 6 hours, respectively. The SIRs, CNRs, and SNRs differed significantly across the three postinjection intervals (all P values <0.001; Figures 4,5). The post hoc analyses revealed that except for the CNRs of the asymptomatic inner ear, the CNRs, SIRs, and SNRs of the otz-3D real IR were significantly higher at 4 hours than at 2 hours after IV-Gd (all pairwise comparison P values <0.001). Meanwhile, the SIRs, CNRs, and SNR were significantly higher at 6 hours than at 2 hours after IV-Gd (all pairwise comparison P values <0.001); the CNR, SNR, and affected SIR parameters were also higher at 6 hours than at 4 hours after IV-Gd (pairwise comparison P=0.002 and P<0.001 for the affected and asymptomatic CNR, respectively; pairwise comparison P=0.001 and P<0.001 for the affected and asymptomatic SNR, respectively; and pairwise comparison P=0.03 for the affected SIR). Conversely, there was no significant difference in asymptomatic SIR at 4 hours and 6 hours (pairwise comparison P=0.13).

Figure 3 Bland-Altman plot showing agreement analysis between radiologist 1 and radiologist 2 in the measurement of (A₁-A₃) the signal intensity on the affected side of the utricle, (B₁-B₃) the scala tympani of the cochlear basal turn’s center, and (C₁-C₃) the left middle cerebellar peduncle, respectively (n=31). SD, standard deviation; SI_endo, signal intensity of endolymph; SI_lmcp, signal intensity of left middle cerebellar peduncle; SI_peri, Signal intensity of perilymph.

Figure 4 The whisker plot of CNR, SNR, and SIR made on GraphPad Prism. (A,C,E) The CNR, SNR, and SIR of the affected side, respectively. (B,D,F) The CNR, SNR, and SIR of the asymptomatic side, respectively. ns, P>0.05; *, P<0.05; **, P<0.01; ***, P<0.001. CNR, contrast-to-noise ratio; SIR, signal intensity ratio; SNR, signal-to-noise ratio.

Figure 5 Axial optimized 3D-ZOOMit SPACE real inversion recovery with T2 preparation images at (A) 2 h, (B) 4 h, and (C) 6 h after the intravenous administration of gadoteridol from a patient with definite unilateral right-sided Ménière’s disease. (A-C) at the level of the middle and apical turn of the cochlea, as well as the saccule and utricle. Grade II cochlear endolymphatic hydrops (arrows) and vestibular III (arrowheads) were easily diagnosed at a delay interval of 2, 4, and 6 h, with equal scores for the separate visualization of the endolymphatic and perilymphatic space. 3D-ZOOMit, three-dimensional zoomed imaging technique with parallel transmission; SPACE, sampling perfection with application-optimized contrasts using different flip-angle evolutions.

Discussion

In this study, adding T2Prep with a long TR to the 3D ZOOMit SPACE real IR sequence shortened the delay interval and scan time, provided sufficiently strong and homogenous PE, and demonstrated high consistency for evaluating EH and assessing BLB impairment.

This otz-3D real IR sequence reduced the scan time to 437 seconds, which was much shorter than the 559–920 seconds reported for studies on 3D-real IR (5,7,10,11). The ZOOMit technique is faster than is the conventional TSE sequence, as it creates a zoom effect during MRI to generate high-quality images (25,26). The 3D SPACE sequence also facilitates the faster acquisition of thin continuous slices. Moreover, the maximum adjustment of the optimized sequence reduced the read resolution from 100% to 53%, significantly shortening the acquisition time. Therefore, the scan time of the sequence based on SPACE was significantly shorter than that of conventional sequences reported in a previous study (27). Consequently, combining ZOOMit with SPACE and using 3D-real IR results in faster screening (25,28).

Furthermore, the delay interval between IV-Gd and post-contrast otz-3D real IR acquisition was shorter than that previously reported (6,11,14). It matched that of a recent study in which the authors concluded that the delay interval could be shortened from 4 hours to 2 hours through use of 3D-FLAIR while retaining very high reliability for evaluating the EH and BLB impairment (16). Moreover, it has been reported that MRI can detect the Gd signal at 1.5 hours but is significantly weaker than that at 3, 4.5, and 6 hours after IV-Gd (29,30). However, T2Prep might increase the SI of the low-concentration Gd in the perilymphatic space at a 2-hour-delay interval. Moreover, previous research has shown that T2Prep increases PE and contrast between the endolymphatic and perilymphatic space (15,31), and this contrast enhancement helps to shorten the delay interval. In another study, 3D-real IR based on SPACE with a longer TR was sensitive to low Gd concentrations (10), resulting in the successful visualization of EH after IV-Gd at a shorter delay interval.

The CNRs, SNRs, and SIRs are growing significantly higher for all affected ears as time progresses (16,32). However, in our study, C-EH and V-EH detection did not differ across the three delay intervals, nor did the scores for overall image quality and endolymph visualizations between 4 hours and 6 hours or those for affected endolymph visualization between 2 hours and 4 hours. This suggests that the contrast between the endolymphatic and perilymphatic space was sufficient at 2 hours, allowing for their separate visualization. Indeed, there was excellent interobserver consistency for endolymph scoring and EH evaluation. However, Naganawa et al. did not recommend a delay interval of 1.5 hours over 3, 4.5, and 6 hours due to the abnormal enlargement of the ratio of the area of the endolymph at that time (29). Conversely, Barlet et al. (16) reported equivalent volumes for the saccule and utricle at 2 hours and 4 hours after IV-Gd. This discrepancy might be explained by the potential misregistration and postprocessing of hydrops used by Naganawa et al. (29). Nevertheless, 3D real IR can differentiate the endolymph from perilymph and the surrounding bone without postprocessing and potential misregistration (5,10), making it superior to hydrops and 3D-FLAIR. Although a 4-hour-delay yielded a higher CNR in our study, the 2-hour-delay achieved comparable diagnostic accuracy and improved workflow efficiency. Therefore, the diagnosis of EH and BLB at a 2-hour-delay interval is feasible and reliable.

Due to its shorter delay interval and scan time, the protocol examined in this study can be easily applied in clinical settings. Reducing the above-mentioned times might improve acceptability among patients and increase the number of patients scanned per day. In turn, this would allow for the development of more refined treatment strategies for a number of patients.

This study involved several limitations that should be addressed. First, the sample size was small, which limited the accuracy of the statistical results. Post hoc power analysis demonstrated that our sample size (N=31) achieved a statistical power of 0.82 for detecting interinterval differences in CNR, exceeding the conventional threshold of 0.8 for adequate sensitivity. Although the sample size may appear modest, these results suggest robust detection capability for clinically relevant effect sizes. Second, unlike in other studies of EH involving in vivo imaging, EH was not confirmed pathologically (4-6), and MRI of animal or human temporal bone specimens might provide further insights. Third, all the participants were recruited from a single center and underwent 3.0-T MRI under similar device settings. Thus, future multicenter studies with standardized protocols across different 3.0-T MR platforms are needed to validate our findings. Additionally, attempts should be made to use a similar 3D-real IR sequence on a 1.5-T MRI device, which is commonly used in clinical practice, with a shorter delay interval and scan time. Fourth, our reliance on visual grading, despite its high interrater agreement, constitutes another methodological limitation. Although semiquantitative grading suffices for clinical diagnosis, it inherently depends on subjective interpretation. For instance, borderline cases between EH grades I and II may be inconsistently classified, potentially affecting treatment decisions. Recent studies have demonstrated the superiority of volumetric analysis in reducing such subjectivity; for instance, it was reported that the endolymph-to-perilymph volume ratio provides continuous numerical data that better captures subtle hydrops changes (33,34). However, volumetric methods require specialized postprocessing software (e.g., ITK-SNAP) and a significantly longer analysis time. Similar to prior feasibility studies on novel MRI sequences (10,12), we focused on protocol optimization first, leaving volumetric validation for subsequent technical development. Future multicenter studies should combine our shortened protocol with automated volumetry tools to achieve both efficiency and objectivity, although our visual grading approach remains to be clinically validated and widely adopted. Finally, image coregistration was not performed but represents a valuable avenue for future research.

Conclusions

The optimized 3D ZOOMit SPACE real IR sequence with T2Prep and a long TR at a delay interval as short as 2 hours was found to be reliable in detecting EH. The 437-second scan time for this sequence was shorter than those previously reported for 3D-real IR and provided excellent reliability for evaluating EH and assessing BLB impairment.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-179/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-179/dss

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-179/coif). M.X.L. is from Diagnostic Imaging, Siemens Healthineers Ltd, Shanghai, China. 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. The Institutional Review Board of Shandong Second Provincial General Hospital approved this single-center prospective imaging study (No. 20220240). All participants gave written informed consent before the study. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

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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(English Language Editor: J. Gray)