Diffusion-weighted imaging as a non-gadolinium alternative for immediate assessing nonperfused area of adenomyosis after magnetic resonance-guided focused ultrasound (MRgFUS) ablation: a potential technique but with slightly overestimate

Introduction

Over the past two decades, magnetic resonance-guided focused ultrasound (MRgFUS) has emerged as a promising noninvasive treatment for various benign and select malignant lesions (1). Preclinical studies show its ability to precisely focus ultrasound energy on targeted areas, converting acoustic power to heat to ablate tissue without harming surrounding structures (2,3). The precision of this process, achieved at temperatures above 56 ℃, underscores its feasibility and effectiveness. Recently, MRgFUS has emerged as a novel treatment option for adenomyosis, offering precision targeting and ablation with real-time magnetic resonance (MR) guidance, further enhancing its appeal as a noninvasive treatment modality. However, some patients do not achieve satisfactory long-term clinical outcomes following MRgFUS treatment for adenomyosis (4). Previous study has shown that higher clinical success rates can be achieved in patients with a larger nonperfused volume (NPV) ratio (5). Therefore, accurate identification of lesions requiring ablation during treatment can help to improve the ratio of ablation. Currently, the imaging gold standard for detecting the necrotic zone of lesions following MRgFUS ablation is NPV, and evaluation of NPV is typically performed with T1-weighted MR imaging after administration of a gadolinium-based contrast agent (5-7). However, contrast-enhanced (CE) imaging is limited for intraoperative guidance of MRgFUS due to some safety concerns associated with the use of gadolinium-based contrast agents (6,8). These agents are currently only recommended for use at the end of treatment and cannot be repeatedly administered during the treatment procedure. Consequently, there is a necessity to explore non-gadolinium alternative in order to improve efficacy and efficiency (7).

In recent years, various studies have demonstrated that diffusion-weighted imaging (DWI) can detect the ablated lesions of uterine fibroids following focused ultrasound treatment (9-11). This technique does not necessitate the use of gadolinium-based contrast agents, thereby rendering it suitable for repeated use during treatment. Similar to patients with uterine fibroids, an increasing number of patients with adenomyosis are seeking MRgFUS therapy to alleviate their clinical symptoms (3,12-14). Nevertheless, MRgFUS ablation of adenomyosis lesions is more challenging than MRgFUS ablation of fibroids, and the NPV is always lower (14,15). A higher ratio of residual lesions may be a significant contributor to unsatisfactory clinical symptom improvement and high recurrence rates (5). It is therefore of great importance to investigate nongadolinium methods that are suitable for intraoperative monitoring to enhance the NPV ratio in MRgFUS ablation of adenomyosis lesions. The study of Cui et al. showed that DWI can replace CE imaging for assessment of the therapeutic efficacy of high-intensity focused ultrasound (HIFU) ablation for treatment of adenomyosis (16). However, because MR examinations could not be performed on HIFU treatment-table, their study only reflected changes of necrotic lesions in approximately one day. In general, intraoperative monitoring methods should be capable of reflecting hyperacute changes within one hour after thermal ablation. To the best of our knowledge, no study has been conducted on the use of nongadolinium techniques for immediate (<1 hour after ablation) assessment of MRgFUS ablation results of adenomyosis lesions. In this study, we compared DWI using 3.0-T MR on the treatment-table within 15 minutes after MRgFUS ablation of adenomyosis lesions with gadolinium-enhanced T1-weighted imaging. The aim was to evaluate the value of DWI in the immediate assessment of necrotic lesions after MRgFUS ablation of women with adenomyosis. We present this article in accordance with the GRRAS reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-453/rc).

Methods

Patients

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Ethics Committee of Foshan Hospital of Traditional Chinese Medicine (No. KY-266-1) and informed consent was taken from all the patients. Our single institution retrospective study analyzed the clinical data of patients who received MRgFUS treatment for adenomyosis from January 2019 to June 2022. The inclusion criteria were as follows: (I) female patients aged between 18 and 55 years old who were not in menopause; (II) patients with symptomatic adenomyosis confirmed by clinical and magnetic resonance imaging (MRI), and a maximum lesion diameter ≥3.0 cm; (III) patients who underwent MRgFUS treatment; and (IV) patients who underwent DWI and CE T1-weighted examination immediately after treatment. Patients who met any of the following criteria were excluded from the study: (I) prior uterine artery embolization or ablation treatment; (II) discontinuation of treatment; (III) missing DWI and/or CE MR examination data; and (IV) poor image quality on DWI and/or CE T1-weighted imaging resulting in the inability to observe or measure.

MRgFUS treatment

MRgFUS ablation was performed using a focused ultrasound system (ExAblate2100, InSightec) guided by a 3-T MR system (Discovery 750 W, GE Healthcare, IL, USA) that was equipped with a phased-array T/R body coil for pelvis examination. Patients assumed a prone position on the treatment table, which is suitable for both MRI scans and focused ultrasound surgery. The physician first delineated the treatment region, and then the computer divided the region into separate sonication spots. The physician proceeded to target the adenomyosis lesion using sonication, one spot at a time, under the supervision and guidance of MR imaging. Upon complete ablation of all designated sonication spots, the treatment was considered to be finished.

MRI immediately after treatment

Since CE MR imaging is not recommended if MRgFUS ablation has not been completed (6,8), we only obtained DWI and CE scans immediately after ablation at the last sonication spot. The MR system and body coil for MRgFUS were also utilized to conduct MR imaging on the treatment table. DWI and CE MR imaging were completed using the same position center within 15 minutes after MRgFUS treatment. In this study, we employed the reduced field-of-view (rFOV) technique for DWI, with a single b-value of 800 sec/mm², based on our experience and previous study (10). The other scanning parameters were as follows: sequence, single-shot echo-planar imaging (ss-EPI); repetition time (TR)/echo time (TE), 4,000.0 ms/72.1 ms; field of view (FOV), 36.0 cm × 18.0 cm (half in the phase coding direction); frequency direction, R/L; section thickness/intersection gap, 5 mm/1 mm; voxel size, 2.2 mm × 2.2 mm × 5.0 mm; number of excitations, 12; and acquisition time, 2 min 28 sec. The gadolinium-based contrast agent gadoteric acid meglumine (Hengrui Pharmaceutical, Lianyungang, China; 0.1 mmol/kg) was administered intravenously for CE MR imaging and then triplanar FSPGR T1-weighted series imaging. For the purposes of comparison, only axial-plane images of DWI and CE were utilized. The scanning parameters of axial T1-weighted imaging were as follows: TR/TE, 250.0 ms/1.9 ms; FOV, 36.0 cm × 36.0 cm; frequency direction, R/L; section thickness/intersection gap, 5 mm/1 mm; voxel size, 1.4 mm × 2.8 mm × 5.0 mm; number of excitations, 2; and acquisition time, 1 min 6 sec.

MR imaging evaluation

The nonenhanced zone of CE T1-weighted imaging was defined as the nonperfused area after MRgFUS treatment (6,7). The images of T1-weighted and DWI were anonymized and downloaded in DICOM format and randomly numbered. Two experienced radiologists (observer 1 and observer 2), with >20 years of experience, were blinded to analyze the images, respectively. Since the maximum slice image is the foundation for observation, a simplified method for the observation and measurement of lesions was employed in this study, utilizing the image of the maximum slice. One radiologist (observer 1) imported the images into the picture archiving and communication system (YLZ Information Technology, Xiamen, China). The observer first determined the presence of abnormal signals on the DWI images and then categorized the type of abnormal signals. The classification criteria were as follows (Figure 1): type 1, a large area of central low-signal with a complete high-signal ring; type 2, a large area of central low-signal with an incomplete high-signal ring; and type 3, inhomogeneous high-signal areas without a ring sign. Finally, the observer independently determined the boundaries of the ablated necrotic lesion on images by tracing along the boundaries using the “area measurement” tool of the workstation and then calculated the maximum area of the ablative lesion (Figure 2). The DWI or CE MR images were measured independently according to random numerical order. The assessment was repeated by the same radiologist 2 weeks later to verify intraobserver consistency. Another radiologist (observer 2) used the same method to assess the ablated necrotic lesion to verify interobserver consistency. The two observers determined the final classification of the lesion on DWI scans after discussing discordant lesions. The final data for the area measured by DWI and CE images were the average of three measurements taken by the observers.

Figure 1 DWI and CE T1-weighted imaging of ablative necrotic lesions of adenomyosis after MRgFUS ablation. The abnormal signals observed in DWI can be classified into three types. (A) Type 1, a large area of central low-signal with a complete high-signal ring; (B) corresponding CE imaging of (A); (C) type 2, a large area of central low-signal with an incomplete high-signal ring; (D) corresponding CE imaging of (C); (E) type 3, inhomogeneous high-signal areas without ring signs. The DWI abnormal signals and nonperfused areas are essentially corresponding; (F) corresponding CE imaging of (E). DWI, diffusion-weighted imaging; CE, contrast-enhanced; MRgFUS, magnetic resonance-guided focused ultrasound.

Figure 2 Comparison of area measurements for DWI and CE imaging. (A) Area measured using DWI was 16.18 cm² (the area outlined by the white curve below the number 1). (B) Corresponding area measured using DWI was 14.32 cm² (the area outlined by the white curve below the number 1). DWI, diffusion-weighted imaging; CE, contrast-enhanced.

Statistical analysis

Continuous variables were expressed as the mean ± standard deviation or median and interquartile range. Categorical variables were expressed as numbers and percentages. Continuous variables were compared using the t-test or paired Wilcoxon signed-rank test. Categorical variables were compared using the Chi-squared test. The intraclass correlation coefficient (ICC) was used to analyze the intraobserver and interobserver consistency and to evaluate the consistency between DWI and CE measurements of the necrotic area. Consistency was categorized as poor (<0.50), moderate (0.51–0.75), good (0.76–0.90), or excellent (0.91–1.00). We performed statistical analysis using IBM SPSS Statistics software (version 22; IBM Corporation). For all analyses, a P value of <0.05 was deemed statistically significant.

Results

Patients and adenomyosis

A total of 48 adenomyosis lesions in 48 Chinese female patients (mean age 39.6±4.9 years, range from 30 to 51 years) were analyzed. The mean body mass index (BMI) was 22.3±3.2 kg/m². Twenty-five (52.1%) had focal adenomyosis lesions, and twenty-three (47.9%) had diffuse adenomyosis lesions. All adenomyotic lesions were subjected to MRgFUS treatment, and the NPV was 55.2±43.7 cm³. The NPV of focal adenomyosis lesions was smaller than that of diffuse adenomyosis lesions (37.7±21.5 vs. 74.2±53.4 cm³, P=0.003).

Imaging findings of DWI

In DWI images, abnormal signal areas were shown in all 48 adenomyosis lesions and could be visually recognized by the two observers. The DWI abnormal signals and nonperfused areas were essentially corresponding. The two observers’ classification of lesion signal types on the DWI images is presented in Table 1. Upon comparison of observer 1’s first and second categorization, 6 (12.5%) lesions were judged inconsistently, including three focal and three diffuse adenomyosis lesions. Furthermore, 6 (12.5%) lesions were found to be inconsistently classified when observer 1’s first classifications was compared to observer 2’s. This included 4 focal and 2 diffuse adenomyosis lesions.

As illustrated in Table 2, following a discussion of discordant lesions by the two observers, the prevalence of lesions categorized as types 1, 2, and 3 on DWI images was found to be 20.8% (10 of 48), 31.3% (15 of 48), and 47.9% (23 of 48), respectively. There was no significant difference in the distribution of focal and diffuse lesions on DWI (P=0.167). The reliability of classifying ablated areas according to lesion type on DWI is presented in Table 3. The intra- and interobserver classifications of overall lesions, focal lesions, and interobserver classification of diffuse lesions exhibited ICC values exceeding 0.75, with the exception of the intraobserver ICC for diffuse lesions, which was 0.74 (all P<0.001).

Comparisons of DWI and CE area measurements

Table 4 also demonstrates the consistency of DWI and CE for measuring nonperfused area across observers. The ICC values for the comparison of the 3 measurements were 0.85, 0.91, and 0.87, respectively (all P<0.001). A subgroup analysis showed that the ICCs for focal lesions ranged from 0.89 to 0.91, while those for diffuse lesions ranged from 0.80 to 0.89 (all P<0.001).

A comparison was conducted between the area of nonperfused lesions measured by DWI and CE images. A significant difference was observed between DWI and CE image measurements (17.17±7.79 vs. 15.41±7.36 cm², P<0.001). A subgroup analysis showed that the area of both focal and diffuse lesions measured by DWI images was also larger than that measured by CE images (Table 5). Figure 3 presents scatter plots of area measurements using CE and DWI images, indicating a significant correlation between the measurements of the two techniques (R=0.91, P<0.001).

Figure 3 The scatter plots and regression lines illustrate the associations between the average area measured using CE MR imaging and DWI. The dashed lines indicate the 95% confidence interval. DWI, diffusion-weighted imaging; CE, contrast-enhanced; MR, magnetic resonance.

Discussion

For a long time, monitoring ablation outcome during MRgFUS treatment using a non-gadolinium technique poses a technical challenge (10,17,18). In this study, we investigated the value of DWI in evaluating the immediate outcomes of MRgFUS ablation of adenomyosis lesions. The results have the potential to provide non-gadolinium guidance for assessing the ablation result during MRgFUS treatment.

In the present study, we conducted the DWI examination using a single b-value. The implemented protocol provides several advantages, positioning DWI as a promising technique for intraoperative monitoring of MRgFUS ablation. Specifically, a b-value of 800 sec/mm² was employed. It may be possible to achieve a more optimal balance between image quality and display capability (16). A single b-value reduces the time required for the scan and eliminates the necessity for extensive postprocessing, rendering it an appropriate choice for dynamic monitoring during treatment. In addition, these images can be conveniently imported into the treatment workstation, where they can be utilized to assist in planning and guiding treatment.

Similar to previous studies on uterine fibroids (9-11), our study on adenomyosis demonstrated that DWI could detect abnormal signals in the ablation area, which were essentially corresponded with nonperfused areas of CE T1-weighted imaging. However, in contrast to the single pattern of nonenhancement displayed by CE MR imaging, the finding of an ablated lesion is more complex on DWI (9-11). Histology revealed coagulative necrosis in the targeted tissues after focused ultrasound thermal ablation, in addition to hyperemia, edematous swelling, hemorrhage, and an inflammatory reaction (19-21). It is hypothesized that within coagulative necrotic areas, the DWI hyperintense areas may be indicative of cytotoxic edema, which is associated with early ischemia and limited diffusion of surrounding water molecules (10). Conversely, the low signal may be associated with water liberation following cell membrane rupture and intense tissue damage (20,22). In the present study, the abnormal signals identified by DWI were categorized into three types: central hypointense lesions with a complete hyperintense peripheral ring in 10 (20.8%) out of 48 lesions, central hypointense lesions with an incomplete hyperintense peripheral ring in 15 (31.3%) lesions, and inhomogeneous hyperintense lesions without a ring in 23 (47.9%) lesions. The present study found high levels of intra- and interobserver agreement in identifying abnormal signals, with ICC values of 0.84 and 0.80, respectively. This indicates that the use of a straightforward typing method could assist physicians in initially identifying ablated necrotic areas without the necessity for CE MR imaging (10).

To confirm the accuracy of DWI in revealing necrotic lesions on ablation, we conducted a further comparison between DWI and CE in measuring the area of necrotic lesions. Our study of adenomyosis showed high consistency between measurements using DWI and CE images, suggesting that, similar to previous studies on leiomyoma (10,11) and adenomyosis (16), DWI can be an important complement to CE MR. Since gadolinium is not necessary, DWI can serve as a substitute for CE MR imaging due to its suitability for repeated intraoperative monitoring. Furthermore, our research demonstrated that DWI may overestimate the extent of ablation of the necrotic lesion compared with CE T1-weighted imaging, both overall and in different types of adenomyosis lesions. A similar overestimation was observed in the study of uterine fibroids by Liao et al. (10). However, the interpretation of peripheral high signals displayed by DWI can be intricate, as they are associated not solely with genuine necrosis but also with hyperemia, edema, or the T2 shine-through effect (23-26). Emerging evidence suggests that DWI is more influenced by T2 than by diffusion alone (25,26). Wáng et al. proposed a potential triphasic relationship between T2 and DWI (26). Therefore, it is crucial to carefully consider factors such as baseline perfusion and post-treatment edema in DWI analyses, as these can elevate the T2 relaxation time, making it difficult to distinguish from genuine coagulation necrosis. Although the overestimation was slight (17.17±7.79 vs. 15.41±7.36 cm², overall), it is important to consider this when evaluating the results of MRgFUS ablation, especially when determining the final NPV ratio.

It is important to note that the narrowed field-of-view ss-EPI DWI employed in this study is prone to various influences, such as motion, convolution artifacts, magnetic field inhomogeneity, and uneven fat suppression (27,28). Our study cohort comprised Chinese women with petite body frames and a mean BMI of 22.3 kg/m². Within this context, DWI generally yielded satisfactory fat suppression, reduced convolution artifacts, and superior image quality. However, it remains uncertain whether a comparable assessment can be achieved in women with a higher BMI, as their pelvises tend to have a greater fat content, necessitating a wider field of view. Given the scarcity of women with a higher BMI in our recruitment, we are unable to substantiate this supposition. In future research, it would be advantageous to gather a more diverse cohort, including women with a higher BMI, especially non-Asian women, and to further investigate the adaptability of DWI across different BMI levels. Additionally, exploring modified pelvic DWI techniques may enhance image quality, meriting further scrutiny (27,28).

One limitation of this study was that only one b-value was empirically used, and the apparent diffusion coefficients value was not obtained. Therefore, future study with different b-value combinations and apparent diffusion coefficients will be necessary to clarify which metric best predicts the necrotic tissue size. Secondly, DWI was performed only at the end of MRgFUS treatment, which did not allow us to observe the dynamic changes during the treatment process. This aspect also necessitates further study. Furthermore, the Dice score is a pivotal metric in the field of medical imaging. It is a reliable indicator of the similarity between different intra- and interobserver contours, as well as the contours in DWI and CE MR images. In our current study, the Dice score could have provided us with valuable insights into the level of agreement between observers and the congruence between the two imaging techniques. However, owing to technical constraints and limitations within our research framework, we were unable to fully leverage this metric. This gap in our analysis necessitates a refinement of our methodology in future endeavors to ensure a more comprehensive and accurate evaluation of the results. Moreover, our institution currently only approves MRgFUS for patients with adenomyosis aged 18 to 55 years. Consequently, we had not included symptomatic patients younger than 18 years or postmenopausal patients. Given the potential for specific clinical and MR manifestations in this group of patients (29,30), the evidence for the applicability of DWI assessment needs to be further summarized when future treatments are performed.

Conclusions

In conclusion, DWI can serve as a non-gadolinium technique for the initial evaluation of nonperfused area of adenomyosis after MRgFUS ablation due to its effective display and good agreement with CE MR imaging. However, it is also important to note that DWI may slightly overestimate the nonperfused areas.

Acknowledgments

We would like to express deep thanks to the staff from the center of MRgFUS and department of gynecology at our hospital, for their support on our research.

Funding: This work was supported by Foshan Science and Technology Bureau Medical Research Plans (No. 2320001006633). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Footnote

Reporting Checklist: The authors have completed the GRRAS reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-453/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-453/coif). The 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 study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Ethics Committee of Foshan Hospital of Traditional Chinese Medicine (No. KY-266-1) and informed consent was taken from all the patients.

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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