Magnetic resonance imaging evaluation and analysis of influencing factors of early uterine seromuscular layer injury after high-intensity focused ultrasound ablation of uterine fibroids

Introduction

Among benign tumors in the female reproductive system, uterine fibroids are the most common (1). Traditional treatments for uterine fibroids, including surgery, medications, and uterine artery embolization (2,3) are effective in alleviating symptoms, but these approaches carry potential risks such as infection, post-embolization syndrome, and permanent amenorrhea (4). In contrast, high-intensity focused ultrasound (HIFU) ablation is a non-invasive technique that employs focused ultrasound waves under imaging guidance to precisely target fibroid tissue. By rapidly increasing the local temperature to 60–100 ℃, HIFU induces coagulative necrosis in the treated tissue (5). At present, HIFU has gained widespread application in the treatment of uterine fibroids due to its non-invasive nature and validated efficacy (6-8). Magnetic resonance imaging (MRI), with its ability to provide high-resolution soft tissue imaging, radiation-free operation, and multi-sequence scanning, is a valuable tool for evaluating fibroids. It enables detailed assessment of their location, size, and vascular features (9). Thus, MRI is widely employed in preoperative diagnosis, as well as in evaluating therapeutic outcomes and safety following treatment of uterine fibroids. Previous studies (10,11) have investigated factors that may cause abdominal and pelvic floor fascial injury by HIFU, but there is limited research on the impact of HIFU on the seromuscular layer. A study (12) showed that some patients exhibit seromuscular-layer injury on early MRI images after HIFU treatment. This study investigates the influencing factors of seromuscular-layer injury to provide a reference basis for timely clinical intervention. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1062/rc).

Methods

Study population

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study received ethical approval from the Ethics Committee of Yongchuan Hospital of Chongqing Medical University, Chongqing, China (approval No. 2024LLS005). As the study was retrospective in design, the requirement for informed consent was waived. A total of 194 patients clinically diagnosed with uterine fibroids and treated with HIFU at Yongchuan Hospital of Chongqing Medical University between January 2021 and December 2023 were included in the analysis. The patients’ ages ranged from 22 to 59 years, with a mean age of 43.5±7.2 years. All participants underwent MRI examinations both before the procedure and within three days afterward. The inclusion criteria were as follows: (I) patients were not pregnant at the time of examination and did not have immediate plans for pregnancy. (II) MRI was performed within three days before and after ablation. (III) No surgery or other treatment was performed before MRI examination. The exclusion criteria were as follows: (I) lesion diameter less than 1 cm. (II) Other uterine diseases requiring surgical treatment.

MRI scanning protocol

All patients underwent MRI scans, including T2-weighted imaging with fat suppression (T2WI-FS) and T1-volume interpolated body examination with fat suppression (T1-VIBE-FS), both prior to and within three days following HIFU treatment. The MRI examinations were performed using a Siemens Verio Dot 3.0T MEI scanner (Siemens, Erlangen, Germany). Specific details regarding the imaging sequences and parameters are outlined in Table 1.

Grouping criteria

Samples showing local perfusion defects in the seromuscular layer on coronal or axial images of postoperative T1-VIBE-FS sequence were classified into the injury group; otherwise, they were classified into the intact group.

Imaging characteristics

Using the T1-VIBE-FS sequence, the longitudinal (D1), anteroposterior (D2), and transverse (D3) diameters of the target uterine fibroid and the non-perfused volume (NPV) were measured both before and after HIFU treatment. The fibroid volume and NPV were then calculated based on the ellipsoid volume formula V(mm3）=0.5233×D1（mm)×D2(mm)×D3(mm), and the non-perfused volume ratio (NPVR); NPVR=NPVFibroidvolume×100% ablation parameters (average power, exposure time) were collected, and the energy efficiency factor (EEF) was calculated using the formula: EEF(J/mm3)=η×averagepower(W)×exposuretime(s)/NPV(mm3), where η reflects the ability of HIFU to concentrate ultrasound energy, and η=0.7.

The information on the location of the fibroid was collected. On T2-weighted imaging (T2WI) sagittal images, measurements were taken of the leiomyosarcoma ventral cutaneous distance, which refers to the shortest distance from the ventral surface of the leiomyosarcoma to the skin of the abdominal wall, and the leiomyosarcoma dorsal cutaneous distance, defined as the longest distance from its dorsal surface to the abdominal wall skin. Additionally, we measured the thickness of the rectus abdominis muscle at the level of the second sacral vertebra. On T2WI-FS axial images, we evaluated the distribution of the myometrial layers around the fibroid. First, we selected the largest cross-sectional area of the fibroid. Then, this plane was divided into four quadrants using two perpendicular lines centered on the fibroid. Each quadrant was subdivided into two sections using dashed lines. For any given quadrant, the myometrial layer was considered present if it covered more than half of the quadrant’s area (Figure 1A-1E). The number of myometrial quadrants was interpreted as follows: a value of 0 indicates no surrounding myometrial layer, 1 quadrant signifies a limited presence, 2 quadrants represent a small distribution, 3 quadrants correspond to a significant distribution, and 4 quadrants denote an extensive distribution.

Figure 1 A method for calculating the distribution of the myometrial layer around the fibroid. (A) No myometrial layer around the fibroid, 0 quadrants; (B) limited distribution, 1 quadrant; (C) small distribution, 2 quadrants; (D) significant distribution, 3 quadrants; (E) extensive distribution, 4 quadrants.

Image analysis

All imaging was assessed independently by two radiologists with extensive experience in diagnosing pelvic diseases. In cases of disagreement, a third radiologist conducted an independent evaluation to reach a consensus. The analysis included MRI characteristics and MRI findings of myometrial damage following ultrasound ablation.

Statistical analysis

Statistical analyses were performed using SPSS 26.0 software (IBM Corp., Armonk, NY, USA). Continuous data with a normal distribution were expressed as mean ± standard deviation (x¯±s), whereas those with a non-normal distribution were reported as median with interquartile range (IQR). To compare continuous variables, independent sample t-tests or Wilcoxon rank-sum tests were applied, depending on the distribution of the data. Categorical variables were analyzed using chi-square tests or Fisher’s exact tests. A P value of less than 0.05 was considered indicative of statistical significance.

Results

Seromuscular-layer injury after HIFU treatment for uterine fibroids

On T1-VIBE-FS sequence taken within three days after HIFU treatment, 55 patients showed signs of seromuscular-layer injury, with an incidence rate of 28.4%. T2WI images displayed a continuous signal in the myometrial layer surrounding the fibroid, whereas the T1-VIBE-FS sequence revealed localized perfusion defects in the uterine myometrium (Figure 2A,2B).

Figure 2 MRI images after HIFU. After ablation, T2WI sequences show continuous signal in the myometrium surrounding the fibroid with clear borders (A); dynamic contrast-enhanced scans display ring-like enhancement in the uterine myometrium with local perfusion defects (B). MRI, magnetic resonance imaging; HIFU, high intensity focused ultrasound; T2WI, T2-weighted imaging.

Univariate analysis of seromuscular-layer injury after HIFU treatment for uterine fibroids

No missing data were observed for the variables analyzed in this study. There were statistically significant differences between the seromuscular-layer injury group and the intact group in terms of age, type of fibroid, thickness of the rectus abdominis muscle, leiomyosarcoma ventral cutaneous distance, fibroid volume, EEF, and the number of myometrial quadrants (P<0.05). However, there were no statistically significant differences in terms of leiomyosarcoma dorsal cutaneous distance, average power, and irradiation time (P>0.05) (Table 2).

Logistic regression analysis of myometrial injury after HIFU treatment for uterine fibroids

A logistic regression analysis was performed on patients with seromuscular-layer injury and those with intact myometrium after HIFU treatment. The results indicated that subserosal fibroid, age ≤43.5 years, thickness of the rectus abdominis muscle ≤8.06 mm, EEF ≤3.6 J/mm³, NPVR ≥67%, and number of myometrial quadrants ≤1 are significant factors influencing the occurrence of myometrial perfusion defects after treatment of uterine fibroids (Table 3).

Discussion

HIFU has demonstrated definite value in fibroid ablation (13,14), but research has found that ultrasound may cause tissue damage beyond the target area due to physical phenomena such as refraction and reflection when passing through acoustic pathways, making its safety a significant concern in clinical practice (15). HIFU technology adjusts treatment parameters such as dosage and exposure time by monitoring real-time changes in the echogenicity of the target area, along with patient tolerance and changes in target area echogenicity, until most of the target area is covered by strong echogenicity, thereby ending the ablation process (11). In this process, it can easily result in damage to non-target tissues. Seromuscular-layer injury serves as a critical parameter in assessing the safety of HIFU treatment. Such injuries may lead to uterine rupture, adhesions, and fertility issues (16). Although there is currently limited evidence directly linking seromuscular-layer injury to adverse clinical outcomes, maintaining an intact enhanced margin on imaging is crucial for ensuring clinical safety. This is especially important for patients with fertility plans, as avoiding substantial damage to the seromuscular layer is vital for preserving uterine integrity.

In this study, patients aged ≤43.5 years had a 2.973 times higher risk of seromuscular layer injury after HIFU compared to those aged >43.5 years. According to relevant studies, uterine fibroids are hormonally dependent, with high estrogen levels considered one of their pathophysiological mechanisms (17). Older patients tend to respond better to HIFU ablation (18), whereas younger patients typically have higher estrogen levels. These higher levels may increase the blood supply to the fibroids, making it more challenging for ultrasound energy to deposit effectively. Consequently, lesions of the same size in younger patients may require higher energy to achieve adequate ablation, which increases the risk of non-target tissue injury. Therefore, age may indirectly influence the occurrence of seromuscular-layer injury through its impact on hormonal levels and treatment parameters. EEF is an indicator for assessing the dosage of HIFU, representing the ultrasound ablation energy required per unit volume of fibroid tissue. Smaller EEF values indicate lower HIFU ablation difficulty (19,20). This study found that EEF ≤3.6 J/mm³ is an independent influencing factor for postoperative uterine seromuscular-layer injury, indicating that lower EEF values (lower ablation difficulty) are associated with a higher risk of seromuscular-layer injury after HIFU, consistent with the findings of Li (21). This suggests that in cases of lower ablation difficulty, ultrasound energy may more easily accumulate in non-target tissues, thereby increasing the risk of seromuscular-layer injury. Another independent influencing factor for postoperative uterine seromuscular-layer injury was shown to be thickness of the rectus abdominis muscle ≤8.06 mm, which was negatively correlated with the probability of seromuscular-layer injury. This means that the thinner the rectus abdominis, the greater the risk of seromuscular-layer injury. This may be related to the attenuation of ultrasound energy during its penetration. When the rectus abdominis is thinner, its ability to absorb and attenuate ultrasound energy is weaker, allowing more energy to penetrate and act on the seromuscular layer, thereby increasing the risk of excessive heat accumulation in the seromuscular layer (22). Additionally, when the rectus abdominis is thinner, the tissue’s blood supply may be relatively insufficient, leading to poorer heat dissipation, making it easier for heat to accumulate and cause irreversible damage to the tissue. Furthermore, from a physical perspective, a thinner rectus abdominis may also lead to uneven distribution of ultrasound energy, further increasing the probability of damage to surrounding tissues, particularly the seromuscular layer. The probability of seromuscular-layer injury after HIFU in subserosal fibroids is 17.129 times higher than that in submucosal fibroids. This may be because the surface of subserosal fibroids is primarily covered by a thin muscle layer and serosa, with fewer blood vessels, making it more susceptible to ultrasound energy deposition. In contrast, submucosal fibroids have a thicker uterine muscle layer between the tumor edge and the serosa, with a rich blood supply, which hinders energy deposition. This study introduced a new index for assessing the distribution of muscle layers around fibroids, namely the number of quadrants around the fibroid. The study found that when the number of quadrants is ≤1, the risk of seromuscular-layer injury after HIFU is 6.383 times higher compared to when the number of quadrants is ≥2, indicating that fibroids with only partial thin muscle layer or serosa coverage are more likely to cause seromuscular-layer injury (23,24). This also explains why subserosal fibroids have a higher probability of seromuscular-layer injury. Therefore, in the treatment of such fibroids, clinicians are advised to closely monitor changes in echogenicity of the target area to avoid excessive thermal injury. Additionally, previous studies have shown that NPVR serves as a significant metric in assessing the effectiveness of HIFU ablation for uterine fibroids (25-27). The larger the NPVR value, the better the treatment outcome, the higher the improvement in symptoms, and the lower the risk of recurrence (5,28-30). However, this study indicates that when NPVR ≥67%, the risk of seromuscular-layer injury after HIFU increases. Therefore, while ensuring treatment efficacy, clinicians should control NPVR and assess related risks to avoid excessive injury to the seromuscular layer.

This was a single-center retrospective study with potential selection bias. Therefore, future multi-center, large-sample prospective studies are needed to support and validate our conclusions. Although T1-VIBE-FS sequence performs well in detecting significant injuries, it has certain limitations in identifying small perfusion defects or subtle injuries, which may be related to imaging resolution. Additionally, some perfusion defects may be caused by transient vascular spasms or blood flow obstruction rather than irreversible tissue damage (31), which partially affects the comprehensive assessment of minor injuries. Moreover, although studies suggest that seromuscular-layer injuries are reversible and can recover within several months (12), there is currently a lack of research focusing on changes in seromuscular-layer injury within the first three days after HIFU treatment. Future studies could employ higher-resolution T1-VIBE-FS sequence techniques combined with other imaging sequences and pathological findings to enhance the detection of small injuries. Additionally, we were able to measure the extent of postoperative seromuscular layer damage and conduct further detailed investigations into the prognosis of seromuscular layer injury. Future studies can also investigate postoperative pelvic fascia injury, pelvic bone injury, and other non-target tissue injuries to comprehensively study the effects of HIFU treatment for uterine fibroids.

Conclusions

This study provides a clear risk assessment framework for seromuscular-layer injury, identifying subserosal fibroids, age ≤43.5 years, thickness of the rectus abdominis muscle ≤8.06 mm, EEF ≤3.6 J/mm³, NPVR ≥67%, and ≤1 quadrant of surrounding muscle layers as the most important factors influencing seromuscular-layer injury. By understanding these risks, clinicians can gradually accumulate experience, optimize personalized treatment plans, and enhance monitoring and follow-up for high-risk patients. Our research offers valuable references for future clinical practice, particularly in the areas of personalized treatment and risk assessment.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-1062/rc

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-24-1062/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 Yongchuan Hospital of Chongqing Medical University, Chongqing, China (approval No. 2024LLS005). Due to the retrospective nature of this study, the requirement for informed consent was waived.

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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