Efficacy of focused ultrasound ablation surgery in patients with adenomyosis and coexisting pelvic adhesions

Objective The objective of this study was to assess the efficacy of focused ultrasound ablation surgery (FUAS) in treating patients with adenomyosis and coexisting pelvic adhesions.

A total of 396 patients diagnosed with adenomyosis and who underwent FUAS between January 2014 and December 2022 were enrolled. Pelvic adhesions were evaluated using magnetic resonance imaging (MRI), and the patients were categorized into either adhesive group or non-adhesive group. The aim was to investigate the comparative efficacy between the two groups.

Among the 396 patients, pelvic adhesions were detected in 123 (31.06%) women. Compared to the non-adhesive group, patients in the adhesive group exhibited a higher preoperative dysmenorrhea score (7 vs. 6, p < 0.001), a lower short-term clinical success rate (74.80% vs. 84.62%, p = 0.025), and a higher long-term cumulative recurrence rate (log-rank p = 0.009). The adhesive group exhibited a high incidence of anal discomfort during the procedure compared to the non-adhesive group (18.70% vs. 7.69%, p = 0.002). Additionally, patients with severe adhesion demonstrated a lower ratio of non-perfused volume ratio (NPVR) (38.81% vs. 46.58%, p = 0.009). Multivariate binary logistic regression analysis revealed that pelvic adhesion independently increased the risk of dysmenorrhea (OR = 4.730, 95%CI: 2.026–11.044, p < 0.001), while severe pelvic adhesion was identified as an independent risk factor for NPVR (OR = 2.226, 95%CI: 1.181–4.196, p = 0.013).

The preoperative assessment of pelvic adhesions plays a crucial role in predicting intraoperative adverse events of FUAS in patients with adenomyosis, as well as determining both short-term and long-term efficacy, thereby providing valuable guidance for the development of comprehensive treatment. 1. Introduction The condition of adenomyosis is characterized by the infiltration of endometrial glands and stroma into the myometrium, accompanied by hyperplasia and hypertrophy of the surrounding muscle fibers. It is a prevalent benign gynecological disorder that frequently leads to infertility, excessive menstrual bleeding and dysmenorrhea [Citation1]. The reported prevalence rates in various studies exhibited substantial variability, ranging from 8.8% to 61.5% [Citation2]. Pelvic adhesions are frequently associated with adenomyosis [Citation3,Citation4], exacerbating pelvic pain symptoms in gynecological patients and significantly impairing their quality of life [Citation5,Citation6]. The magnetic resonance imaging (MRI) technique offers high-resolution visualization of soft tissues and demonstrates the characteristic indicators of adenomyosis with a diagnostic accuracy comparable to that of histologic examination [Citation7,Citation8]. Additionally, it can reveal indications of adhesions and anatomical alterations such as obliteration of the posterior cul-de-sac [Citation9,Citation10]. The definitive treatment for adenomyosis is hysterectomy, which is considered a radical intervention [Citation11]. However, there has been a gradual shift toward a more comprehensive strategy based on conservative surgery for patients who wish to preserve their reproductive capabilities or keep their uterus intact. This includes procedures such as focal lesion excision and focused ultrasound ablation surgery (FUAS) [Citation12]. The FUAS technique is an innovative noninvasive therapy that harnesses the penetrability, directivity, and focusing capabilities of ultrasound waves to precisely target and concentrate them on specific lesion areas in vivo. By employing high-intensity focused ultrasound ablation, tissue temperature can be elevated above 60 °C, inducing coagulation necrosis of targeted tissue cells while ensuring the preservation of surrounding tissues unharmed [Citation11]. Extensive research has consistently demonstrated its safety and efficacy for treating adenomyosis [Citation13–16]. The application of FUAS resulted in the emergence of a non-perfused volume (NPV) within the lesion, leading to a loss of activity in the ectopic endometrium. Consequently, it lost its proliferative ability and ceased bleeding with changes in the ovarian cycle, ultimately alleviating symptoms associated with dysmenorrhea. Non-perfused volume ratio (NPVR) is commonly employed as an indicator to evaluate the effectiveness of FUAS [Citation14,Citation15,Citation17]. Studies have reported that pelvic adhesion plays a significant role in influencing the surgical outcomes of gynecological procedures [Citation18–20]. In cases of extrinsic adenomyosis accompanied by pelvic adhesions, FUAS necessitates higher dosage and may lead to an increased incidence of sciatica or buttock pain [Citation21]. However, no previous studies have explored the potential association between pelvic adhesions and the efficacy of focused ultrasound ablation on adenomyosis. Therefore, our objective was to evaluate the efficacy of FUAS in patients with adenomyosis and coexisting pelvic adhesions, aiming to establish guidelines for appropriate patient selection. 2. Materials and methods The retrospective investigative research was approved by our institution’s Ethics Committee (Ethical Approval Number: HF2023-013). Informed consent documents were obtained from each patient prior to undergoing FUAS. Verbal approval was granted for follow-up. All procedures adhered to the principles outlined in the Declaration of Helsinki and the ethical guidelines established by the hospital. 2.1. Patients From January 2014 to December 2022, patients diagnosed with adenomyosis and treated with FUAS at the Ultrasonic Ablation Center of the First Affiliated Hospital of Chongqing Medical University and Chongqing Haifu Hospital in China were included in this study. The inclusion criteria were as follows: (1) premenopausal women aged over 18 years; (2) patients diagnosed with adenomyosis by ultrasound and MRI who experienced dysmenorrhea or/and menorrhagia; (3) the myometrium adjacent to the lesion had a minimum thickness of 30 mm; (4) comprehensive pelvic MRI data collected both before and after surgery. Exclusion criteria were as follows: (1) patients who had received endocrine therapy within the 3 months preceding FUAS; (2) patients with a history of surgery excision for uterine adenomyosis lesions; (3) patients with uterine fibroids larger than 20 mm in diameter. 2.2. MRI evaluation Patients underwent MRI scans as part of the standard protocol, both prior to and within 3 days following FUAS. Adhesion evaluation was primarily conducted using T2 sagittal fat-saturated sequences as well as T1 or T2 axial sequences. Adhesions were observed as burr fiber bundles at the interface of blurred organs, with equal to mild low signal on T1-weighted images (T1WI), low signal on T2-weighted images (T2WI), or lack of a clear interface between adjacent organs, disappearance of the fat layer, needlelike low signal traction between organs, and angulation and distortion of adjacent intestinal loops [Citation9]. The imaging findings of posterior cul-de-sac obliteration included: retroflexed uterus; retrouterine mass; displacement of intraperitoneal fluid; elevation of the fornix; adherence of bowel loops [Citation10]. Mild adhesion was classified when an adhesion signal was present on MRI without evidence of posterior cul-de-sac obliteration (), whereas severe adhesion was indicated by the presence of a posterior cul-de-sac obliteration signal (). MR image evaluations were performed by a radiologist with 7 years of experience and a gynecologist with 14 years of clinical experience. In case of any discrepancies, consultation with the imaging department’s chief physician, who possesses 15 years of experience, was sought to reach an agreement. The open-source program ITK-SNAP version 4.0.0 (www.itksnap.org) was utilized to generate volume measurements through layer-by-layer sketches and automatic calculations. NPVR was determined using the formula: NPVR = NPV/adenomyosis volume × 100%. 2.3. FUAS system and treatment procedure The Focused Ultrasound Tumor Therapeutic System (Model-JC, Chongqing, Haifu Medical Technology Co. Ltd., China) was utilized. The ultrasonic transducer had adjustable power and operating frequency within the range of 350–400 W and 0.8–0.95 MHz, respectively. Prior to FUAS, all patients underwent bowel preparation, degreasing, and degassing of the skin along the acoustic pathway. The anterior abdominal wall of the patients made contact with the degassed water while they were positioned in a prone manner. Throughout the procedure, real-time guidance was provided by an ultrasound imaging device (Esaote, MyLab 70, Italy) with a frequency of 3.5 MHz. The endometrium or serosa was maintained at least 10 mm away from the target, and the extrauterine tissue structure was remained at least 15 mm away. The overall gray level of the target area or the changes in the mass’s gray level were used for measuring the tissue reaction. The procedure ceased when the increased gray area covered the planned treatment region adequately enough. Patients received midazolam hydrochloride (0.02–0.03 mg/kg) and fentanyl (0.8–1.0 g/kg) to minimize discomfort and movement while maintaining a state of conscious sedation state. Ultrasound dosage was adjusted based on patient tolerance level and effectiveness achieved. All patients were monitored for two hours before being transferred back to their ward. Complications were categorized according to the classification criteria established by the Society of Interventional Radiology (SIR). In the SIR classification system, classes A and B were classified as minor complications, whereas classes C through F were designated as major complications [Citation22]. 2.4. Symptom assessment and follow-up The numeric rating scale (NRS) was utilized to quantitatively assess the degree of dysmenorrhea and rank the severity of dysmenorrhea based on the following criteria: (1) inadequate efficacy, defined as a reduction in NRS score of 20% or less; (2) partial relief, defined as a decrease in NRS score ranging from 20% to 50%; (3) significant relief, characterized by a decrease in NRS scores between 50% and 80%; (4) complete relief, defined as a reduction in NRS scores of at least 80% or greater. Clinical success was determined if any of the outcomes mentioned above (2), (3), (4) were achieved [Citation23]. Follow-up visits or phone calls were scheduled at 3, 6 and 12 months post-treatment and annually thereafter. The follow-up period concluded in March 2024. Recurrence of symptoms was considered if the NRS score reached 80% of their preoperative level following clinical success [Citation23], or if menorrhagia symptoms were reappeared after being relieved for at least three months [Citation24]. Follow-up endpoints included ineffectiveness, symptom recurrence and improvement until menopause. Failure to establish contact with patients multiple times within 2 weeks was regarded as loss to follow-up. 2.5. Statistical analysis SPSS version 27.0 software (IBM, Armonk, NY) was utilized for conducting the statistical analysis. The mean ± standard deviation was employed to report normally distributed data, while percentiles (p25, p75) were used for reporting non-normally distributed data. Categorical data were presented using numerical values and percentages (%). Comparisons between groups were performed utilizing the non-parametric tests, t-tests and chi-squared tests. Statistical significance were considered when p < 0.05. Factors influencing dysmenorrhea, NPVR and short-term efficacy were examined through binary logistic regression analysis. The recurrence process was described and the variation in recurrence events between the two groups was compared using the Kaplan–Meier curve. 3. Results 3.1. Patients A total of 396 patients were enrolled, with a median age of 40 (36, 44) years. Among them, 379 (95.71%) patients experienced dysmenorrhea, and 323 (81.57%) had menorrhagia. Additionally, pelvic adhesions were present in 123 cases (31.06%), while ovarian endometriosis cysts were found in 77 (19.44%) patients (Table S1). 3.2. Comparison between adhesive and non-adhesive groups Among the 396 patients, 273 (68.94%) were categorized as non-adhesive group while the remaining 123 (31.06%) belonged to adhesive group. In comparison with the non-adhesive group (as shown in ), the dysmenorrhea NRS score was higher (7 vs. 6, p < 0.001), there was a greater proportion of non-steroidal analgesics usage (78.86% vs. 63.00%, p = 0.002), gravidity number was lower (2 vs. 4, p < 0.001), volume of adenomyosis was smaller (80.04 vs. 95.60 cm3, p = 0.046) and age of patients were younger (38.31 ± 5.58 vs. 40.60 ± 5.54 years, p < 0.001). Predominantly observed lesions in the adhesive group included posterior wall lesions (58.55%) and extrinsic adenomyosis (53.66%). The proportion of endometriosis cysts was significantly higher in the adhesive group compared to that in non-adhesive group (56.10% vs. 2.93%, p < 0.001). (The comparative analysis of baseline data across the three groups was presented in of the Supplementary Material). 3.3. Effect of pelvic adhesions on dysmenorrhea Based on the degree of adhesions, there were 273 cases (68.94%) in the non-adhesive group, 56 cases (14.14%) in the mild adhesive group and 67 cases (16.92%) in the severe adhesive group. There was a significant difference in the preoperative NRS scores among the different groups (p < 0.001) (Table S2). The preoperative NRS score was 7 (6, 8) in the mild adhesive group and 7 (6, 9) in the severe adhesive group, which were significantly higher than that of the non-adhesive group 6 (4, 8) (p < 0.05) (). Multivariate binary logistic regression analysis demonstrated that pelvic adhesion served as an independent risk factor for dysmenorrhea (odds ratio [OR] = 4.730, 95% confidence interval [CI]: 2.026–11.044, p < 0.001) (). 3.4. FUAS ablation results and adverse events All 396 patients successfully completed FUAS treatment without experiencing any severe adverse events. The mean values for NPVR were 43.23% (30.84%, 59.46%) and 46.58% (30.21%, 62.96%) in the adhesive and non-adhesive groups, respectively. With no significant difference observed between the two groups (p = 0.333). The adhesive group exhibited lower treatment efficiency compared to the non-adhesive group (40.62 vs. 61.09 mm3/s, p < 0.001) (). Moreover, the energy efficiency factor (EEF) was significantly higher in the adhesive group than in the non-adhesive group (6.58 vs. 4.45 J/mm3, p = 0.001). Among all intraprocedural adverse effects reported, treatment area pain had the highest incidence rate of occurrence at 65.66%, followed by sacrococcygeal pain at 46.72%, skin burning at 32.32%, lower limb radiation pain at 26.26% anal discomfort at 11.11%, buttock pain at 14.65%, groin pain at 9.60% and perineal pain at 2.53%. Notably, there was a statistically significant difference in the incidence of anal discomfort between the adhesive group (18.70%) and the non-adhesive group (7.69%) (p = 0.002) (). Anal discomfort was completely resolved one day after undergoing the FUAS procedure. In the adhesive group, 44 cases (35.77%) were classified as SIR grade A and 39 cases (31.71%) as SIR grade B. In contrast, in the non-adhesive group, 99 cases (36.26%) were classified as SIR grade A and 58 cases (21.25%) as SIR grade B. Among these cases, 97 (24.49%) required supplementary treatments, which included analgesic management in 95 cases (23.99%), prophylactic antimicrobial treatments in 2 cases (0.51%) and adrenal cortical hormone therapy for lower limb numbness in 1 case (0.25%). One patient received both analgesic and prophylactic antimicrobial treatments. 3.5. Effect of pelvic adhesion on FUAS ablation results A comparison of NPVR revealed a significant difference among groups (p = 0.006) (Table S2). The severe adhesive group exhibited lower NPVR compared to both the non-adhesive group (38.81% vs. 46.58%, p = 0.009) and the mild adhesive group (38.81% vs. 48.06%, p = 0.003) (). There was no significant difference in NPVR between the non-adhesive and the mild adhesive groups (p > 0.05). Severe pelvic adhesion emerged as an independent risk factor for NPVR (OR = 2.226, 95%CI: 1.181–4.196, p = 0.013) (). 3.6. Comparison of treatment efficacy After a 3-month follow-up assessment, the clinical success rate was found to be 81.57%. There was a significant difference between the adhesive group (74.80%) and the non-adhesive group (84.62%) in terms of clinical success rates (p = 0.025). The median postoperative NRS scores for dysmenorrhea were 3 (2, 5) in the adhesive group and 2 (1, 4) in the non-adhesive group, indicating mild dysmenorrhea, there was a statistically significant difference between these two groups (p < 0.001) as shown in . Multivariate logistic regression analysis revealed that NPVR was the sole influencing factor for postoperative dysmenorrhea scores (OR = 1.014, 95%CI: 1.002–1.026, p = 0.020) (Table S3). 3.7. Comparison of symptom recurrence A total of 310 (78.28%) patients completed a 10-year follow-up, with a median follow-up duration of 58 months (46–122 months). Additional treatment, including the administration of a levonorgestrel-releasing intrauterine system and a gonadotropin-releasing hormone agonist (GnRHa), was given to 32 patients (8.08%). Cox regression analysis revealed that pelvic adhesion was the single factor influencing recurrence after FUAS. Kaplan–Meier curve analysis demonstrated that the cumulative recurrence rates at 1, 2, 3 and 5 years after FUAS for the non-adhesive group were as follows: 22.00%, 34.90%, 37.20% and 40.50%, respectively, whereas for the adhesive group they were 38.1%, 47.60%, 51.20% and 53.80%. There was a significant difference between these two groups in terms of recurrence rates (log-rank p = 0.009) (). 4. Discussion The presence of pelvic adhesions significantly impacts the efficacy and safety of surgery for gynecological patients [Citation19,Citation20]. The MRI-based internal attributes of adenomyosis lesions are closely associated with the ablation effect of FUAS, yet insufficient attention has been given to the abnormal signal characteristics outside the uterus. Furthermore, there is a lack of studies reporting on the efficacy of FUAS for patients with adenomyosis and coexisting pelvic adhesions. Therefore, MRI, a reliable and noninvasive detection method [Citation9,Citation25], was utilized to evaluate the presence and severity of pelvic adhesions and further investigate the efficacy of FUAS for patients with adenomyosis and coexisting pelvic adhesions. The results demonstrated that pelvic adhesion was identified as an independent risk factor, with patients suffering from adenomyosis and pelvic adhesions exhibiting higher dysmenorrhea scores, which aligns with previous reports [Citation26,Citation27]. However, no significant difference was observed in the impact of varying degrees of pelvic adhesions on dysmenorrhea symptoms. The exacerbating of dysmenorrhea associated with pelvic adhesions can be attributed to the distortion of the normal anatomical structures within pelvis [Citation28]. Furthermore, a strong correlation was found between aberrant sacral nerves and both adhesions and dysmenorrhea [Citation29]. Nevertheless, there is no relationship between sensory nerve fibers and the size or position of adhesions [Citation27]. This may explain why there was no significant difference in dysmenorrhea scores among patients with different degrees of adhesions in this study. Additionally, the presence of pelvic adhesions may indirectly indicate the severity of pelvic endometriosis in patients with adenomyosis [Citation6,Citation30,Citation31]. Consequently, individuals experiencing concurrent adenomyosis and pelvic adhesions are likely to encounter significantly severe dysmenorrhea. The adhesive group demonstrated a significantly higher incidence of adverse events in the anal region, which can likely be attributed to the anatomical location of the lesion within the pelvic cavity and associated intestinal adhesions. Adhesions may raise concerns about an increased risk of pelvic organ damage during the ablation of posterior uterine wall lesions that penetrate the serosa. Our data indicate that while the proportion of SIR grade B cases was marginally elevated in the adhesive group, patients with severe adhesions did not report gastrointestinal-related symptoms during subsequent follow-up examinations. Consequently, it is clear that experienced surgeons can effectively reduce the risk of serosal penetration and damage to pelvic organs through appropriate technical adjustments. The NPVR served as an indicator of the efficacy of FUAS technology [Citation14,Citation15,Citation17]. In general, the NPVR for women with severe adhesion adenomyosis is approximately 40%, while those with mild or no adhesion can achieve around 50%. Our study revealed that women with adenomyosis complicated by severe pelvic adhesions exhibited significantly lower NPVR. Multivariate logistic regression analysis identified severe adhesion as an independent influencing factor for NPVR. Given that the lesions are tethered and fixed in position due to adhesions, constructing a viable treatment channel becomes more challenging compared to patients without adhesions. Additionally, the distance from the adenomyosis ventral side to the skin is greater in these cases. This suggests that ultrasound waves may experience greater energy loss during conduction. Therefore it is recommended to consider adhesions as a significant factor in clinical practice. The cumulative recurrence rate following FUAS was significantly higher in the adhesive group compared to the non-adhesive group. In addition to pelvic adhesions, the higher proportion of ovarian endometriotic cysts may contribute to the observed higher cumulative recurrence rate in the adhesive group. Endometriosis is a major cause of posterior cul-de-sac obliteration, and is closely associated with pelvic adhesions [Citation31,Citation32]. In the context of endometriosis, it has been shown that the coexisting ovarian endometriosis cyst is suggestive of deeper and more severe endometriosis [Citation33]. Consequently, it is speculated that patients with adenomyosis and ovarian endometriotic cysts have higher recurrence rates after FUAS treatment. Another possible reason could be that patients in the adhesive group are younger. It is evident that age significantly influences the long-term recurrence of adenomyosis due to its association with hormone alterations, as supported by other studies [Citation34–36]. To the best of our knowledge, we are the first to report a significant correlation between pelvic adhesions observed through MRI and FUAS ablation in patients diagnosed with adenomyosis. Additionally, this study represents the first-ever 10-year follow-up investigation on adenomyosis following FUAS. However, it is important to acknowledge several limitations within this study. First, due to its retrospective nature, potential data bias may exist. Moreover, given the extended duration of the follow-up period, there is a possibility of recall bias influencing our findings. Additionally, conducting a separate analysis on pelvic adhesions posed challenges due to their close association with endometriosis. Lastly, it should be noted that the number of patients exhibiting pelvic adhesions in this study was relatively limited. 5. Conclusion Patients with adenomyosis and coexisting pelvic adhesions experience severe dysmenorrhea. The short-term efficacy of FUAS in these patients was less satisfactory, while the long-term recurrence rate was significantly higher. Pelvic adhesions exacerbate anal discomfort during FUAS procedure. Therefore, preoperative assessment of adhesions is beneficial for predicting intraoperative adverse events, short-term and long-term efficacy, and serves as a guide for formulating a comprehensive treatment plan. Supplemental material Supplemental Material Download Zip (45.6 KB)Supplemental MaterialDisclosure statement The authors affirm that they do not possess any known competing financial interests or personal relationships that could have potentially influenced the findings presented in this article. Data availability statement The corresponding author can be contacted to request access to the study’s data. Due to potential privacy concerns for research participants, the data is not publicly available. Additional information Funding

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