Transvaginal ultrasound- and laparoscopy-guided percutaneous microwave ablation for adenomyosis has short- and long-term benefits: a single-center study

Abstract

Objectives

Transvaginal ultrasound- and laparoscopy-guided percutaneous microwave ablation (TLPMA) is a minimally invasive alternative technique with low risk, fast recovery and few side effects. We aimed to evaluate the safety and long-term efficacy of TLPMA for treating adenomyosis.

Methods

We included 79 patients with symptomatic adenomyosis who underwent TLPMA and 44 patients with adenomyosis who received the levonorgestrel-releasing intrauterine system (LNG-IUS). We evaluated the role of laparoscopy in TLPMA as well as the short- and long-term effects of TLPMA.

Results

The mean age of the 79 patients who underwent TLPMA was 41.8 years. There was no difference in the mean age between the TLPMA and LNG-IUS groups. Laparoscopy could help to separate pelvic adhesions, provide a wide antenna path, and observe the uterine surface and bowel movement. No major complications were found in patients who underwent TLPMA. There was a significant post-treatment reduction in both the uterine and lesion volumes (p < 0.001). After a median follow-up duration of 36 months (range: 1–60 months), the uterine and lesion volumes remained stable. Additionally, most patients remained without dysmenorrhea, which confirms the long-term efficacy of TLPMA.

Conclusions

TLPMA is a feasible, minimally invasive technique for the treatment of adenomyosis, which significantly decreases the uterine and lesion volumes and has a good long-term effect.

Keywords:

• Adenomyosis
• microwave ablation
• transvaginal ultrasound and laparoscope

Introduction

Adenomyosis is a relatively common disease characterized by the presence of endometrial glands and stroma within the myometrium [1]. Its prevalence among women of childbearing age ranges from 8% to 27% [2,3]. Symptomatic patients often complain of dysmenorrhea and heavy menstrual bleeding [4]. Chronic pelvic pain, dyspareunia, infertility and obstetric complications are associated with adenomyosis, which adversely influences the quality of daily life [5]. Adenomyosis frequently occurs in the posterior uterine wall with uterine enlargement [6]. Women with adenomyosis are often diagnosed after experiencing symptoms for extended periods, and thus choose to undergo hysterectomy [7].

The levonorgestrel-releasing intrauterine system (LNG-IUS) is the most effective first-line treatment for adenomyosis-related pain, bleeding and anemia [7]. Although medical therapy may relieve adenomyosis symptoms to a certain degree, its long-term efficacy is limited, with frequent occurrence of symptom relapse [3].

Hysterectomy may be unsuitable for women of reproductive age who desire to preserve fertility [8]. Recently, several less invasive treatments, including image-guided ablation techniques, including high-intensity focused ultrasound ablation (HIFU), uterine artery embolization (UAE), radiofrequency ablation (RFA) and microwave ablation (MWA), have emerged, which have provided alternatives to hysterectomy [7,9–12].

However, these aforementioned treatments have several limitations. HIFU guided by ultrasound or magnetic resonance imaging (MRI) is a safe and effective treatment strategy for adenomyosis; however, its range of applications is limited by technical eligibility [13]. Although UAE is considered safe and effective, its impact on ovarian function and fertility remains unclear [14–16]. Further, RFA is an effective, minimally invasive treatment; however, it has low thermal efficiency and involves a relatively long treatment time. There has been increasing attention on MWA given its high thermal efficiency [17–19]. Taken together, there is a need for a minimally invasive alternative technique with low risk, faster recovery and fewer side effects.

We previously reported that laparoscope-guided percutaneous MWA (PMWA) could reduce the risk of collateral thermal damage to the intestinal tract and relieve pelvic adhesions [3]. The PMWA may lead to serious complications such as penetration or thermal damage to other pelvic organs and abdominal bleeding, especially in patients with uterine adhesion to surrounding organs [3]. The LNG-IUS is an effective, reversible and long-term treatment option for adenomyosis. It is often used in patients with a limited uterine volume. Accordingly, this study included patients who underwent LNG-IUS implantation as a reference for treatment effect [20]. We aimed to further assess the feasibility, safety, efficacy and long-term effects of transvaginal ultrasound- and laparoscopy-guided percutaneous MWA (TLPMA) for adenomyosis.

Methods

Patients

This prospective study included 79 patients with diffuse adenomyosis who underwent TLPMA and 44 patients with diffuse adenomyosis who underwent implantation of the LNG-IUS (Mirena, BayerAg, Germany) [21] from February 2016 to April 2021 at our center.

All patients were diagnosed with adenomyosis through transvaginal ultrasonography and/or MRI. The diagnostic criteria for uterine adenomyosis were as follows: 1) asymmetry of the posterior and anterior myometrium; 2) no distinction between the endometrium and myometrium; 3) myometrial cysts and fibrosis [22,23]; 4) subendometrial myometrial striations; and 5) heterogeneous myometrial echotexture [3,24]. The diagnostic criteria for uterine adenomyosis on MRI were as follows:1) myometrial mass with indistinct margins of primarily low intensity; 2) diffuse or local widening of junctional zones on T2-weighted images; 3) junctional zone thickness > 15 mm; 4) uterine enlargement; and 5) small hypointense myometrial spots [3,25]. The study was approved by the Human Ethics Review Committee of the Central Hospital of Wuhan (WHZXKYL2021-051) and conducted according to the principles of the Declaration of Helsinki. All participants provided written informed consent for their treatment.

The inclusion criteria of the study were as follows: 1) adenomyosis diagnosed through transvaginal ultrasonography or MRI and the related syndrome (e.g., dysmenorrhea and/or menorrhagia); 2) strong desire to preserve the uterus and fertility; and 3) voluntary acceptance of the TLPMA technique or LNG-IUS (Mirena). The exclusion criteria were as follows: 1) comorbidity with severe disease involving other important organs, including the brain, heart, and liver; 2) menopausal status; 3) history of other interventional treatments, including UAE and high-frequency focused ultrasonography; and 4) uterine length greater than 9 cm.

TLPMA procedure

To avoid between-operator variability, both transvaginal ultrasonography and PMWA were performed by the same operators during the study period. TLPMA was performed in an inpatient operating room. The patient was placed in the supine lithotomy position and underwent laparoscopy (OLYMPUS HD EndoEYE, Japan) under general anesthesia. Artificial pneumoperitoneum was used to widen the distance between the uterus and surrounding organs. The uterine surface color and shape could be clearly observed. Pelvic adhesions (if present) were initially loosened and treated laparoscopically. Under real-time guidance using laparoscopy and transvaginal ultrasound (4–9 MHz, Philips IU22, Netherlands), a 16-gauge needle (BARD, Tempe, AZ) was inserted into the lesion for biopsy to avoid important blood vessels. A cooled-shaft microwave tumor coagulator (ECO-100, Yigao Microwave System Corp., Nanjing, China) that comprised a 15-gauge needle antenna with a 1.0 cm exposed tip was used for PMWA. It can produce 150 W of power at 2450 MHz [3].

Based on the location and size of the lesion, MWA needle insertion was performed using the ‘moving shot’ technique. The lesion was divided into several small conceptual ablation units, with WMA being performed unit-by-unit by moving the electrode until the lesion was completely ablated. The antenna was percutaneously inserted across the abdominal wall and placed close to the uterine serosa under laparoscopic monitoring. Furthermore, to avoid large vessels, the antenna was inserted into the planned lesion site under transvaginal ultrasound guidance. A power output of 60 W was used during the PMWA. The between-unit distance was approximately 1.5–2.5 cm; moreover, each unit was ablated for 2.5–3.5 min. On transvaginal ultrasonography, once the hyperechogenic signal covered the entire lesion or reached 3–5 mm near the margin of the uterine serosa or endometrium, the ablation procedure was halted and the needle was withdrawn. A satisfactory ablation effect was indicated by a change in the color of the lesion surface from bright red to dark red and finally to pale red on laparoscopy. Contrast-enhanced ultrasonography (CEUS, SonoVue, Bracco, Italy) was immediately performed transabdominally to assess the effectiveness of WMA, with necrotic areas being identified as non-enhanced areas on CEUS³.

LNG-IUS procedure

Ultrasound was used to evaluate the uterine size before LNG-IUS implantation. Patients with a uterine length <9 cm were allowed to undergo LNG-IUS implantation. Ultrasound was again used to locate the LNG-IUS position.

Complications and follow-up

Complications during and after the procedure were recorded. The patients in the LNG-IUS group were asked to return to the hospital at 1, 6 and 12 months, while the patients in the TLPMA group were asked to return to the hospital at 1, 3, 6 and 12 months, followed by subsequent annual visits, after the ablation procedure for follow-up. The median follow-up duration was 36 months (range: 1–60 months). Uterine and lesion volumes were measured using transvaginal ultrasonography or MRI resonance imaging. At each follow-up visit, the patients were assessed using the sensation quantity scale (SQC) and visual analog scale (VAS) questionnaires. After TLPMA or LNG-IUS implantation, if the clinical symptoms (main symptoms: dysmenorrhea) reappeared at the pretreatment levels, worsened, or new lesions reappeared, it was considered a symptom relapse.

Statistical analysis

Normally distributed data are expressed as mean ± standard deviation. Student’s t-test was used to compare normally distributed data. The Wilcoxon signed-rank test was used to compare data with skewed distributions. Fisher’s exact test was used to compare the proportions. All statistical analyses were performed using R software (version 4.0.3). Statistical significance was set at p < 0.05.

Results

Patient information

The mean age of patients who underwent TLPMA and LNG-IUS implantation was 41.8 and 43.4 years, respectively, with no significant between-group difference (p = 0.1) (Table 1). Compared with the LNG-IUS group, the TLPMA group had a larger uterine volume (TLPMA group: 178.0 ± 60.5 cm³, LNG-IUS group:147.01 ± 70.47 cm³; p = 0.002) and larger lesion volume (p < 0.001, Table 1, Figure 1(A, B)). Most patients in the TLPMA group had menorrhagia (97.5%) and dysmenorrhea (97.5%). Compared with the LNG-IUS group, the TLPMA group had significantly higher SQC and VAS scores (Table 1, Figure 1(C, D)).

Figure 1. Short-term and long-term results of different treatments. (A, B) Uterine (A) and lesion (B) volume before and after different treatments at different follow-up times. (C, D). SQC (C) and VAS (D) before and after different treatments at different follow-up times.

Table 1. Baseline information before treatment.

	Mirena (n = 44)	TLPMA (n = 79)	p
Age, years	43.4 ± 4.60	41.8 ± 3.82	0.0625
Uterine volume (cm^3)	147.01 ± 70.47	178 ± 60.5	0.002
Lesion volume (cm^3)	36.14 ± 22.01	69.8 ± 42.5	<0.001
Symptom (n)
Menorrhagia	38 (86.4%)	77 (97.5%)
Dysmenorrhea	36 (81.8%)	77 (97.5%)
Symptom (score)
SQC	4.11 ± 0.62	4.29 ± 0.51	0.126
VAS	7.75 ± 1.37	8.39 ± 1.01	0.009

SD: standard deviation; TLPMA: transvaginal ultrasound- and laparoscopy-guided percutaneous microwave ablation; SQC: sensation quantity scale; VAS: visual analog scale

Safety

None of the patients in the LNS-IUS group experienced ring downward movement or detachment. No major complications were observed during or after TLPMA. During follow-up, a few adverse reactions were reported. Specifically, vaginal discharge was found in 19 (24.1%) patients, which spontaneously disappeared within 2 weeks. Fourteen patients (17.7%) experienced abdominal pain, which spontaneously disappeared within 3 d.

The short-term and long-term outcomes of patients undergoing laparoscopic vaginal ultrasound therapy

At 1 month after TLPMA, the mean uterine volume significantly reduced from 178.1 ± 60.5 cm³ to 107.5 ± 37.6 cm³ while the mean lesion volume significantly reduced from 69.8 ± 42.5 cm³ to 35.7 ± 18.4 cm³ (Table 2, Figures 1(A, B) and S1(A, B)). Notably, although the uterine volume was larger in the TLPMA group than in the LNG-IUS group, there was no between-group difference at 1 post-treatment month (Table 2, Figure 1(A)), with a similar trend being observed for lesion volume (Table 2, Figure 1(B)). Five patients were lost to follow-up after 6 months. During the long-term follow-up, the uterine volume showed a continuous decrease in the TLPMA group; contrastingly, it remained stable in the LNG-IUS group (Table 2, Figure 1(A)). The lesion volume was stable during long-term follow-up in both groups (Table 2, Figure 1(B)). The SQC and VAS scores in both groups significantly decreased and remained stable during the long-term follow-up (Table 2, Figure 1(C, D). After the long-term follow-up, only 31.6% (25/79) of patients in the TLPMA group showed relapse, which was non-significantly lower than the proportion in the LNG-IUS group (Figure S2).

Table 2. Uterine volume, lesion volume, SQC and VAS score before and after different treatments.

			Post-treatment
		Pretreatment	1 month	3 months	6 months	12 months	24 months	36 months	48 months	60 months
TLPMA	Number of patients	79	79	79	78	74	69	57	39	18
	Uterine volume (cm^3)	178.1 ± 60.5	107.5 ± 37.6	92.2 ± 31.5	86.9 ± 31.3	81.3 ± 33.1	77 ± 35.5	69.1 ± 37.7	71.7 ± 45.4	61.8 ± 48.5
	Lesion volume (cm^3)	69.8 ± 42.5	35.7 ± 18.4	29.5 ± 15.1	26.9 ± 12.9	27.3 ± 15.9	26.8 ± 15.3	25.3 ± 18.2	29.4 ± 24.9	27.6 ± 31
	SQC	4.3 ± 0.5	2.3 ± 0.6	2.3 ± 0.7	2.3 ± 0.8	2.3 ± 0.9	2.2 ± 1.2	2 ± 1.3	2.2 ± 1.3	1.8 ± 1.4
	VAS	8.4 ± 1	2.3 ± 1.7	2.3 ± 1.7	2.5 ± 1.9	2.6 ± 1.9	2.6 ± 2.2	2.4 ± 2.3	2.9 ± 3.1	2.1 ± 3.1
LNG-IUS	Number of patients	44	44	0	44	44	42	37	35	31
	Uterine volume (cm^3)	147 ± 70.5	122.6 ± 67.8		127 ± 70.9	139.7 ± 85	140.8 ± 82.9	136.4 ± 98.3	115.5 ± 62.3	124.2 ± 123
	Lesion volume (cm^3)	36.1 ± 22	33.1 ± 22.4		28.3 ± 21.3	26.8 ± 21.6	33.5 ± 26.9	28.8 ± 20.4	29.4 ± 22.2	26.3 ± 21.4
	SQC	4.1 ± 0.6	2.2 ± 0.4		2.1 ± 0.4	2.2 ± 1	2.3 ± 0.9	2.3 ± 0.9	2.2 ± 1.2	2.1 ± 1.3
	VAS	7.8 ± 1.4	3.1 ± 1		3 ± 1.2	3.3 ± 1.8	3.2 ± 1.7	2.9 ± 1.8	2.7 ± 2.3	2.7 ± 2.4

TLPMA: transvaginal ultrasound- and laparoscopy-guided percutaneous microwave ablation; LNG-IUS: levonorgestrel-releasing intrauterine system; SQC: sensation quantity scale; VAS: visual analog scale.

Discussion

Our findings demonstrated in this study, we introduce several advantages of laparoscopy before, during, and after MWA. First, before MWA, laparoscopy allows the detection and removal of small cysts, small fibroids, especially small malignant lesions, and adhesions that cannot be resolved through MWA alone (Figure 2(A)). Second, it provides a safe space and observation field for ablation in order to separate the ablated adenomyoma from the surrounding organs, pelvic wall, and abdominal wall, and thus ensure the safety of ablation (Figure 2(B)). Third, it allows observation of blood vessels in the abdominal/uterine wall during the needle insertion process as well as monitoring of puncture and ablation needles entering the abdominal/uterine wall to prevent and stop bleeding (Figure 2(C)).

Figure 2. Laparoscope images before ablation. (A) Laparoscope image shows adhesions; (B) Laparoscope image shows the safe space and observation field for the ablation; (C) Laparoscope image shows the blood vessels in the abdominal wall during the needle insertion process.

During the MWA process, laparoscopy allows observation of the ablation effect (including changes in the color, shape and size of the uterine surface, as well as changes in blood vessels) (Figure 3(A)). Moreover, it facilitates ablation in the following aspects: (1) Thermal insulation: overhead thermal insulation, cotton yarn heat insulation, water injection heat insulation (Figure 3(B)). (2) The suture is used to raise the uterus, which allows the safe insertion of the puncture needle for adenomyoma ablation. (3) The wound surface was cleaned to facilitate observation of changes in the uterine surface (Figure 3(C)).

Figure 3. Laparoscope images during ablation. (A) Laparoscope image shows the color changes of the uterine surface; (B) Laparoscope image shows the cotton yarn heat insulation to get a safe space; (C) Laparoscope image shows a clean wound surface during ablation.

After MWA, laparoscopy allowed wound flushing and cleaning of the field of vision (Figure 4(A)). Second, laparoscopy allows assessment of the condition of the uterus and surrounding organs (including the intestine, bladder, pelvic wall and abdominal wall). Specifically, in case bleeding or effusion is detected, they can be stopped or aspirated, respectively (Figure 4(B)). In addition, it can be used as an anti-adhesion treatment.

Figure 4. Laparoscope images after ablation. (A) Laparoscope image shows the process of flushing the wound and cleaning the field of vision; (B) Laparoscope image shows the process of checking the condition of the uterus and surrounding organs after ablation.

Additionally, the role of transvaginal ultrasound in MWA is important. Compared with transabdominal ultrasound, transvaginal ultrasound allows more accurate measurement of various distances. Further, transvaginal ultrasound allows more accurate observation of the needle insertion; the angle, direction and depth of the needle path; and the interaction with the endometrium (parallel) (Figure 5(A)). Specifically, it can measure the distance between the ablation needle tract, endometrium, and uterine serosal layer. Moreover, it facilitates observation of the process and scope of ablation and vaporization (Figure 5(B, C)), as well as the distance from the needle to the endometrium.

Figure 5. Transvaginal ultrasound images of the uterus. (A–C) Hyperechogenic signal under transvaginal ultrasound guidance indicates the ablation area, and the scope of the hyperechogenic signal becomes more and more larger. The red dots: the direction of the endometrium; the long arrow: the position of the ablation needle path; the short arrow: the position of the needle tip; the red circle: the range of ablation gasification and with the continuous progress of ablation, the range of strong echo gasification gradually increases.

Adenomyosis is a common pathological uterine condition. Recently, patients with adenomyosis have preferred less invasive treatment options compared with hysterectomy. Further, there is a need to develop a feasible and safe method that can avoid the potential risks associated with PMWA.

Under the guidance of transabdominal ultrasound, PMWA can effectively relieve symptoms, improve microwave heat efficiency and reduce the treatment duration [26]. Yang et al. evaluated the efficacy of PMWA guided by transabdominal ultrasound in 142 women with adenomyosis [12]. Although this technique only requires local anesthesia and is easy to perform, it still has several drawbacks. The intestine may interfere with antennal insertion; moreover, thermal ablation only guided by transabdominal ultrasound may cause severe complications, including penetration of other pelvic organs, thermal damage and abdominal bleeding, especially among patients with adhesions between the uterus and surrounding organs [27–29].

During PMWA, artificial ascites can be used to achieve a clear antenna path and prevent damage to the surrounding organs [30]. However, artificial ascites cannot separate adhesions between the uterus and surrounding organs; additionally, it cannot reduce heat conduction from the uterus to other organs through adhesions.

We previously introduced laparoscopy to separate pelvic adhesions and provide a wide antenna path. Laparoscopy can be used to observe the uterine surface and bowel movement; further, it can be combined with PMWA to reduce the potential risk. We previously observed pelvic adhesions between the uterus and surrounding organs in 51% of patients (36/70), which could be detached using a laparoscope at least to the cervical level. There was a significant post-TLPMA decrease in the uterine and lesion volume, which remained stable during the long-term follow-up. The uterine volume in the TLPMA group was smaller than that in the LNG-IUS group during the long-term follow-up. Further, the SQC and VAS scores were significantly reduced, which indicated the effectiveness of this method [3].

This study has several limitations. First, this was a prospective study and not a randomized controlled study, the basic clinical characteristics and main prognostic factors of the experimental group and the control group may be unevenly distributed, which is easy to bias the research results, reduce the authenticity of the research results. Second, the lesion boundary was unclear; additionally, subjective factors may have affected the judgment of the extent of ablation.

In conclusion, TLPMA is a feasible, minimally invasive technique for treating adenomyosis. It is an effective treatment option with excellent long-term outcomes and no severe side effects; therefore, it may be a good choice for the treatment of adenomyosis.

Acknowledgments

We thank all participants recruited for this study.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability

The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.

Additional information

Funding

This work was supported by the Health and Family Planning Commission of Wuhan Municipality (WX21C36).