Combined transabdominal and transvaginal ultrasound-guided percutaneous microwave ablation of uterine myomas: an effective monitoring technique

Abstract Objective This study compared the feasibility and efficacy of transabdominal ultrasound (TAU) and combined transabdominal and transvaginal ultrasound (TA/TV US)-guided percutaneous microwave ablation (PMWA) for uterine myoma (UM). Method This study enrolled 73 patients with UM who underwent PMWA via the transabdominal ultrasound-guided (TA group) or the combined transabdominal and transvaginal ultrasound-guided (TA/TV group) approaches. The intraoperative supplementary ablation rates, postoperative immediate ablation rates, lesion reduction rates and other indicators three months postoperatively were compared between the groups. The display of the needle tip, endometrium, uterine serosa, rectum and myoma feeding vessels under the guidance of TAU, transvaginal ultrasound (TVU) and TA/TV US were evaluated in the TA/TV group. Results In the TA/TV group, the real-time position of the needle tip and the endometrium complete display rate of the same lesions with TVU guidance were significantly higher than those using TAU. TA/TV US guidance significantly improved the complete display rate of each indicator. The intraoperative supplementary ablation rate in the TA/TV group was lower than that in the TA group. Similarly, the postoperative immediate ablation and volume reduction rates of the lesions three months postoperatively were higher than those in the TA group, especially for lesions with a maximum diameter ≥6 cm. Conclusion TA/TV US is an effective monitoring method that can be used to improve imaging display. Its use is recommended in patients with obesity, poor transabdominal ultrasound image quality and large myoma volumes.


Introduction
Uterine myoma (UM) is the most common benign gynecological tumor among people of reproductive age.At present, the main treatment methods involve drugs, minimally invasive treatments, and surgical treatments.Some patients discontinue drug therapy because of a lack of desired response or side effects from the drugs.Hysterectomy is not applicable in patients who wish to retain their uterus.With the development of medical technology, minimally invasive treatments have received increasing clinical attention, such as laparoscopic myomectomy, hysteroscopic submucous myomectomy, and uterine artery embolization, among others.In addition, image-guided ablation is a novel and minimally invasive treatment modality for patients wishing to preserve their uterus [1][2][3].Image-guidance technologies, such as magnetic resonance imaging (MRI) and ultrasound, play a crucial role in percutaneous, transvaginal and transcervical thermal ablation, which are used for the treatment of UM.These image-guidance technologies enable planning the needle course and formulating a treatment plan before surgery.Spatial guidance simplifies the process of reaching the target lesion during surgery.Moreover, it is helpful to monitor the ablation process in real-time and improve the safety and treatment effects.This method is also used to evaluate treatment efficacy postoperatively [4,5].The affordable price, convenience, real-time application, and lack of ionizing radiation have led to the widespread application of ultrasound in the diagnosis, monitoring and treatment of UM [6].Transabdominal ultrasound (TAU) and transvaginal ultrasound (TVU) are used in the ultrasound monitoring of microwave ablation (MWA) for UM [7][8][9].TAU-guided percutaneous microwave ablation (PMWA) of benign uterine lesions is conducive to selecting the best puncture path.The bowel or mesentery in front of the uterus can be pushed away by pressurizing the probe to insert the needle further; however, gas with a strong echo signal, generated by heating the tissue during ablation, shadows the needle tip and posterior tissue structure.This often hinders the complete image from being displayed, resulting in incomplete ablation or complications [10], especially in the case of high-risk lesions adjacent to the rectum.TVU can be used to observe the uterus and the surrounding organs [11]; moreover, it can display the position of the needle tip, its distance from the endometrium and serosa, and the diffusion range of the strong echoes during ablation more clearly and thoroughly.However, the scan depth is shallow, and the scan range is limited because of the probe frequency and mobility angle; hence, it is difficult to display multiple or large myomas, and the image quality is often degraded [12].Whether combined transabdominal/transvaginal ultrasound (TA/TV US) guidance and monitoring can complement each other to display the lesions, needle tip, and surrounding tissues more vividly and thoroughly, as well as monitor the ablation therapy more safely and effectively, warrants further exploration.No previous studies on TA/TV US-guided thermal ablation for the treatment of UM have been reported.Therefore, the present study investigated the feasibility and efficacy of TA/TV US monitoring of PMWA for the treatment of UM.

Research participants
This study included patients with symptomatic UM who underwent US-guided PMWA treatment at our hospital between July 2019 and December 2021.The inclusion criteria were as follows: (1) patients diagnosed with UM by ultrasound and magnetic resonance imaging (MRI) before surgery and whose lesions were classified as type 1-6 according to the International Federation of Gynecology and Obstetrics (FIGO); (2) patients with one or more clinical symptoms and whose conditions were not improved or were aggravated after treatment with medications or other conservative therapies; (3) patients with an available safe transabdominal puncture course; (4) patients with no signs of perimenopause and (5) patients who strongly wished to preserve their uterus, refused to accept other treatments, and voluntarily accepted ablation treatment.The exclusion criteria were as follows: (1) patients with FIGO type 7 UM; (2) postmenopausal patients; (3) patients in the acute inflammation stage; (4) patients in whom malignant tumors could not be excluded; (5) patients who could not tolerate anesthesia and interventional surgery owing to cardiopulmonary insufficiency or serious cardiovascular or cerebrovascular diseases; (6) patients with severe coagulation dysfunction; (7) patients with a history of interventional therapy such as uterine artery embolization and high-intensity focused ultrasound and (8) patients with atypical endometrial hyperplasia.This study included 73 patients with UM, divided into the combined TA/TV US and TAUguided treatment groups according to their willingness to accept combined transvaginal ultrasound monitoring.The TA group included 37 patients with 45 myomas, while the TA/ TV group included 36 patients with 40 myomas.This study was approved by the Ethics Review Committee of our hospital (ethics number: [2021] Ethics Committee Approval for Scientific Research No. 151).All patients provided informed consent before surgery for the publication of any images or data included in this article.

Instruments and materials
Ultrasound was performed using a color Doppler ultrasound diagnostic instrument (Philips EPIQ 5; Philips, Amsterdam, Netherlands) equipped with a convex array probe (C5-1) and a vaginal ultrasound probe (C10-3V).Ablation was performed using a Nanjing Kangyou KY-2000 type cold-cycle microwave ablation therapeutic instrument with a needle antenna (KY2450B).Contrast-enhanced ultrasonography (CEUS) was performed using SonoVue sulfur hexafluoride microbubbles.

Preoperative preparation
All patients understood the treatment principles, protocols, expected effects, complications, and possible alternative treatments before undergoing ablation.Anticoagulants or antiplatelet drugs were discontinued five to seven days before surgery.Ablation was performed three to seven days after the last day of menstruation.Intrauterine devices were removed prior to surgery.
Preoperative questionnaires, including the Uterine Fibroid Symptom and Quality of Life (UFS-QOL) scores and menstrual volume scores, were completed.The UFS-QOL score was divided into the symptom severity score (SSS, items 1-8) and the health-related quality of life (HRQL, items 9-37) score [13].Menstrual volume was scored on a five-point scale according to the patient's description: normal (one point), mildly increased (two points), moderately increased (three points), severely increased (four points) and extremely severely increased (five points) [14].
All patients underwent gynecological TA and TV US to determine the number, location, size, shape, FIGO classification, and blood supply of the myoma, as well as its relationships with the surrounding structures.The volume of the myoma was calculated using the following equation: myoma volume (cm 3 ) ¼ upper and lower diameter (cm) Â left and right diameter (cm) Â anteroposterior diameter (cm) Â 0.523.Routine blood tests, coagulation function, routine leucorrhea examinations, screening tests for cervical cancer, pelvic enhanced MRI and electrocardiography were completed.Patients were instructed to refrain from consuming solids and liquids for 6 h before surgery.Placement of an indwelling catheter and bowel preparation were undertaken when necessary.Wet vaginal gauze was applied during the ablation of lesions close to the endometrium in the TA group.

Operation methods
(1) Before initiating ablation, CEUS was performed to assess the scope of the lesion and the surrounding and internal blood supply; the presence of a main feeding vessel was also confirmed.Artificial ascites was established.The distance between the uterus and the adjacent structures was >0.5 cm during surgery.Normal saline was dripped continuously into the pelvic cavity during ablation.
(2) TA group: the ablation needle was advanced into the lesion under real-time TAU guidance.The ablation instrument was then turned on, with an ablation power of 50-65 W. The ablation needle was moved from deeper to shallower regions to ablate the lesion layer-by-layer until it was completely covered by strong echoes.Ablation was then discontinued (Figure 1(A)).
TA/TV group: TAU and TVU were used to guide the movement of the single needle to ablate the same lesion layer-bylayer in the same patient (Figure 1(B)).During the surgery, the images displayed for the different guidance techniques were evaluated to assess whether the needle tip, uterine serosa, endometrium, rectum and the vessels feeding the myomas were completely displayed for TAU, TVU or TA/TV US guidance and recorded.During TAU or TVU-guided ablation, the needle tip, endometrium, uterine serosa, rectum, and myoma feeding vessels can be fully displayed, defined as complete display.Incomplete display was defined as instances in which some areas could not be displayed; complete display on TA/TV US was defined as a full display by TAU or TVU; similarly, if neither technique fully displayed the situation, the display was defined as incomplete.
(3) CEUS was performed immediately after the dissipation of bubbles in the thermal field after ablation to evaluate the perfusion of the ablated area.Supplementary ablation was performed if the ablation was insufficient.The number of myomas undergoing supplementary ablation was recorded.Intraoperative supplementary ablation rate ¼ the number of myomas undergoing supplementary ablation/the total number of myomas Â 100%.Areas without perfusion were observed in the lesions after full ablation.Three diameters were measured in three perpendicular planes and the nonperfusion volume (NPV) was calculated as follows: NPV (cm 3 ) ¼ upper and lower diameter (cm) Â left and right diameter (cm) Â anteroposterior diameter (cm) Â 0.523.The postoperative immediate ablation rate was calculated using the following formula: NPV immediately after surgery/myoma volume before surgery Â 100%.All CEUS procedures were performed by the same physician, who had >3 years of experience in CEUS.

Postoperative follow-up and adverse reactions and complications
Patients were reexamined three months after surgery and completed the UFS-QOL and menstrual volume score assessments.Gynecological color Doppler ultrasound was performed to calculate the myoma volume and reduction rate (myoma reduction rate ¼ [preoperative myoma volume À current myoma volume]/preoperative myoma volume Â 100%).Intraoperative and postoperative adverse reactions and complications were recorded.Serious or life-threatening adverse reactions or complications were defined as severe adverse reactions or complications, while symptoms requiring only symptomatic treatment or no treatment were defined as minor adverse reactions or complications.

Statistical analysis
Data were analyzed using SPSS Statistics (version 25.0;IBM Corp., Armonk, NY, USA).Normally distributed measurement data were expressed as X 6S and analyzed using independent-samples t-tests.Non-normally distributed measurement data were expressed as median P 50 (P 25 , P 75 ) and analyzed using nonparametric rank-sum tests.Enumeration data were expressed as frequency or percentage and analyzed using v 2 tests or Fisher's exact test.McNemar's test was used to compare the complete display rates of images of the same lesions according to the different guidance techniques.The differences were considered statistically significant at p < .05. 3. Results

Comparisons of clinical baseline data
In this study, there were no significant differences in age, lesion classification, lesion location, largest lesion diameter, preoperative lesion volume, hemoglobin (Hb), SSS, HRQL, and menstrual volume scores between the two groups (Table 1).

Image displays of the same lesions with different guidance techniques in the TA/TV group
The complete display rates of the TVU-guided needle tip and endometrium of the same lesion were significantly higher than those of TAU (p < .001);however, the displays of the uterine serosa, rectum, and feeding vessels did not differ significantly between the groups (p > .05).TA/TV US guidance significantly improved the complete display rates of the needle tip, uterine serosa, endometrium, rectum, and myoma feeding vessels (p < .001),as shown in Table 2 and Figure 2. Artificial ascites helped improve the identification of the uterus against surrounding tissues (Figure 3).

Intraoperative supplementary ablation rate and postoperative efficacy analysis
All patients underwent intraoperative CEUS and supplementary ablation for areas with insufficient ablation and completed the three-month follow-up.The results suggested that the intraoperative supplementary ablation rate in the TA/TV group was lower than that in the TA group.The TA/TV group also showed significantly higher postoperative immediate ablation and lesion volume reduction rates three months after the surgery compared with those in the TA group (p < .05).According to the myoma size and type, the results indicated that the postoperative immediate ablation rates of the lesions with maximum diameters !6 cm and of type III-IV, V-VI, and II-V were higher in the TA/TV group than those in the TA group (p < .05).The Hb, SSS, HRQL, and menstrual volume values in the two groups had improved three months after surgery; however, the differences were not statistically significant (p > .05)(Table 3).

Adverse reactions and complications
No patients in either group experienced serious adverse reactions or complications, such as uterine perforation or pelvic organ injury, during surgery.Minor adverse reactions and complications after the operation included vaginal discharge, pain at the surgical site, fever, and pelvic infection.Vaginal discharge was mostly brown, pale pink, or pale yellow, with durations varying from 0 to 60 days, and resolved spontaneously.Pain at the surgical site was tolerated without specific treatment and resolved spontaneously within three days.Two patients experienced postoperative fever and pelvic infection that resolved after treatment with antibiotics.One patient with low fever recovered to normal after physical cooling.The incidence of various adverse reactions and complications did not differ significantly between the TA and TA/ TV groups (p > .05)(Table 3).

Discussion
The results of the present study showed that both TAU and TA/TV US could safely and effectively monitor PMWA for the treatment of symptomatic UM and lead to an improvement in symptoms.TA/TV US monitoring can significantly improve the complete display rate of images, reduce the intraoperative supplementary ablation rate, and improve the postoperative immediate ablation and lesion reduction rates three months after surgery.It can compensate for the insufficiency of simple TAU monitoring.TVU was used to observe the uterus and adjacent organs at a close distance owing to the higher resolution of the probe and its ability to display some tissues that are difficult to visualize using TAU [11].The results confirmed that TVU facilitated the complete display of the needle tip and endometrium, which ensured a safe distance for ablation.Although there was no significant difference in the display of uterine serosa, rectum, and feeding vessels between TAU and TVU in the TA/TV group, when the two guidance methods were combined, they improved display and significantly improved the complete display rate of each observation index.
No severe adverse reactions and complications were observed in the TA or TA/TV groups in this study.Nevertheless, the adverse reactions and complications associated with PMWA in the treatment of UM should be considered.Hyo et al. [15] reported the case of a patient with intramural UM and pelvic endometriosis who developed a fistula between the posterior uterine wall and the rectum after undergoing combined laparoscopy and TVU-guided percutaneous thermal ablation.Tan et al. [16] reported three cases of ileal fistula that occurred after microwave ablation of adenomyosis and UM, among which the UM in one case was located in the posterior wall with a maximum diameter of approximately 5.4 cm.The patient had no history of previous surgery or radiotherapy in the area to be ablated and surrounding areas.One of the high-risk factors for injury may be poor visibility of the needle tip due to strong gas echoes.Therefore, a clear and complete display of the needle tip, lesions and surrounding tissues during the operation can reduce the risk of complications resulting from judging the position of the needle tip by retracting the needle rod or repeated puncture.In addition, artificial ascites can expand the space between the uterus and the surrounding tissues, improve the image display quality [17] and limit the damage caused by heat conduction to surrounding organs.
Three months after surgery, the lesions in both the TA/TV and TA groups were significantly reduced, and clinical symptoms improved compared to before the surgery.The reduction rate of the lesions with the largest diameter !6 cm in both groups was lower than that of those with the largest diameter <6 cm.Jiang et al. [18] divided patients with UM into two groups according to the average diameter ( 5 cm and >5 cm to 8.5 cm).The reported reduction rates of the myomas three months after surgery were approximately 57.6% and 51.4%, respectively.Kim et al. [19] reported myoma reduction rates in two groups with average diameters <8 cm and !8 cm as 58.7% and 49.9%, respectively, three months after thermal ablation.The results of the previous studies and the current study suggest that larger lesions lead to lower postoperative reduction rates.It is worth noting that the volume reduction rate of lesions in the TA/TV group three months after surgery in the present study was significantly higher than that in the TA group, especially for lesions with a maximum diameter !6 cm.Therefore, the use of TA/TV US for monitoring PMWA treatment of larger myomas showed considerable value.Kanaoka et al. [20] studied the relationships among the parameters related to the reduction rate of myomas after thermal ablation and reported that the postoperative immediate ablation rate was closely related to the reduction rate.The higher the postoperative immediate ablation rate, the more significant the lesion reduction.Zhao et al. [21] also verified this result.In the present study, the TA/TV group used TA/TV US guidance to display the different types of lesions and their distances from surrounding tissues more clearly and achieved the largest range of ablation while ensuring safety.When ablating V-VI and II-V myomas, the complete display of the needle tip, uterine serosa and rectum is conducive to ablating the parts of the myoma closest to the uterine serosa and reducing the risk of the needle penetrating the uterine serosa leading to damage to the rectum.When ablating type I-II, III and II-V myomas, especially in patients with a desire to retain fertility, a clear and complete display of the endometrium and the needle tip can ensure that the needle tip can avoid the endometrium and accurately puncture the lesion, thereby preventing thermal damage to the endometrium, reducing the risk of intrauterine adhesions and facilitating the ablation of parts of myomas closest to the endometrial border.Additionally, the complete display rate of the feeding vessels of the myomas under TA/TV US guidance was significantly improved.The feeding vessels of the myomas are preferentially and effectively blocked to weaken the heat sink effect caused by blood flow during the surgery.This preferential and effective blocking can increase the rate of temperature increase of the tissue surrounding blood vessels in the ablation area to avoid a smaller-than-expected actual ablation range, as the temperature is not sufficiently high to cause tissue coagulation and necrosis, thereby further improving the postoperative immediate ablation rate [22][23][24].
The limitations of this study were its single-center design, small sample size and short follow-up duration.Therefore, future studies with larger sample sizes are needed.Moreover, the conclusions of the present study require verification using long-term follow-up periods in multi-center prospective studies.
In conclusion, TA/TV US is an effective monitoring method that can be used to improve imaging display.Its use is recommended in patients with obesity, poor transabdominal ultrasound image quality, and large myoma volumes.

Figure 2 .
Figure 2. TA/TV US-guided PMWA for the treatment of UM. A. TAU disturbed by strong echo, in which the needle tip is not clearly displayed (white arrow).B. TVU is not disturbed by strong echo, with clear display of the needle tip (white arrow).C. The strong echo generated by ablation under TAU monitoring interferes with the display of the posterior tissue.D. Clear display of the posterior tissue and part of uterine serosa in TVU monitoring.TA/TV: combined transabdominal and transvaginal; US: ultrasound; PMWA: percutaneous microwave ablation; UM: uterine myoma; TAU: transabdominal ultrasound; TVU: transvaginal ultrasound

Figure 3 .
Figure 3. US-guided establishment of artificial ascites and PMWA treatment for UM.A-B.Artificial ascites (white stars) form a water barrier between the uterus and surrounding tissue structures, allowing a clear display of the uterine serosa.US: ultrasound; PMWA: percutaneous microwave ablation; UM: uterine myoma.

Table 1 .
Comparison of clinical baseline data before treatment for uterine myomas in the TA group and the TA/TV group.

Table 2 .
Image display of the same lesion in the same patient in the TA/TV group according to guidance technique.

Table 3 .
Intraoperative supplementary ablation, postoperative efficacy and safety comparison of PMWA treatment for uterine myomas according to different guidance technique.