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ORIGINAL ARTICLE
Year : 2020  |  Volume : 16  |  Issue : 2  |  Page : 365-371

Use of contrast-enhanced ultrasound in evaluating the efficacy and application value of microwave ablation for adenomyosis


1 Department of Oncology, The Tumor Hospital of Liaocheng, Liaocheng, China
2 Department of Radiology, The Tumor Hospital of Liaocheng, Liaocheng, China
3 Department of Ultrasound, The Tumor Hospital of Liaocheng, Liaocheng, China

Date of Submission14-Nov-2018
Date of Decision27-Nov-2018
Date of Acceptance01-Jan-2020
Date of Web Publication28-May-2020

Correspondence Address:
Yingying Zhao
Department of Ultrasound, The Tumor Hospital of Liaocheng, Liaocheng 252000, Shandong
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_769_18

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 > Abstract 

Aim: This study aims to assess the use of contrast-enhanced ultrasonography (CEUS) and dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) in the evaluation of percutaneous microwave ablation (PMWA) of localized adenomyosis.
Materials and Methods: Sixty-six patients with single-onset adenomyosis who underwent PMWA at the Liaocheng Tumor Hospital of Shandong Province from January 2013 to February 2019 were enrolled. Venous CEUS and DCE-MRI examinations were performed before and 1-2 days after the surgery. The ablation rates calculated by CEUS and DCE-MRI were compared and analyzed for accuracy.
Results: After microwave ablation (MWA), CEUS showed that the volume and ablation rate of the ablated zone were 52.03 28.39 cm3 and 90.90% 6.61%, respectively. By DCE-MRI, the ablation volume and ablation rate of adenomyosis were 52.20 28.65 cm3 and 90.88% 6.32%, respectively. Dysmenorrhea was significantly relieved within 3 months of the operation, and nonmenstrual hemoglobin levels were significantly improved at 3 and 6 months after the operation (P < 0.05). All 66 cases of adenomyosis were treated using PMWA. Postoperatively, 17 patients reported a change in vaginal fluid; however, no special treatment was required as this disappeared 2-11 days after surgery.
Conclusions: CEUS can accurately evaluate the ablation rate of localized adenomyosis treated with MWA, which is consistent with DCE-MRI. It is convenient and easy to perform ablation of adenomyomas, with incomplete ablation and angiography, and is a method worthy of clinical promotion.

Keywords: Adenomyosis, contrast agent, magnetic resonance imaging, microwave ablation, ultrasound


How to cite this article:
Xu C, Tang Y, Zhao Y, Li Y, Feng Q. Use of contrast-enhanced ultrasound in evaluating the efficacy and application value of microwave ablation for adenomyosis. J Can Res Ther 2020;16:365-71

How to cite this URL:
Xu C, Tang Y, Zhao Y, Li Y, Feng Q. Use of contrast-enhanced ultrasound in evaluating the efficacy and application value of microwave ablation for adenomyosis. J Can Res Ther [serial online] 2020 [cited 2020 Jul 16];16:365-71. Available from: http://www.cancerjournal.net/text.asp?2020/16/2/365/285199




 > Introduction Top


Adenomyosis is a benign lesion of the female reproductive system caused by endometriosis of the myometrium. It results in uterine enlargement, excessive menstrual volume, dysmenorrhea, anemia, and other clinical manifestations. Severe symptoms can seriously affect work and life.[1],[2] Noninvasive and minimally invasive therapeutic techniques for adenomyosis have been developed rapidly in recent years.[3] As a minimally invasive treatment, microwave ablation (MWA) has been applied in the treatment of various solid tumors.[4],[5],[6],[7] Ultrasound-guided percutaneous MWA (PMWA) is an effective alternative treatment for symptomatic adenomyosis, with advantages of convenient operation, minimal trauma, safety, effectiveness, short treatment time, less pain for patients, and less adverse reactions.[8],[9],[10],[11],[12] Contrast-enhanced ultrasonography (CEUS) is important in the diagnosis and efficacy evaluation of liver and kidney tumors, breast diseases, gynecological benign and malignant tumors, and other multiorgan diseases.[13],[14],[15] CEUS and dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) have been applied to evaluate the efficacy of MWA for various tumors.[7],[16],[17] In this study, ultrasound ablation and DCE-MRI were performed on 66 patients with localized adenomyosis. Contrast-enhanced ultrasound and DCE-MRI were used to evaluate the effect of MWA. The clinical efficacy and adverse reactions were observed.


 > Materials and Methods Top


Patients

From January 2013 to February 2019, adenomyosis patients diagnosed with dysmenorrhea (66 cases) and menorrhagia (59 cases) underwent MWA by CEUS and DCE-MRI at the Liaocheng Tumor Hospital of Shandong Province. Sixty-six patients were enrolled, all aged between 32 and 54 years and with single-onset localized lesions (14 in the anterior wall, 34 in the posterior wall, and 18 in the lateral wall). The average patient age was 44.44 ± 6.43 years. Inclusion criteria for the study were as follows: (1) the presence of obvious clinical symptoms, including menorrhagia, prolonged menstruation, progressive dysmenorrhea, and anemia; (2) no need to maintain fertility; (3) no significant improvement in symptoms following conservative treatment with drugs; (4) no use of hormonal drugs within the 3 months prior to MWA; (5) there is a safe transabdominal wall puncture path; and (6) no signs of perimenopause. Exclusion criteria for the study were as follows: (1) need to maintain fertility; (2) patient was undergoing a menstrual period, pregnancy, or lactation; (3) Grade 3 or higher cervical intraepithelial neoplasia; (4) the presence of endometrial atypical hyperplasia; (5) the presence of acute pelvic inflammation; (6) the presence of serious organ diseases (i.e., heart, brain, and liver), malignant tumors, and blood diseases; and (7) contraindications for MRI. The use of ultrasound-guided PMWA was approved by our ethics committee, and all patients signed informed consent forms before undergoing treatment.

Instruments

Treatment was carried out using the Nanjing Yigao dual-source MWA therapy device, with a frequency of 2450 MHz and power of 40–120 W. We used a water-cooled circulating low-bar temperature 15 G microwave antenna, with a front microwave radiation length of 1.1 cm. The ultrasound system utilized was a GE Logiq E9 color Doppler ultrasound system with a probe frequency of 3.5–5.5 MHz and a puncture guide, which used low mechanical index imaging. MRI was performed using a GE 1.5 T magnetic resonance instrument.

Methods

Preoperative routine ultrasonography and CEUS were performed to determine the location, internal and peripheral blood flow, and size of the lesion. The best puncture point and needle route were chosen according to the ultrasound results. During the procedure, a routine disinfection drape, 1% Lido Cain localized anesthesia, and intravenous analgesia were used. The number of ablation needles used was chosen according to the size of the lesion (double needles were chosen when lesions were >5 cm). Under the guidance of ultrasound, the lesion was percutaneously punctured with the MWA needle; the MWA instrument was then turned on and the power output was set to 50 W or 60 W. Initially, high echo gasification appeared in the lesion and gradually expanded. During the ablation process, ultrasound monitored echo changes and thermal field diffusion in the ablation zone in real time, at various angles in the three-dimensional space. Ablation was stopped when the hyperechoic reached the edge of the predetermined ablation area about 0.3 cm. Changes in the endometrium and intrauterine echo were monitored, and the microwave radiation was stopped once a hyperechoic flow was detected in the endometrium or intrauterine cavity to prevent endometrial thermal damage.[18]

Dynamic contrast-enhanced magnetic resonance imaging evaluation methods and criteria

MRI and enhanced scans were performed before and 1–2 days after treatment, and a Magenwei contrast agent was injected uniformly through the elbow vein at a dose of 0.1 mmol/kg to make sagittal plane. The horizontal axis T1-weighted image (T1WI)-enhanced scanning and the imaging parameters are dynamic-enhanced scanning, and time of repetition (TR) is 6.6 ms, time of echo (TE) is 2.5 ms, and cross-section TR = 5.8 ms TE = 2.1 ms. Pre- and post-operatively, the maximum length diameter (a), maximum transverse diameter of the sagittal plane (b), anteroposterior diameter (c), and the maximum postoperative diameter (a, b, c) of the lesion or area without enhancement were measured, respectively.[19] The volume of the lesion or nonenhanced zone was calculated according to the formula: volume (V) = 4/3 πR3 (R = average radius). The lesion ablation rate was calculated as follows: ablation rate = postoperative adenomyosis volume without an enhanced zone/preoperative lesion volume ×100%.[20]

Intravenous contrast-enhanced ultrasonography evaluation method and standard

We rapidly injected 5.0 ml of a 0.9% sodium chloride solution into a SonoVue contrast agent bottle, which was shaken to ensure complete dissolution. A 2.4 ml suspension was extracted and injected intravenously, followed by a 5.0 ml quick bolus of 0.9% sodium chloride solution. CEUS was performed on the same day as DCE-MRI, before and after MWA. After ablation, the coagulative necrosis of the lesion formed a nonperfusion area. The upper and lower diameters of the maximal plane of the longitudinal incision were measured, before and after ablation. The diameter of the nonperfusion zone is calculated according to the formula: Volume (V) = 4/3 πR3 (R = average radius). The ablation rate postoperative adenomyosis volume/preoperative lesion volume × 100%.

Clinical effects and adverse reactions

The degree of dysmenorrhea was evaluated both 1–2 days before and 3–6 months after treatment. Dysmenorrhea was scored out of ten points using a self-evaluation questionnaire as follows:[21] one–two points (no obvious dysmenorrhea), three–four points (mild dysmenorrhea, can tolerate pain, does not affect life or sleep, painkillers not needed), five–six points (moderate dysmenorrhea, cannot endure pain, affects sleep, need to use painkillers), seven–eight points (severe dysmenorrhea, cannot stand, severely interferes with sleep, may be accompanied by autonomic dysfunction or passive position, analgesics must be used), and nine–ten points (dysmenorrhea cannot be tolerated, accompanied by vomiting, unable to live and work normally). Hemoglobin concentrations were measured 3 and 6 months after treatment. The following are the evaluation criteria for MWA:[22],[23],[24],[25] (1) complete remission (dysmenorrhea score of zero after MWA), (2) treatment effect is very significant (dysmenorrhea score ≥4 points upon review, pain was significantly, if not completely, relieved, the nonmenstrual hemoglobin concentration was normal or >3 g/L after MWA), (3) treatment effect was remarkable (dysmenorrhea score decreased by ≤4 points on review and the dysmenorrhea was partially relieved, the nonmenstrual hemoglobin concentration increased by ≥2 g/L before MWA), (4) effective treatment (the nonmenstrual hemoglobin concentration increased by 1 g/L before MWA), (5) ineffective treatment (there was no significant change between the dysmenorrhea scores before and after MWA), and (6) aggravation (the dysmenorrhea score was higher after than before MWA).

We observed patients for signs of pain, skin burns, bleeding, pelvic effusion, vaginal drainage, pelvic infection, uterine rupture, large areas of endometrial thermal injury, and other complications, both during and after PMWA surgery.

Statistical analysis

Statistical analyses were performed using the SPSS 19.0 statistical software. The volume and ablation rate of contrast-free ultrasound and DCE-MRI after ablation of adenomyosis were expressed as-x ± s. The ablation rates calculated for CEUS and DCE-MRI were compared. Statistical significance for a paired t-test was set at P > 0.05.


 > Results Top


Contrast-enhanced ultrasonography and dynamic contrast-enhanced magnetic resonance imaging before and after ablation

Before ablation, 45 adenomyosis cases showed synchronous enhancement of the entire lesion, and 21 cases showed that the contrast agent slowly filled from the periphery to the center of the lesion. At the peak of the angiography, 66 lesions had unclear boundaries with the myometrium [Figure 1]. In the late stage of angiography, uneven and low enhancement of the lesions was observed [Figure 2]. After ablation was completed, the ablation zone was not enhanced, the edges were rough, and the posterior border of the lesion was unclear [Figure 3]. In total, three cases of incomplete ablation were computed by CEUS. For these cases, the ablation rates were 56.3%, 53.7%, and 49.3%, respectively. According to the scope of lesion enhancement, supplementary ablation was performed, and 1~2 days after surgery, ceus was performed again, and the ablation rates were calculated as follows: 84.3%, 87.4%, and 92.6% respectively. The DCE-MRI performance was assessed before and after ablation: ablation before and after injection of Magenwei contrast agents, lesions presented obvious uneven enhancement [Figure 4], melting after the completion of performance for ablation and necrotic area enhancement [Figure 5] and [Figure 6].
Figure 1: Enhancement of the lesion at the peak of contrast-enhanced ultrasonography perfusion before ablation of localized adenomyosis

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Figure 2: Contrast-enhanced ultrasonography in the late stage before ablation of localized adenomyosis

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Figure 3: Contrast-enhanced ultrasonography after completion of microwave ablation for localized adenomyosis

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Figure 4: Dynamic contrast-enhanced magnetic resonance imaging of the adenoma before ablation of adenomyosis

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Figure 5: Sagittal dynamic contrast-enhanced magnetic resonance imaging after ablation of adenomyosis

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Figure 6: Cross-sectional dynamic contrast-enhanced magnetic resonance imaging after ablation of adenomyosis

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Ablation volume and ablation rate were measured by contrast-enhanced ultrasonography and dynamic contrast-enhanced magnetic resonance imaging, before and after ablation

Before treatment, the lesion volumes in 66 patients with localized adenomyosis were calculated as 16.58–121.99 cm3, and the volume of the nonperfused area noted after performing CEUS was 16.22–108.54 cm3 and the ablation rate was 73.71%–105.25%. DCE-MRI calculated the volume of the unenhanced area in these cases as 16.38–111.79 cm3, and the ablation rate was 74.93%–107.82%.

Comparison of ablation volume and ablation rate between dynamic contrast-enhanced magnetic resonance imaging and contrast-enhanced ultrasonography after microwave ablation

The ablation volume measured by DCE-MRI and CEUS, and the calculated ablation rates after MWA of localized adenomyosis were compared, and there was no statistically significant difference between the measured values (P > 0.05) [Table 1]. A scatter diagram of the ablation rates calculated by DCE-MRI and CEUS is shown in [Figure 7].
Table 1: Comparison of the ablation volume and ablation rate between dynamic contrast-enhanced magnetic resonance imaging and contrast-enhanced ultrasonography after microwave ablation of 66 patients with localized adenomyosis (x̶±s)

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Figure 7: Scatter plot of the ablation rates calculated by dynamic contrast-enhanced magnetic resonance imaging and contrast-enhanced ultrasonography after microwave ablation of localized adenomyosis

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Evaluation of the clinical effect of percutaneous microwave ablation on adenomyosis

The average dysmenorrhea score of the 66 patients before MWA was 7.5 ± 1.3, whereas, 3 months after MWA, the average dysmenorrhea score had decreased to 3.8 ± 1.4. The average nonmenstrual hemoglobin concentration of these patients was 90.7 ± 18.5 g/L before MWA, 105.0 ± 11.9 g/L 3 months after MWA, and 122.3 ± 7.7 g/L 6 months after MWA.

Complications

The 66 patients who underwent PMWA had stable vital signs and suffered no nausea, vomiting, or other anesthetic side effects. There were no cases of pelvic infection due to the strict aseptic nature of the operation, no bleeding or pelvic fluid buildup, no vaginal mucosal scalding, and no serious uterine complications, such as rupture and extensive endometrial thermal damage. However, 29 patients experienced pain at the puncture site and ablation area after PMWA treatment, for which 18 patients were administered painkillers once. Eleven patients required no special treatment or pain relief. Within 8 h, the pain symptoms of all 29 patients were alleviated. Seventeen patients had different degrees of vaginal discharge, including one case of bloody secretions. This disappeared in all 17 patients within 2–11 days. None of the 66 patients experienced adverse effects associated with contrast agents.


 > Discussion Top


In the treatment of adenomyosis, MWA can improve the clinical symptoms, and DCE-MRI is of great significance and value in detecting the effect of localized ablation.[17],[26] CEUS images are characterized by coagulation necrosis in the effective ablation area after MWA.[16],[21] Lei et al.[21] deemed there to be good consistency between CEUS and DCE-MRI in evaluating the ablation results of benign lesions in the myometrium. Therefore, CEUS can replace DCE-MRI in the clinical evaluation of benign myometrial lesions. The authors believed that the contrast-enhanced rate of ultrasound is timelier and more intuitive when evaluating the ablation rate of localized adenomyosis by MWA.

The performance of contrast-enhanced ultrasonography

In the early stage of enhancement, 45 patients with localized adenomyosis showed synchronous enhancement of the lesion as a whole, with the blood supply and normal uterine arteries enhanced to the same degree, and the blood supply artery branching into the lesion. Consistent with the pathological characteristics of adenomyosis, lesions had a thickened torus of the uterine artery, no obvious hyperplasia and vascular network formation, no clear boundary for staining, a diffuse distribution of blood vessels in the lesion, and no inclusion formation. In the other 21 cases, early stage enhancement showed that the contrast agent slowly filled into the central area from irregular nodules or branches around the lesion. This occurs as there is a distorted or prolonged branch-like change in the uterine artery, and a branch of the hyperplastic artery that is finely meshed.[27] At the peak of angiography, the boundaries of lesions in all 66 cases were unclear with the myometrium, with uniform or uneven high enhancement. In the late stage of angiography, the lesions in all 66 cases showed uneven and low enhancement, with an unclear boundary, and where the boundary with the normal myometrium was also unclear. CEUS after ablation showed that there was no enhancement in the effective ablation area of the lesion and the area margin was rough.

The performance of dynamic contrast-enhanced magnetic resonance imaging

Before ablation of localized adenomyosis, T2WI showed a limited circular or elliptical low-signal mass in the uterine wall. There was no obvious boundary with the normal myometrium, and the occupancy effect was light, similar to the signal intensity of the binding zone. In total, 41 cases showed patchy, high-signal lesions of different sizes, and three cases showed zonal high-signal lesions. DCE-MRI T1WI showed that the enhancement intensity of lesions was significantly lower than that of the myometrium, with unclear boundaries. The original T2WI showed the high signal structure is enhanced. The presence of focal hyperintensity in lesions is associated with ectopic endometrial tissue, cystic dilation of ectopic glands, or focal hemorrhage. The reason for the occurrence of banded hyperintensity is the direct invasion of the endometrial basal layer into the uterine wall.[28] However, after ablation, no enhancement in the ablation necrosis area was observed among our 66 patients, as there was no blood perfusion in the lesion tissue after treatment.

Application of contrast-enhanced ultrasonography in evaluating the ablation rate of localized adenomyosis following microwave ablation

In this study, 66 patients with localized adenomyosis who underwent MWA were analyzed. A paired t-test was used to compare the ablation rates calculated by CEUS and DCE-MRI and no significant difference was observed between them (t = 0.084, P = 0.933). In addition, in the present study, after thefirst ablation of the three lesions in the same treatment, the immediate ablation rate was 56.3%, 53.7%, and 49.3%, respectively, indicating that the ablation was incomplete, and the supplementary ablation was accurately located according to contrast-enhanced ultrasound. Ultrasound angiography was performed 1–2 days after the operation, and the calculated ablation rates were 84.3%, 87.4%, and 92.6%, respectively. These results showed that the ablation effect was good.

Precautions after microwave ablation of localized adenomyosis

This study found that when using ultrasound contrast examination immediately after MWA treatment, a line and flaky region similar to the contrast agent filling inside the lesion ablation area, are present, which are related to the artifacts generated when the thermal field bubbles around the needle channel not completely disappearing. Careful observations revealed that this area had different image characteristics to the perfusion and regression processes of the normal myometrium; however, maintaining a static intensity at a local level does not affect the measurement of the ablation range by experienced physicians. On the edge of the lesion ablation zone, the microcirculation is still open; therefore, the contrast agent can pass through.[16] Ultrasound angiography was performed 1–2 days after MWA to accurately measure the volume without enhancement.

Previous studies have suggested that for those women who wish to maintain their fertility, disturbance of the endometrium should be avoided and the extent of ablation should be reduced.[29] The patients in this study had no need to maintain fertility. To avoid recurrence, lesions should be as thoroughly ablated as possible. Therefore, the ablation rate is higher among our patients.

Limitations of contrast-enhanced ultrasonography and dynamic contrast-enhanced magnetic resonance imaging in microwave ablation of localized adenomyosis

CEUS and DCE-MRI are highly accurate when used to evaluate the ablation rate of localized adenomyosis following MWA, and immediate ultrasound angiography after MWA shows residual lesions in the ablation zone. The lesion did not ablate the scope, and the ultrasound was accurately positioned to perform ablation again, effectively avoiding incomplete ablation.[16] CEUS is an invasive examination, and contrast agent allergic reactions may occur; however, the incidence of such reactions is significantly lower than for other imaging enhancement examinations.[30] For patients who have dentures, arterial stents, metal foreign bodies in the eyeball, residual metal foreign bodies, or a metal prosthesis in the body, it is easy for the NMR machine to work normally; however, DCE-MRI is not suitable for the same.

Clinical effects and complications

The hyperechoic range of the heat field was closely monitored during PMWA of uterine adenomyosis, and no pathomorphological damage was found in the bladder, intestine, and other organs around the uterus after the operation. We both ensured patient safety and alleviated patient symptoms, including dysmenorrhea and anemia.

Dysmenorrhea scores had decreased by one–six points in all 66 patients at a re-examination 3 months after MWA. Among these, 42 patients had a dysmenorrhea score of ≥4 after treatment, and in 24 cases, the dysmenorrhea score decreased by one–four points, suggesting that all 66 patients with adenomyosis were treated effectively with MWA.[31] Due to the limited sample size of this study, only the nonmenstrual hemoglobin concentration at 3 and 6 months after PMWA was counted. The nonmenstrual hemoglobin at both of these time-points significantly improved after treatment (P < 0.05), indicating that the symptoms of anemia were significantly less and that the treatment was effective. Of the 66 adenomyosis patients treated with PMWA, 17 patients reported a vaginal fluid phenomenon, of mostly pale pink, brown or washed water-like liquid, which was considered to be caused by liquefaction necrosis after lesion ablation. One patient self-reported bloody secretions, which was considered to be the response of the endometrium after ablation stimulation following MWA.[32] No special treatment was required for these 17 patients, and the vaginal fluid or bloodshed disappeared after 2–11 days. Most patients had pain at the puncture site and ablation area. This is a common adverse reaction of PMWA, and was not related to the use of the SonoVue contrast agent. Therefore, CEUS was useful in evaluating the efficacy and safety of PMWA in the treatment of adenomyosis.


 > Conclusions Top


The effect of MWA on the evaluation of localized adenomyosis can be observed dynamically and in real time by intravenous CEUS. The ablation can be supplemented immediately in patients with incomplete ablation by CEUS, which can be used as the preferred examination method to evaluate the effect and ablation rate of localized adenomyosis by MWA.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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