Correlation between sonographic classification and the efficacy of microwave ablation for adenomyosis

Introduction

Adenomyosis is a common benign condition that involves the invasion and growth of the endometrial glands and stroma in the myometrium (1). Patients often experience abnormal uterine bleeding, dysmenorrhea, and infertility, but approximately 33.3% are asymptomatic (2,3). Adenomyosis is primarily diagnosed via transvaginal ultrasound (TVS), magnetic resonance imaging (MRI), or pathological biopsy. An international expert panel published a consensus on the standardized classification and reporting of adenomyosis based on TVS (4), and the characteristics of adenomyosis can be assessed using this method.

Hysterectomies are radical operative procedures and are not a first-line treatment for patients who have fertility requirements or desire preservation of the uterus; however, more conservative treatments, such as medication, may be ineffective (5,6). Recently, image-guided tumor ablation techniques have been introduced for treating multiple organ masses (7,8), and an increasing number of gynecologists and interventional doctors have adopted image-guided thermal ablation, including microwave ablation (MWA), radiofrequency ablation (RFA), and high-intensity focused ultrasound (HIFU), as an option for treating symptomatic adenomyosis (9,10). The interest in microwaves is growing due to their high thermal efficiency (11,12). Our previous study confirmed that percutaneous MWA (PMWA) relieves symptoms, corrects anemia, reduces uterus size, and significantly improves quality of life (13,14). In addition, another study reported that PMWA does not affect ovarian function (15). Therefore, PMWA is a promising treatment for adenomyosis. However, no studies on whether there are differences in the efficacy of PMWA in patients with adenomyosis of different severities have been conducted. Due to the complex mechanism and presentation of adenomyosis, many clinical types of adenomyosis have been reported in previous studies (4,16,17), and there is no gold standard for the clinical classification of adenomyosis. In our practice, sonographic classification proposed by Lazzeri et al. (16) is used due to its ease of operation and high repeatability, providing clinical application value. In this study, we aimed to clarify the application value of sonographic classification in evaluating the efficacy of PMWA in the treatment of adenomyosis. It is hoped our findings can aid clinicians in understanding the postablation efficacy achievable in different types of patients before operation is performed and thus guide personalized treatment. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-933/rc).

Methods

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the ethics board of Longyan First Affiliated Hospital of Fujian Medical University (approval No. LYREC2023-k045-01). The requirement for individual consent was waived due to the retrospective nature of the analysis.

Study participants

This cross-sectional study included patients with adenomyosis who were treated with PMWA in Longyan First Affiliated Hospital of Fujian Medical University between May 2019 and October 2022. The inclusion criteria were as follows: (I) adenomyosis-related symptoms such as abnormal uterine bleeding and dysmenorrhea as confirmed by TVS and MRI; (II) no fertility requirement, request to preserve the uterus, or refusal of other treatments; (III) no signs of perimenopause; and (IV) a follow-up period of 12 months. Meanwhile, the exclusion criteria were as follows: (I) use of hormonal drugs and/or levonorgestrel releasing-intrauterine system (LNG-IUS) for 6 months preoperatively and/or 1 year postoperatively; (II) number of combined uterine fibroids >3 cm; (III) MRI or ultrasound indicating deep endometriosis; (IV) hysterectomy within 1 year postoperatively; (V) history of other interventional treatments, including HIFU or uterine artery embolization; and (VI) incomplete clinical data.

Sonographic diagnosis and grouping

All patients completed the ultrasound examination 1 day prior to the operation. The examination was completed by two ultrasound doctors with more than 10 years’ experience in gynecological ultrasound diagnosis using an E8 color Doppler ultrasound diagnostic instrument (GE HealthCare, Chicago, IL, USA) equipped with a 5- to 9-MHz transvaginal three-dimensional volume probe. First, the uterine ultrasound features were assessed with conventional two-dimensional ultrasound. Subsequently, the adnexa (the surrounding tissues and organs, including the bladder, ureter, rectum, colon, rectovaginal septum, uterovesical pouch, and uterosacral ligament) were scanned for features of deep endometriosis. If the two doctors disagreed, a third, more senior doctor with more than 15 years’ experience in gynecological ultrasound diagnosis was consulted to assess the features of the image. Volume contrast imaging was then applied to assess the morphological characteristics of the junctional zone (JZ), and the thickness was measured.

Adenomyosis was diagnosed when at least one direct feature was observed on ultrasound (18-20). Direct features included myometrial cysts, hyperechogenic islands, and echogenic subendometrial lines and buds. Globular uterus, asymmetrical myometrial thickening, fan-shaped shadowing, translesional vascularity, irregular JZ, and interrupted JZ were included as indirect features.

Ultrasonic images were obtained for all patients, and the patients were divided into five types according to the sonographic classification proposed by Lazzeri et al. (16) and then graded according to the scope and number of lesions involved. If the same patient had combined features with multiple types, each type was scored separately, and the score was added (Table 1). Groups were divided according to the total scores as follows: mild, 1–3 points; moderate, 4–6 points; and severe, ≥7 points (Figure 1).

Figure 1 Ultrasound images of three groups of patients with adenomyosis. (A1-A3) Mild focal adenomyosis. (B1-B3) Moderate diffuse adenomyosis. (C1-C3) Severe diffuse adenomyosis. (A1) A focal lesion (white arrow) visible in the outer myometrium of the anterior wall of the uterine fundus. (A2) Lesion diameter of approximately 15.1 mm (score =2). (A3) Interruption visible in the upper part of the anterior wall JZ (white arrow), with a cyst area <10 mm in the fundus JZ (red arrow) (score =1, total score =3). (B1) Diffuse lesions visible in the anterior and posterior outer myometrium, with a thickness of 29.3 mm in the anterior wall and 27.6 mm in the posterior wall (score = 3). (B2) Hyperechoic islands in the myometrium (white arrows). (B3) JZ infiltration length of 27.7 mm in the anterior wall (score =2, total score =5). (C1) Spherically enlarged uterus with diffuse involvement of the anterior, posterior, and fundal myometrium, 42.1 mm at the thicker part (score =4). (C2) Myometrial cyst (white arrow). (C3) JZ infiltration length (dashed line) 50–80% of total JZ length (score =3, total score =7). JZ, junctional zone.

Information collection

Clinical questionnaire data were obtained for all patients preoperatively and 3, 6, and 12 months postoperatively and included their pictorial blood loss analysis chart (PBAC), visual analog scale (VAS), and uterine fibroid symptom and health-related quality of life (UFS-QOL) score. (I) PBAC scores above 100 indicated heavy menstrual bleeding (21). (II) VAS scores of 0 and 10 corresponded to “no pain” and “maximum pain”, respectively (22). VAS scores ≥5 indicated severe dysmenorrhea (23). (III) UFS-QOL scores were based on the symptom severity scale (SSS) (items 1–8) and health-related quality of life scale (HRQL) items (items 9–37) (24).

The superoinferior, mediolateral, and anteroposterior diameters of the uterine corpus were measured preoperatively and 3, 6, and 12 months postoperatively. The uterine corpus volume (UCV) was calculated using the following formula:

UCV=4/3πr3[1]

where r = D/2, and D = (superoinferior diameter + mediolateral diameter + anteroposterior diameter)/3.

The UCV reduction rate (UCR) was then calculated 3, 6, and 12 months postoperatively using the following formula:

UCR=preoperative volume−current currentpreoperative volume×100%[2]

PMWA operation

PMWA procedures were all performed by the same doctor with 10 years of interventional experience. Contrast-enhanced ultrasound (CEUS) (SonoVue, Bracco, Milan, Italy) was performed before ablation to determine the extent of the lesion, blood supply distribution, and its relationship to the surrounding tissue structures. Before ablation, puncture biopsy was performed via insertion of an 18-G needle into the adenomyosis lesion under the guidance of ultrasound, and 1–2 specimens were extracted and placed into a specimen bottle for pathology examination. The puncture path was selected under real-time ultrasound guidance, and artificial ascites were created. The ablation needle (cat. No. KY2450B) was inserted into the lesion using an ablation instrument (cat. No. KY-2000A; Nanjing Kangyou Microwave Energy Research Institute, Nanjing, China), and the mobile layered ablation technique was used with a microwave output energy of 50–60 W. Ablation was stopped when the hyperechoic signal covered the entire lesion or reached 0.3–0.5 cm from the serosal layer or endometrial margin on real-time ultrasound. CEUS was performed immediately after ablation was completed, and additional ablation was performed for incompletely ablated areas. Intraoperative and postoperative adverse reactions and complications were recorded.

PMWA postoperative efficacy evaluation criteria

Efficacy was evaluated according to the improvement of dysmenorrhea and/or menstrual volume 12 months postoperatively. The evaluation scheme was as follows (25): (I) complete remission, complete disappearance of dysmenorrhea and/or PBAC score <100 points; (II) significant remission, dysmenorrhea score decreased by ≥4 points and/or PBAC score decreased by ≥50%; (III) mild remission, dysmenorrhea score decreased by <4 points or PBAC score decreased by <50% and score ≥100 points; (IV) no remission, no increase in dysmenorrhea score or PBAC score; and (V) exacerbation, dysmenorrhea and/or PBAC scores higher than those before treatment.

According to the patients’ subjective responses, complete and significant remission were defined as satisfactory efficacy, while mild remission, no remission, and exacerbation were defined as unsatisfactory efficacy.

Evaluation of adverse reactions and complications

Adverse reactions during intraoperative and postoperative follow-up were evaluated according to the Society of Interventional Radiology (SIR) classification (26) as follows: SIR A, no treatment required or adverse consequences; SIR B, simple treatment, observation, and no adverse consequences; SIR C, necessary hospitalization for a short period of time (<48 hours); SIR D, major treatment, increased grade of care, and longer hospital stay (>48 hours); SIR E, permanent adverse sequelae; and SIR F, death.

Statistical analysis

Statistical analyses were performed using SPSS version 26 (IBM Corp., Armonk, NY, USA). Normally distributed data are expressed as the mean ± standard deviation, and one-way analysis of variance tests were performed for comparisons among multiple groups. Nonnormally distributed data are expressed as the median and interquartile range, and the Kruskal-Wallis test was used to compare groups. Bonferroni post hoc adjustment was used for multiple comparisons. The Friedman test was used for intragroup comparisons. All statistical analyses were two-sided for one-way analysis and nonparametric tests, with a P value <0.05 being considered to indicate statistical significance. Categorical variables are expressed as frequencies and percentages, and comparisons between groups were made using the Chi-square test or Fisher exact test, All statistical analyses for the Chi-square or Fisher exact test were two-sided, with a Bonferroni adjusted P value <0.017 being considered to indicate statistical significance. Correlation analyses were performed via Spearman rank correlation analysis.

Results

Comparison of baseline clinical characteristics

Overall, 192 patients with adenomyosis received PMWA. The follow-up time of five cases was less than 12 months, which did not meet the inclusion criteria; seven cases were diagnosed with deep endometriosis; three cases demonstrated uterine fibroids larger than 3 cm; and four cases were excluded due to the use of hormonal drugs and/or LNG-IUS within 6 months. Finally, 173 patients were included; 129 patients completed the 12-month follow-up and were grouped according to their sonographic classification. This included 31 patients in the mild group, 50 patients in the moderate group, and 48 patients in the severe group (Figure 2). Three unintended pregnancies occurred after PMWA treatment, one of which stopped developing at 12 weeks, with the others being carried to term.

Figure 2 Patient flowchart. PMWA, percutaneous microwave ablation; LNG-IUS, levonorgestrel releasing-intrauterine system.

No significant differences were observed in patient age, parity, or body mass index between the three groups (P>0.05). The types of adenomyosis in the severe group were significantly different from those in the mild and moderate groups (P<0.017), and the proportion of diffuse type (complicated with adenomyoma) in the severe group was 89.6%. The severe group had the highest proportion of posterior wall lesions; however, no significant difference in the proportion of posterior wall lesions was found between the three groups (P>0.017). The severe group had the most menstrual blood loss and largest uterine volume, which significantly differed from those of the other two groups (P<0.05). Additionally, the severe group had the highest proportion of heavy menstrual bleeding, which was significantly different when compared with the mild group (P<0.017) but not with the moderate group (P>0.017). The severe group had higher SSS and lower HRQL scores, which significantly differed when compared with the mild group (P<0.05) but not with the moderate group. The moderate group had the highest VAS score, which was significantly different when compared with the mild group (P<0.05) but not with the severe group (P>0.05). Furthermore, the moderate group had the highest proportion of patients with severe dysmenorrhea, which was significantly different when compared with that of the severe group (P<0.017) (Table 2).

Efficacy evaluation

The efficacy of different degrees of PMWA treatment in adenomyosis over time

The results of Friedman testing indicated that all indices in the three groups had improved within 1 year postoperatively (P<0.05) (Table 3). A decreasing trend was observed in the PBAC, VAS, and SSS scores and the UCV, while an increasing trend was observed for the HRQL scores and UCR.

In the mild group, VAS scores decreased more significantly at 3 months postoperatively and then stabilized, while SSS and HRQL scores improved more significantly at 6 months postoperatively and then stabilized. The decrease in VAS scores was more significant in the moderate and severe groups over 6 months postoperatively and then tended to stabilize, while the SSS and HRQL scores gradually improved over 1 year postoperatively. The UCV decreased more drastically in the mild and severe groups at 6 months postoperatively and then stabilized; in the moderate group, the UCV gradually decreased for 1 year postoperatively. In all three groups, the PBAC score gradually decreased, while the UCR gradually increased. The line chart of the treatment effect in the three groups is shown in Figure 3.

Figure 3 Line chart of the treatment effect in the three groups. (A) PBAC; (B) VAS; (C) SSS; (D) HRQL; (E) UCV; (F) UCR. PBAC, pictorial blood loss analysis chart; pre, preoperative; m, months; VAS, visual analog scale; SSS, symptom severity scale; HRQL, health-related quality of life scale; UCV, uterine corpus volume; UCR, uterine corpus volume reduction rate.

Comparison of therapeutic effect of PMWA according to the severity of adenomyosis

As shown in Table 3, the PBAC and UCV in the severe group were higher than those in the mild and moderate groups (P<0.05) at 3, 6, and 12 months postoperatively. There was no significant difference in the improvement of VAS, SSS, or HRQL between the three groups at any time point postoperatively (P>0.05). There was no significant difference in the UCR at 3 months postoperatively between the three groups (P>0.05). The UCR of the moderate group at 6 and 12 months postoperatively was higher than that in the mild and severe groups (P<0.05). The proportions of satisfactory and unsatisfactory efficacy were the highest in the mild and severe groups, respectively, significantly so (P<0.017), but no significant differences were observed between the mild and moderate groups (P>0.017). Figure 4 shows the symptom remission of the three groups at 12 months postoperatively.

Figure 4 Symptom relief histogram of the three groups 12 months postoperatively.

Adverse reactions and complications

Postoperative adverse reactions included vaginal fluid, pain in the operative area, fever, nausea, and vomiting, and no serious complications such as uterine perforation or intestinal or bladder injury were observed. The incidence of SIR A, SIR B, SIR C, and SIR D classification was 69.76%, 6.98%, 1.55%, and 1.55%, respectively. There was no significant difference in the incidence of adverse reactions between the three groups (P>0.05) (Table 3). Postoperative pain developed in 66.67% (86 of 129) of the patients, which was relieved within 24 hours. Most patients had a small amount of vaginal fluid after the operation, typically light pink or coffee-colored, which usually disappeared spontaneously. Postoperatively, 10.08% (13 of 129) of patients had fever of different degrees, with most having a low-grade fever.

Analysis of the correlation between ultrasound scores and symptoms

Ultrasound scores were positively correlated with preoperative PBAC [Spearman’s rank correlation coefficient (r_s) =0.573; 95% confidence interval (CI): 0.384–0.727; P<0.001], SSS (r_s =0.299; 95% CI: 0.122–0.467; P=0.002), UCV (r_s =0.575; 95% CI: 0.421–0.715; P<0.001), and 12-month postoperative UCR (r_s =0.623; 95% CI: 0.485–0.739; P<0.001); meanwhile, ultrasound scores were negatively correlated with preoperative HRQL (r_s =−0.301; 95% CI: −0.478 to −0.111; P=0.002). There was no significant correlation between ultrasound scores and preoperative VAS (r_s =0.076; 95% CI: −0.119 to 0.262; P=0.450). The correlation results are shown in Figure 5.

Figure 5 Correlation of ultrasound scores and symptoms. UCR₁₂, uterine corpus volume reduction rate 12 months postoperatively; UCV, uterine corpus volume; HRQL, health-related quality of life scale; SSS, symptom severity scale; VAS, visual analog scale; PBAC, pictorial blood loss analysis chart; CI, confidence interval.

Discussion

The findings of this study suggest that the sonographic classification of adenomyosis can be used to assess the preoperative severity of adenomyosis in patients, which is useful for predicting the efficacy of PMWA in the treatment of adenomyosis. All measured indices improved postoperatively in all three groups. The improvement in UCR was most significant in the moderate group, and the proportions of satisfactory and unsatisfactory efficacy were the highest in the mild and severe groups, respectively. Thus, PMWA demonstrated significant efficacy in the treatment of symptomatic adenomyosis, and sonographic classification can be used for preoperative clinical evaluation.

The main thermal ablation methods for adenomyosis include MWA, RFA, and HIFU. These three ablation methods have remarkable efficacy for treating symptomatic adenomyosis (27-29) and have been gradually introduced into clinical practice. At present, most of the thermal ablation paths of the uterus are percutaneous abdominal ablation, and its guidance methods include transabdominal ultrasound, TVS, and laparoscopy. The transabdominal ultrasound-guided method can improve ablation efficacy and reduce treatment time; however, it has some disadvantages, such as intestinal interference with needle tip insertion, and is more likely to cause serious complications, including penetration of pelvic organs, heat damage, and abdominal bleeding. TVS provides a clearer view of the angle at which the needle is inserted, a better direction and depth of the path, and a more accurate measurement of the distance between the tip of the needle and the endometrial and serous layers of the uterus; however, ablation under this guided approach depends on the technical proficiency of the operator. Laparoscopic guidance can help separate pelvic adhesions, provide a wide operating path, and observe uterine surface and bowel movements (30), but the specific ablation range within the lesion cannot be observed during ablation. With the advancement of ablation equipment and techniques, intrauterine ultrasound-guided transcervical ablation has also been used to improve adenomyosis symptoms (31). The advantages of this method include a lack of abdominal incision, short ablation time, and a low risk of pelvic adhesion. It is also a promising alternative to traditional surgery, and its safety and efficacy should be further studied. No serious complications occurred this study, which may be related to the use of water isolation technology and preservation of a safe distance around the serosal layer in avoiding injuries to surrounding organs such as the bladder and rectum.

In this study, the severe group had the highest amount menstrual blood loss, largest UCV, highest SSS score, and lowest HRQL score preoperatively, which may be related to the more severe extent of myometrial involvement. Exacoustos et al. (23) discovered that patients with severe diffuse adenomyosis had pronounced menstrual bleeding, with the greatest menstrual bleeding observed in patients with combined adenomyomas, which is consistent with our results in terms of menstrual blood loss in patients with severe adenomyosis. Naftalin et al. reported that the amount of menstrual blood loss was significantly positively correlated with the number of adenomyosis-related ultrasound features (21), and the scoring criteria of the ultrasound scoring system in our study was also related to the number of adenomyosis-related ultrasound features. There were differences in the PBAC, SSS, HRQL, and UCV between the three groups preoperatively, and the increasing severity of adenomyosis was correlated with more obvious symptoms and a more pronounced increase in UCV. In addition, ultrasound scores were weakly to moderately correlated with preoperative PBAC, SSS, HRQL, and UCV, indicating that sonographic classification may be able to reflect the severity of symptoms and signs of patients with varying degrees of adenomyosis to some extent.

Previous studies have not reached a consensus regarding the correlation between the severity of adenomyosis and the severity of dysmenorrhea. Naftalin et al. (32) discussed the correlation between the number of ultrasonic features of adenomyosis and dysmenorrhea (numerical rating scale score) and found that the dysmenorrhea score was positively correlated with the sonographic severity, but the study did not consider the scope of the lesions. Exacoustos et al. (23) did not identify a correlation between severity and dysmenorrhea when they classified intrauterine lesions as mild, moderate, or severe using a sonographic scoring system. In our study, when grouping was conducted with the same scoring system as that of Exacoustos et al. (23), no correlation was found between the severity of lesions and the severity of dysmenorrhea. The preoperative VAS score was highest in the moderate group, but there was no significant difference between the moderate and severe groups. This inconsistency may be due to the fact that the pain mechanism of adenomyosis is relatively complex, which involves not only the number and scope of lesions but also the central nervous system and psychological and social factors (33).

Postoperatively, all three groups showed significant improvements in all measured indicators. The UCR of the moderate group improved more than that of the mild and severe groups, which may attributable to the following. First, in the mild group, the uterus was small in size and freely moveable in the artificially ascitic environment. During the ablation process, the uterus corpus oscillated greatly with the movement of the ablation needle, which increased the difficulty of operation, and ablation may have been incomplete. In addition, in the mild group, the lesion scope was small; therefore, even if the ablation was complete, the ablated lesion accounted for a small proportion of the total uterine volume, and the postoperative UCR only changed slightly. Second, most patients in the severe group had diffuse adenomyosis with large lesion sizes and ablation areas, resulting in slow absorption of the ablation sites postoperatively. Patients with severe diffuse adenomyosis may have increased involvement of the junctional area or serous layer; consequently, a certain ablation distance should be preserved during ablation to prevent damage to the intima and to protect the serous layer. This group had more cases of incomplete ablation and recurrence of residual lesions, as well as minimal changes in the UCR. Finally, in the moderate group, the lesion size ranged between mild and severe, and superior ablation could be achieved during the operation. Thus, recurrence of the lesion was unlikely after the operation, and symptomatic relief was more prominent. The proportion of satisfactory efficacy was higher in the mild group than in the moderate group, but this difference was not significant; thus, patients in the mild and moderate groups had better therapeutic outcomes than did those in the severe group. The PBAC and UCV in the severe group were higher than those in the mild and moderate groups 12 months preoperatively, and the proportions of patients with mild remission, no remission, and exacerbation were the highest. Therefore, those with severe conditions may need a longer follow-up to estimate the difference in long-term efficacy compared to those with a mild condition and to determine whether reablation or other treatment is required.

There are some limitations to this study. We employed a single-center design with a small sample size and short follow-up time. Moreover, the influence of PMWA on fertility and future pregnancy outcomes requires further follow-up study. Therefore, a long-term follow-up study including multiple centers and an expanded sample size is needed in the future.

Conclusions

Sonographic classification can reflect the severity of adenomyosis. The therapeutic effect of PMWA for adenomyosis varies according to severity. Sonographic classification can be used as a potential preoperative image-evaluation tool to predict the ablation effect of PMWA.

Acknowledgments

Funding: This work was supported by the Longyan City Science and Technology Plan Project (No. 2022LYF17105).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-933/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-933/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the ethics board of Longyan First Affiliated Hospital of Fujian Medical University Medical University (approval No. LYREC2023-k045-01). The requirement for individual consent was waived due to the retrospective nature of the analysis.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Struble J, Reid S, Bedaiwy MA. Adenomyosis: A Clinical Review of a Challenging Gynecologic Condition. J Minim Invasive Gynecol 2016;23:164-85. [Crossref] [PubMed]
2. Bazot M, Daraï E. Role of transvaginal sonography and magnetic resonance imaging in the diagnosis of uterine adenomyosis. Fertil Steril 2018;109:389-97. [Crossref] [PubMed]
3. Van den Bosch T, Van Schoubroeck D. Ultrasound diagnosis of endometriosis and adenomyosis: State of the art. Best Pract Res Clin Obstet Gynaecol 2018;51:16-24. [Crossref] [PubMed]
4. Van den Bosch T, de Bruijn AM, de Leeuw RA, Dueholm M, Exacoustos C, Valentin L, Bourne T, Timmerman D, Huirne JAF. Sonographic classification and reporting system for diagnosing adenomyosis. Ultrasound Obstet Gynecol 2019;53:576-82. [Crossref] [PubMed]
5. Pontis A, D'Alterio MN, Pirarba S, de Angelis C, Tinelli R, Angioni S. Adenomyosis: a systematic review of medical treatment. Gynecol Endocrinol 2016;32:696-700. [Crossref] [PubMed]
6. Lee KH, Kim JK, Lee MA, Ko YB, Yang JB, Kang BH, Yoo HJ. Relationship between uterine volume and discontinuation of treatment with levonorgestrel-releasing intrauterine devices in patients with adenomyosis. Arch Gynecol Obstet 2016;294:561-6. [Crossref] [PubMed]
7. Zhou Y, Xu ZF, Xing W, Liu Y, Xu Z, Tan GL, Wang SR, Xu D. Comparative study of ultrasound-guided microwave ablation and traditional surgery in the treatment of plasma cell mastitis: a multicenter study. Quant Imaging Med Surg 2023;13:1838-48. [Crossref] [PubMed]
8. Huang K, Hong R, Luo L, Zhao H, Wang Y, Li Y, Jiang Y, Zhou H, Li F. Efficacy and safety of different thermal ablative therapies for desmoid-type fibromatosis: a systematic review and meta-analysis. Quant Imaging Med Surg 2023;13:6683-97. [Crossref] [PubMed]
9. Chen J, Porter AE, Kho KA. Current and Future Surgical and Interventional Management Options for Adenomyosis. Semin Reprod Med 2020;38:157-67. [Crossref] [PubMed]
10. Li X, Zhu X, He S, Jiang Z, Li H, Tian X, Long W, Xue M, Deng X, Ye M. High-intensity focused ultrasound in the management of adenomyosis: long-term results from a single center. Int J Hyperthermia 2021;38:241-7. [Crossref] [PubMed]
11. Lin XL, Hai N, Zhang J, Han ZY, Yu J, Liu FY, Dong XJ, Liang P. Comparison between microwave ablation and radiofrequency ablation for treating symptomatic uterine adenomyosis. Int J Hyperthermia 2020;37:151-6. [Crossref] [PubMed]
12. Liu JX, Li JY, Zhao XY, Zhang QH, Cao Y, Huang XJ, Sun XF, Xie YL, Zhang ST, Yang SS. Transvaginal ultrasound- and laparoscopy-guided percutaneous microwave ablation for adenomyosis: preliminary results. Int J Hyperthermia 2019;36:1233-8. [Crossref] [PubMed]
13. Li Z, Li X, Lin M, Qiu S, Wang L, Lai L, Luo X, Mo Z, Dong G, Lyu G, Li S. Clinical efficacy of myometrial and endometrial microwave ablation in the treatment of patients with adenomyosis who had anemia. Int J Hyperthermia 2022;39:1335-43. [Crossref] [PubMed]
14. Li S, Li Z, Lin M, Li X, Gao L, Qiu J, He J, Zhang J, Lyu G. Efficacy of Transabdominal Ultrasound-guided Percutaneous Microwave Ablation in the Treatment of Symptomatic Adenomyosis: A Retrospective Cohort Study. J Minim Invasive Gynecol 2023;30:137-46. [Crossref] [PubMed]
15. Yang Y, Zhang J, Han ZY, Ma X, Hao YL, Xu CT, Xu RF, Zhang BS. Ultrasound-guided percutaneous microwave ablation for adenomyosis: efficacy of treatment and effect on ovarian function. Sci Rep 2015;5:10034. [Crossref] [PubMed]
16. Lazzeri L, Morosetti G, Centini G, Monti G, Zupi E, Piccione E, Exacoustos C. A sonographic classification of adenomyosis: interobserver reproducibility in the evaluation of type and degree of the myometrial involvement. Fertil Steril 2018;110:1154-1161.e3. [Crossref] [PubMed]
17. Munro MG. Classification and Reporting Systems for Adenomyosis. J Minim Invasive Gynecol 2020;27:296-308. [Crossref] [PubMed]
18. Exacoustos C, Manganaro L, Zupi E. Imaging for the evaluation of endometriosis and adenomyosis. Best Pract Res Clin Obstet Gynaecol 2014;28:655-81. [Crossref] [PubMed]
19. Van den Bosch T, Dueholm M, Leone FP, Valentin L, Rasmussen CK, Votino A, Van Schoubroeck D, Landolfo C, Installé AJ, Guerriero S, Exacoustos C, Gordts S, Benacerraf B, D'Hooghe T, De Moor B, Brölmann H, Goldstein S, Epstein E, Bourne T, Timmerman D. Terms, definitions and measurements to describe sonographic features of myometrium and uterine masses: a consensus opinion from the Morphological Uterus Sonographic Assessment (MUSA) group. Ultrasound Obstet Gynecol 2015;46:284-98. [Crossref] [PubMed]
20. Harmsen MJ, Van den Bosch T, de Leeuw RA, Dueholm M, Exacoustos C, Valentin L, Hehenkamp WJK, Groenman F, De Bruyn C, Rasmussen C, Lazzeri L, Jokubkiene L, Jurkovic D, Naftalin J, Tellum T, Bourne T, Timmerman D, Huirne JAF. Consensus on revised definitions of Morphological Uterus Sonographic Assessment (MUSA) features of adenomyosis: results of modified Delphi procedure. Ultrasound Obstet Gynecol 2022;60:118-31. [Crossref] [PubMed]
21. Naftalin J, Hoo W, Pateman K, Mavrelos D, Foo X, Jurkovic D. Is adenomyosis associated with menorrhagia? Hum Reprod 2014;29:473-9. [Crossref] [PubMed]
22. Karcioglu O, Topacoglu H, Dikme O, Dikme O. A systematic review of the pain scales in adults: Which to use? Am J Emerg Med 2018;36:707-14. [Crossref] [PubMed]
23. Exacoustos C, Morosetti G, Conway F, Camilli S, Martire FG, Lazzeri L, Piccione E, Zupi E. New Sonographic Classification of Adenomyosis: Do Type and Degree of Adenomyosis Correlate to Severity of Symptoms? J Minim Invasive Gynecol 2020;27:1308-15. [Crossref] [PubMed]
24. Spies JB, Coyne K, Guaou Guaou N, Boyle D, Skyrnarz-Murphy K, Gonzalves SM. The UFS-QOL, a new disease-specific symptom and health-related quality of life questionnaire for leiomyomata. Obstet Gynecol 2002;99:290-300. [Crossref] [PubMed]
25. 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 Cancer Res Ther 2020;16:365-71. [Crossref] [PubMed]
26. Cardella JF, Kundu S, Miller DL, Millward SF, Sacks DSociety of Interventional Radiology. Society of Interventional Radiology clinical practice guidelines. J Vasc Interv Radiol 2009;20:S189-91. [Crossref] [PubMed]
27. Zhao Y, Luo S, Liu Y, He Y, Liu X, Guohua H, He J. High intensity focused ultrasound treatment for adenomyosis: comparison of efficacy based on MRI features. Int J Hyperthermia 2023;40:2197574. [Crossref] [PubMed]
28. Stepniewska AK, Baggio S, Clarizia R, Bruni F, Roviglione G, Ceccarello M, Manzone M, Guerriero M, Ceccaroni M. Heat can treat: long-term follow-up results after uterine-sparing treatment of adenomyosis with radiofrequency thermal ablation in 60 hysterectomy candidate patients. Surg Endosc 2022;36:5803-11. [Crossref] [PubMed]
29. Liu L, Wang T, Lei B. Image-guided thermal ablation in the management of symptomatic adenomyosis: a systematic review and meta-analysis. Int J Hyperthermia 2021;38:948-62. [Crossref] [PubMed]
30. Shunshi Y, Li J, Li J, Huang L, Chen Y, Zhao X, Dong H, Huang X, Yu F, Li X, Zhang Q. Transvaginal ultrasound- and laparoscopy-guided percutaneous microwave ablation for adenomyosis has short- and long-term benefits: a single-center study. Int J Hyperthermia 2023;40:2233713. [Crossref] [PubMed]
31. Piriyev E, Schiermeier S, Römer T. Transcervical radiofrequency ablation of focal adenomyosis: pilot results. Int J Hyperthermia 2023;40:2217366. [Crossref] [PubMed]
32. Naftalin J, Hoo W, Nunes N, Holland T, Mavrelos D, Jurkovic D. Association between ultrasound features of adenomyosis and severity of menstrual pain. Ultrasound Obstet Gynecol 2016;47:779-83. [Crossref] [PubMed]
33. Vader K, Bostick GP, Carlesso LC, Hunter J, Mesaroli G, Perreault K, Tousignant-Laflamme Y, Tupper S, Walton DM, Wideman TH, Miller J. The Revised IASP Definition of Pain and Accompanying Notes: Considerations for the Physiotherapy Profession. Physiother Can 2021;73:103-6. [Crossref] [PubMed]