Abstract
Purpose
To investigate the feasibility of percutaneous intrauterine instillation of chilled saline to protect the endometrium during microwave ablation (MWA) treating types 1–3 uterine fibroids.
Materials and methods
Twenty-six patients with types 1–3 uterine fibroids were prospectively enrolled in an intrauterine saline instillation group (study group). The same number of patients with types 1–3 uterine fibroids who previously received MWA without endometrial protection were retrospectively included in a control group. Endometrial impairment was evaluated by hysteroscopy and magnetic resonance imaging (MRI).
Results
In the study group, hysteroscopy revealed an intact endometrium in 17 patients, congestion and reddening of the endometrium due to heat in 8 patients, and a burnt necrosis with a size < 1 cm on the functional layer of the endometrium in 1 patient. On MRI, in the study group, there were 17 (65.4%), 6 (23.1%), and 3 (11.5%) patients with grades 0, 1, and 2 endometrial impairment, respectively, but no grade 3 endometrial impairment. In the control group, there were 8 (30.8%), 8 (30.8%), 7 (26.9%), and 3 (11.5%) patients with grades 0, 1, 2, and 3 endometrial impairment, respectively. Endometrial impairment in the study group was significantly better than that in the control group (p = 0.006). One patient had puncture tunnel bleeding and no other complications occurred in the study group.
Conclusion
Intraoperative percutaneous intrauterine instillation of chilled saline may be effective and safe in reducing the thermal damage to the endometrium caused by MWA for treating types 1–3 uterine fibroids.
Introduction
Uterine fibroids, also known as leiomyomas, are the most common benign tumors of the uterus. Uterine fibroids are composed of smooth muscle cells, fibroblasts, and a large amount of fibrous extracellular matrix [Citation1]. Uterine fibroids can cause abdominal distension, abdominal pain, constipation, frequent urination, and increased menstrual flow and may lead to infertility in severe cases, significantly affecting the health of women of childbearing age [Citation2]. The choice of fibroid treatment depends not only on the number, size, and location of the fibroids but also on the patient’s age and desire to maintain fertility or avoid hysterectomy. Treatment options for uterine fibroids include drug therapy, hysteroscopic myomectomy, laparotomic or laparoscopic myomectomy, uterine artery embolization, and thermal ablation (e.g., microwave ablation (MWA), high-intensity focused ultrasound (HIFU) ablation, and radiofrequency ablation) [Citation3]. As a thermal ablation technique, MWA has been reported to be safe and effective in the treatment of uterine fibroids [Citation4].
Whether MWA treating uterine fibroids, especially those adjacent to the endometrium, will cause endometrial impairment or even affect fertility is the most concerning issue for patients who want to preserve fertility and a popular topic for clinicians to discuss and study. Several studies [Citation5–9] have shown thermal ablation to be safe and effective in the treatment of submucosal fibroids. The results of some previous studies [Citation10–13] have indicated that pregnancy after the thermal ablation of uterine fibroids is safe, with pregnancy rates and pregnancy outcomes similar to those after the surgical resection of uterine fibroids. However, this does not mean that the endometrium is not impaired during thermal ablation. Indeed, it does exist in clinical practice. Kim et al. [Citation14] reported that 43.6% of submucosal fibroids showed endometrial impairment after HIFU thermal ablation treating 117 submucosal fibroids. Damage to the basal layer of the endometrium can result in amenorrhea and even affect the reproductive function of patients. Therefore, minimizing the thermal damage of ablation to the endometrium has a great significance for reducing the impact of endometrial impairment on preserving fertility and subsequent pregnancies.
In clinical work, to avoid thermal damage to the endometrium during MWA treating fibroids adjacent to the endometrium, a common protective measure is to preoperatively place an angiographic catheter or urinary catheter in the uterine cavities and intraoperatively perfuse the uterine cavities with a cold sterile coupling agent or chilled normal saline by the catheter to lower the temperature. However, these methods have certain limitations, and may not be suitable for patients with compressed and deformed uterine cavities or no sexual experience. Therefore, finding a more effective method to protect the endometrium will be very helpful for MWA treating patients with fibroids proximal to the endometrium. However, to our knowledge, there are currently no relevant reports in this regard.
Herein, we propose a method, percutaneous intrauterine instillation of chilled saline, to reduce thermal endometrial impairment during using MWA treating fibroids adjacent to the endometrium. This method can lower the temperature of the uterine cavity by taking the heat away through continuous water flow. We conducted a comparative study of postoperative endometrial impairment to investigate the feasibility of this technique.
Materials and methods
Patients
From January 2022 to December 2022, patients with uterine fibroids adjacent to the endometrium were prospectively enrolled in an intrauterine chilled saline instillation group (study group) through a nonrandomized study design. To compare the efficacy and safety of MWA under the intrauterine instillation of chilled saline and conventional MWA without endometrial protection in the treatment of uterine fibroids, patients who previously received MWA treatment of uterine fibroids adjacent to the endometrium without endometrial protection were retrospectively included in a control group.
The inclusion criteria of patients in the two groups were as follows: (1) 18 years of age or older; (2) types 1, 2 and 3 uterine fibroids according to the International Federation of Gynecology and Obstetrics (FIGO) classification method [Citation15]; (3) pathological diagnosis of uterine fibroids by ultrasound-guided needle biopsy before ablation; and (4) no pregnancy, breastfeeding, pelvic infection, coagulation dysfunction, heart disease or malignant tumor. The study protocol was approved by the Ethics Review Committee of the Second Affiliated Hospital of Shantou University Medical College (No. 202311), and informed consent was obtained from each patient.
Percutaneous intrauterine instillation of saline
Patients in the study group were treated with percutaneous intrauterine instillation of chilled saline to protect the endometrium. All patients took laxatives one day before surgery to empty the intestinal contents and emptied the bladder before puncture. Applying pressure to the abdominal wall during puncture can push the intestinal tracts and omentum aside. This helps to puncture the uterus, even the retroverted uterus. Additionally, the retroverted uterus can be punctured in the direction from the cervix to the fundus. Before the ablation started, an 18 gauge puncture needle was percutaneously penetrated into the uterine cavity under the guidance of ultrasound, and the outer end of the needle was supplied with chilled saline for instillation under continuous pressure to protect the endometrium throughout the operation (). The instilled normal saline was discharged from the uterine cavity through the vagina. A funnel-shaped drainage bag was placed at the perineum to avoid spillage and drain the water into a bucket. The puncture needle was removed immediately after the operation.
Figure 1. The schematic diagram of percutaneous intrauterine instillation of chilled saline under the ultrasonic guidance for microwave ablation treating uterine fibroid adjacent to the endometrium. The submucous fibroid (red arrow); the 18 gauge puncture needle (blue arrows); the uterine cavity filled with chilled saline (green arrow).
MWA ablation
Ultrasound-guided percutaneous MWA of uterine fibroids was performed using a microwave ablation system (ECO-100A1; ECO, Nanjing, China) at a frequency of 2450 MHz. The ablation needle was 14 gauge in diameter and 18 cm in length with an internal water circulation cooling system and a 1.5-mm microwave emission point 11 mm from the needle tip. In general, one ablation needle was used for fibroids smaller than 5 cm in diameter, and two ablation needles were used for fibroids larger than 5 cm in diameter. The ablation needle was percutaneously punctured into the uterine fibroids under ultrasound guidance, and the output power was set to 40 W or 50 W for 300 s. After ablation, contrast-enhanced ultrasonography was performed immediately to identify residual active fibroids. If residual contrast-enhanced fibroid tissue was observed, supplementary ablation was performed immediately. Ablation was terminated when no enhancement was observed in the entire fibroid.
Assessment of endometrial impairment
Patients in the study group underwent hysteroscopy within 3 days after the operation to investigate the thermal damage to the endometrium. The examination was conducted by two authors (MHC and PSC). The endometrial thermal damage was evaluated as normal (no signs of burnt damage to the endometrium), mild (congestion and reddening of the endometrium), moderate (burnt injury to the functional layer of the endometrium), or severe (burnt injury to the basal layer of the endometrium). In addition, patients in both the study and control groups underwent contrast-enhanced magnetic resonance imaging (MRI) at 1 month postoperatively to assess endometrial integrity. The assessment was carried out by two authors (SHH and WBZ). On contrast-enhanced T1 images, a lack of endometrial enhancement was considered endometrial impairment. Referencing previous research [Citation14], endometrial impairment was assessed as grade 0 (continuous endometrium), grade 1 (pin-point, full-thickness discontinuity of the involved endometrium), grade 2 (between grades 1 and 3), or grade 3 (full-thickness discontinuity of the involved endometrium >1 cm). The evaluators were blinded to the group allocation when evaluating the integrity of and thermal damage to the endometrium.
Adverse events
The adverse events related to percutaneous uterine puncture included hemorrhage in the puncture tunnel, needle track infection, and intestinal tract or bladder injury. After removing the puncture needle, bleeding at the puncture point observed under color Doppler ultrasound was classified as hemorrhage in the puncture tunnel. Needle track infection was defined as the infection occurs at the puncture site with 2 weeks after surgery. Intestinal tract or bladder injury refers to the injury caused by the puncture needle during puncture.
Statistical analysis
Continuous variables that conformed to a normal distribution are expressed as the mean ± standard deviation, and continuous variables that did not conform to a normal distribution are expressed as medians (quartiles). Categorical variables are expressed as frequencies (percentages). Continuous variables were compared using the T test or the Mann–Whitney U test. Categorical variables were compared using the chi-square test or Fisher’s test. Rank data of endometrium impairment for the two groups were compared using the Mann–Whitney U test. All statistical analyses were performed using SPSS 24.0 software (SPSS Inc., Chicago, IL). A P value < 0.05 was considered statistically significant.
Results
Baseline characteristics
As shown in , there were no significant differences in age, body mass index, preoperative hemoglobin level, pregnancy history, or history of cesarean section between the study and control groups. The numbers of patients with FIGO types 1, 2 and 3 fibroids in the study group were 4, 13 and 9, respectively, and the numbers of patients with FIGO types 1, 2 and 3 fibroids in the control group were 5, 10 and 11, respectively, with no significant differences between the groups. The maximum diameter and volume of fibroids were not significantly different between the study group (6.4 ± 1.8 cm and 49.2 (21.6–100.1) ml, respectively) and the control group (5.8 ± 1.9 cm and 38.0 (12.9–74.9) ml, respectively).
Table 1. The baseline characteristics of the study population.
Evaluation of endometrial damage by hysteroscopy
A schematic diagram of postoperative endometrial impairment observed during hysteroscopy is shown in . In the study group, postoperative hysteroscopy revealed an intact endometrium in 17 patients, congestion and reddening of the endometrium due to heat in 8 patients, and a size less than 1 cm burnt necrosis of the functional layer surface of the endometrium in 1 patient, while the deep portion of the functional layer and the basal layer of the endometrium was intact.
Figure 2. The schematic diagram of endometrial impairment observed during postoperative hysteroscopy. (a) Normal endometrium: a 31-year-old patient with a type 2 fibroid; the endometrium was intact and the opening of the endometrial glands (blue arrows) could be observed. (b) Mild thermal damage: a 49-year-old patient with a type 3 fibroid; mild disorder, congestion and reddening of the endometrium (blue arrows) due to heat injury were observed. (c) Moderate thermal damage: a 39-year-old patient with a type 2 fibroid; a burnt necrosis with a size < 1 cm on the functional layer surface of the endometrium (blue arrow) was observed while the deep portion of the functional layer and the basal layer of the endometrium was intact (green arrow).
Evaluation of endometrial damage by MRI
A schematic diagram of the postoperative endometrial impairment grades on MRI for patients is shown in . As shown in , there were 17 (65.4%), 6 (23.1%), and 3 (11.5%) patients in the study group with grades 0, 1, and 2 endometrial impairment, respectively. No patients in the study group developed grade 3 endometrial impairment. There were 8 (30.8%), 8 (30.8%), 7 (26.9%), and 3 (11.5%) patients in the control group with grades 0, 1, 2, and 3 endometrial impairment, respectively. The difference in endometrial impairment between the two groups was statistically significant (p = 0.006).
Figure 3. The schematic diagram of endometrial impairment grades indicated by red marks on postoperative magnetic resonance imaging. (a) Grade 0 (normal endometrium). (b) Grade 1 (pin-point, full-thickness discontinuity of involved endometrium). (c) Grade 2 (between grade 1 and 3). (d) Grade 3 (full-thickness discontinuity of involved endometrium over 1 cm in size).
Table 2. The comparison of endometrial impairment between two groups.
Complications
In the control group, there were no complications related to the percutaneous intrauterine instillation of chilled saline because this procedure was not performed. In the study group, needle track infection and intestinal tract or bladder injury caused by percutaneous uterine puncture were not observed. However, one patient had hemorrhage in the puncture track monitored by using color Doppler ultrasound after removing the puncture needle. We performed hemostasis immediately by ablating the bleeding point with 50 W for 30 s. The postoperative hemoglobin level decreased by 2 g/L, which did not affect the patient’s recovery.
Discussion
Currently, MWA is increasingly used to treat uterine fibroids, which has been proven to be effective in relieving symptoms and improving the quality of life of patients [Citation4,Citation16,Citation17]. However, patients who want to preserve fertility, especially those with fibroids close to the endometrium, are concerned about endometrial impairment and worry that impairment will affect reproductive function. The results of previous research [Citation14] indicated that the thermal ablation of uterine fibroids could cause endometrial impairment. In response to this situation, several approaches have been taken clinically to prevent endometrial impairment. One method is to indwell an angiographic catheter or urinary catheter in the uterine cavity before surgery and perfuse the uterine cavity with cold sterile coupling agent or chilled saline by catheter during the operation to lower the temperature, thus avoiding thermal damage to the endometrium. However, for some patients with compressed and deformed uterine cavities, urinary catheters or angiographic catheters are difficult to place into the uterine cavities, and this method is not suitable for patients who have no sexual experience because it is likely to damage the hymen. In addition, the water-filled balloon of the urinary catheter may block the internal cervical orifice, and thus, water in the uterine cavity cannot flow out through the vagina, which diminishes the cooling effect of water circulation. Moreover, overly high pressure in the uterine cavity may cause the water to flow back into the pelvic cavity along the fallopian tube and even cause the catheter to move into the vagina. During the operation, the ablation needle may puncture the water-filled balloon of the catheter, causing the catheter to dislodge into the vagina. Additionally, some patients have a particularly tight cervix, making it more difficult to place an indwelling catheter. The transvaginal procedure increases the risk of infection. Therefore, although this method is effective, it has many shortcomings and is not suitable for all patients. Another approach is to ablate the fibroid while preserving a small portion of the fibroid adjacent to the endometrium. However, for some fibroids with a rich blood supply, the residual fibroid tissue may grow quickly, leading to recurrence, secondary surgeries and more economic losses. Another common method to reduce heat damage is to decrease the ablation power and use the role of the uterine fibroid membrane so that the heat is confined to the uterine fibroid capsule, thereby protecting the endometrium. However, this method greatly depends on the experience and technical skills of the surgeon; it is difficult for beginners to master and can easily result in residual fibroids.
In the present study, a new method was adopted. An 18-gauge needle was percutaneously punctured into the uterine cavity, and the outer end of the needle was supplied with chilled normal saline for instillation under continuous pressure. Compared to the above methods, this method has some advantages. First, percutaneous puncture into the uterine cavity under ultrasonic guidance is more convenient than transvaginal catheterization in the uterine cavity. This operation is not difficult for experienced operators and is also suitable for patients in whom transvaginal uterine catheterization may be difficult or contraindicated. Second, the method does not involve a transvaginal procedure, reducing the risk of infection. Third, the instillation of chilled saline under continuous pressure during the operation can immediately dissipate heat through vaginal flow, providing a better protection effect. Fourth, the position of the puncture needle in the uterine cavity can be adjusted at any time during the operation to protect the endometrial tissue adjacent to the uterine fibroid. However, the disadvantage of this method is that the puncture needle can become displaced from the uterine cavity due to changes in the fibroid or movement of the uterus during the ablation process. Therefore, the operator is required to check the position of the puncture needle from time to time and make adjustments when necessary.
In this study, we performed hysteroscopy within 3 days after the operation for patients in the study group to assess thermal damage to the endometrium. Most of the patients in the study group showed no signs of thermal damage to the endometrium. Ten patients showed a disturbed endometrium with congestion and reddening, which was likely caused by heat. Such lesions were mild and were quickly repaired by the endometrium itself. In a 39-year-old patient with a FIGO type 2 fibroid, burnt necrosis with a range of < 1 cm on the functional layer surface of the endometrium was observed after ablation. However, the deep portion of the functional layer and the basal layer of the endometrium were intact. Due to the higher water content [Citation18] and vascularity [Citation19,Citation20] of the endometrium, this type of impaired endometrium can be repaired spontaneously [Citation14] without affecting reproductive function. This patient had superficial endometrial impairment and necrosis that was probably caused by the loss of the cooling effect due to failure to detect the displacement of the needle in a timely manner during the operation. Therefore, this method requires the operator to check for puncture needle displacement from time to time, especially when ablating fibroids adjacent to the endometrium.
Contrast-enhanced MRI was performed at 1 month postoperatively to compare endometrial integrity between the two groups. The results indicated that postoperative endometrial impairment was significantly milder in the patients in the study group than in those in the control group. The number of patients with grades 1 and 2 endometrial impairment was significantly lower in the study group than in the control group. Furthermore, no patients in the study group developed grade 3 endometrial impairment. However, 3 patients in the control group had grade 3 endometrial impairment. Hence, percutaneous intrauterine instillation of chilled normal saline can effectively prevent endometrial thermal damage caused by MWA of FIGO types 1–3 uterine fibroids.
To our knowledge, there is no report of endometrial impairment caused by MWA of uterine fibroids. Kim et al. [Citation14] reported that nearly half of the patients had endometrial impairment after HIFU ablation treating submucosal fibroids, and they found that only slightly impaired endometrium may automatically recover. However, severely impaired endometrium may become permanently damaged. Thus, reducing endometrial damage is important and necessary. Herein, we propose a new method to protect the endometrium during MWA and have confirmed that this method can effectively reduce thermal damage to the endometrium.
Notably, our method is an invasive operation to protect the endometrium when ablating uterine fibroids adjacent to the endometrium, which requires operators who have received a certain training. It may cause some adverse events including hemorrhage in the puncture tunnel, needle track infection, and intestinal tract or bladder injury. In the study, only one patient had complications of puncture tunnel bleeding. No other related complications were observed. Therefore, the method is safe for experienced operators.
This study has some limitations. First, most patients required a maximum protection of the endometrium. The number of patients receiving microwave ablation without protecting the endometrium was very small. Due to the limited number of cases, previous patients were included for retrospective analysis in the control group. Therefore, our study exists selection bias, and the confounding factors, including age, body mass index, FIGO classification and fibroid size, may have impact on the statistical power of the results. However, the differences in these confounding factors between the two groups were not statistically significant. Second, this is a single-center study with a small sample size. Thus, the findings of this study should be considered preliminary, and a multicenter randomized controlled trial with a large sample is needed to validate our results. Third, patients in the control group did not undergo postoperative hysteroscopy and could not be compared with the study group in terms of postoperative hysteroscopic findings. Fourth, contrast-enhanced MRI was performed 1 month after the operation, during which damage to the endometrium may have repaired to some extent, resulting in an underestimation of the damage. Finally, we did not follow up on the recovery of endometrium by MRI or the pregnancy of patients with fertility requirements.
Conclusion
In summary, intraoperative percutaneous intrauterine instillation of chilled saline is likely to effectively and safely reduce the thermal damage to the endometrium caused by MWA for treating FIGO types 1–3 uterine fibroids.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Data availability statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Additional information
Funding
References
- Harris HR, Petrick JL, Rosenberg L. The epidemiology of uterine fibroids: where do we go from here? Fertil Steril. 2022;117(4):841–842. doi: 10.1016/j.fertnstert.2022.01.037.
- Stewart EA, Laughlin-Tommaso SK, Catherino WH, et al. Uterine fibroids. Nat Rev Dis Primers. 2016;2:16043. doi: 10.1038/nrdp.2016.43.
- Donnez J, Dolmans MM. Uterine fibroid management: from the present to the future. Hum Reprod Update. 2016;22(6):665–686. doi: 10.1093/humupd/dmw023.
- Liu H, Zhang J, Han ZY, et al. Effectiveness of ultrasound-guided percutaneous microwave ablation for symptomatic uterine fibroids: a multicentre study in China. Int J Hyperthermia. 2016;32(8):876–880. doi: 10.1080/02656736.2016.1212276.
- Wang W, Wang Y, Wang T, et al. Safety and efficacy of US-guided high-intensity focused ultrasound for treatment of submucosal fibroids. Eur Radiol. 2012;22(11):2553–2558. doi: 10.1007/s00330-012-2517-z.
- Wang Y, Liu X, Wang W, et al. Long-term clinical outcomes of US-Guided High-Intensity focused ultrasound ablation for symptomatic submucosal fibroids: a retrospective comparison with Uterus-Sparing surgery. Acad Radiol. 2021;28(8):1102–1107. doi: 10.1016/j.acra.2020.05.010.
- Xie B, Zhang C, Xiong C, et al. High intensity focused ultrasound ablation for submucosal fibroids: a comparison between type I and type II. Int J Hyperthermia. 2015;31(6):593–599. doi: 10.3109/02656736.2015.1046406.
- Hu L, Zhao JS, Xing C, et al. Comparison of focused ultrasound surgery and hysteroscopic resection for treatment of submucosal uterine fibroids (FIGO type 2). Ultrasound Med Biol. 2020;46(7):1677–1685. doi: 10.1016/j.ultrasmedbio.2020.02.018.
- Yang Y, Zhang J, Han ZY, et al. Ultrasound-guided percutaneous microwave ablation for submucosal uterine fibroids. J Minim Invasive Gynecol. 2014;21(3):436–441. doi: 10.1016/j.jmig.2013.11.012.
- Zou M, Chen L, Wu C, et al. Pregnancy outcomes in patients with uterine fibroids treated with ultrasound-guided high-intensity focused ultrasound. BJOG. 2017;124 Suppl 3(Suppl 3):30–35. doi: 10.1111/1471-0528.14742.
- Qin J, Chen JY, Zhao WP, et al. Outcome of unintended pregnancy after ultrasound-guided high-intensity focused ultrasound ablation of uterine fibroids. Int J Gynaecol Obstet. 2012;117(3):273–277. doi: 10.1016/j.ijgo.2012.01.011.
- Jiang Z, Li Q, Li W, et al. A comparative analysis of pregnancy outcomes of patients with uterine fibroids after high intensity focused ultrasound ablation and laparoscopic myomectomy: a retrospective study. Int J Hyperthermia. 2021;38(1):79–84. doi: 10.1080/02656736.2021.1874547.
- Li W, Yang Z, Gao B, et al. Comparison of ultrasound-guided high-intensity focused ultrasound ablation and hysteroscopic myomectomy for submucosal fibroids: a retrospective study. Int J Hyperthermia. 2021;38(1):1609–1616. doi: 10.1080/02656736.2021.1995053.
- Kim YS, Kim TJ, Lim HK, et al. Preservation of the endometrial enhancement after magnetic resonance imaging-guided high-intensity focused ultrasound ablation of submucosal uterine fibroids. Eur Radiol. 2017;27(9):3956–3965. doi: 10.1007/s00330-017-4765-4.
- Munro MG, Critchley HOD, Fraser IS, FIGO Menstrual Disorders Working Group The FIGO classification of causes of abnormal uterine bleeding in the reproductive years. Fertil Steril. 2011;95(7):2204–2208.e2203. doi: 10.1016/j.fertnstert.2011.03.079.
- Liu L, Wang T, Lei B. Ultrasound-guided microwave ablation in the management of symptomatic uterine myomas: a systematic review and meta-analysis. J Minim Invasive Gynecol. 2021;28(12):1982–1992. doi: 10.1016/j.jmig.2021.06.020.
- Zhang J, Feng L, Zhang B, et al. Ultrasound-guided percutaneous microwave ablation for symptomatic uterine fibroid treatment–a clinical study. Int J Hyperthermia. 2011;27(5):510–516. doi: 10.3109/02656736.2011.562872.
- Zhao W-P, Chen J-Y, Chen W-Z. Effect of biological characteristics of different types of uterine fibroids, as assessed with T2-Weighted magnetic resonance imaging, on Ultrasound-Guided High-Intensity focused ultrasound ablation. Ultrasound Med Biol. 2015;41(2):423–431. doi: 10.1016/j.ultrasmedbio.2014.09.022.
- Hoad CL, Fulford J, Raine-Fenning NJ, et al. In vivo perfusion, T1, and T2 measurements in the female pelvis during the normal menstrual cycle: a feasibility study. J Magn Reson Imaging. 2006;24(6):1350–1356. doi: 10.1002/jmri.20784.
- Kim YS, Kim BG, Rhim H, et al. Uterine fibroids: semiquantitative perfusion MR imaging parameters associated with the intraprocedural and immediate postprocedural treatment efficiencies of MR imaging-guided high-intensity focused ultrasound ablation. Radiology. 2014;273(2):462–471. doi: 10.1148/radiol.14132719.