ORIGINAL ARTICLE Year : 2023  |  Volume : 12  |  Issue : 1  |  Page : 32-37

Laparoscopic surgery for atypical endometrial hyperplasia with awareness regarding the possibility of endometrial cancer

Misato Kamii1, Yoko Nagayoshi2, Kazu Ueda2, Motoaki Saito1, Hirokuni Takano1, Aikou Okamoto1
1 Department of Obstetrics and Gynecology, The Jikei University School of Medicine, Minato-Ku, Tokyo, Japan
2 Department of Obstetrics and Gynecology, The Jikei University School of Medicine; Department of Obstetrics and Gynecology, International University of Health And Welfare, Mita Hospital, Minato-Ku, Tokyo, Japan

Date of Submission01-Mar-2022Date of Decision01-Jun-2022Date of Acceptance10-Aug-2022Date of Web Publication26-Dec-2022

Correspondence Address:
Dr. Misato Kamii
Department of Obstetrics and Gynecology, The Jikei University School of Medicine, 3-25-8 Nishi-Shinbashi, Minato-Ku, Tokyo 105-8461
Japan

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/gmit.gmit_44_22

Objectives: Although atypical endometrial hyperplasia (AEH) is considered a precancerous disease, the frequency with which AEH and endometrial cancer (EC) coexist is not low. Broadly, total laparoscopic hysterectomy (TLH) is performed for treating AEH; however, it is unclear what perioperative precautions need to be taken. This study aimed to clarify the points to be considered when performing TLH for AEH.
Materials and Methods: We retrospectively identified 57 patients who underwent TLH for AEH in our hospitals. We extracted data on clinical characteristics, preoperative examinations (endometrial sampling and diagnostic imaging), surgical procedures, and final pathological diagnoses. Then, we statistically analyzed the difference in clinicopathological features and preoperative examinations between patients postoperatively diagnosed with EC and those diagnosed with AEH.
Results: Twenty patients (35%) who underwent TLH for AEH were diagnosed with EC postoperatively (16 [28%] with stage IA EC and four [7.0%] with stage IB EC). We found no significant differences in clinical characteristics and preoperative evaluations between patients postoperatively diagnosed with EC and those diagnosed with AEH. The group with stage IB EC had a significantly higher median age and a significantly higher proportion of postmenopausal patients and patients with adenomyosis.
Conclusion: It is important to recognize the risk of coexisting EC when performing TLH for AEH. High-precision endometrial sampling and contrast-enhanced magnetic resonance imaging are recommended for diagnosing AEH. In addition, surgical procedures for AEH are required to prevent cancer spillage in consideration of its coexistence, such as tubal sealing before manipulator insertion or avoiding using manipulator.

Keywords: Atypical endometrial hyperplasia, hysterectomy, laparoscopic surgery

How to cite this article:
Kamii M, Nagayoshi Y, Ueda K, Saito M, Takano H, Okamoto A. Laparoscopic surgery for atypical endometrial hyperplasia with awareness regarding the possibility of endometrial cancer. Gynecol Minim Invasive Ther 2023;12:32-7
How to cite this URL:
Kamii M, Nagayoshi Y, Ueda K, Saito M, Takano H, Okamoto A. Laparoscopic surgery for atypical endometrial hyperplasia with awareness regarding the possibility of endometrial cancer. Gynecol Minim Invasive Ther [serial online] 2023 [cited 2023 Feb 10];12:32-7. Available from: https://www.e-gmit.com/text.asp?2023/12/1/32/365315   Introduction 

Atypical endometrial hyperplasia (AEH) is considered a precancerous disease. However, 27%–52% of patients with preoperative AEH were reportedly diagnosed with endometrial cancer (EC) after hysterectomy.[1],[2],[3],[4],[5],[6],[7],[8] Total laparoscopic hysterectomy (TLH) is being widely used to treat AEH, but no consensus exists on the preoperative evaluation, surgical procedure, and laparoscopic techniques for AEH.

We retrospectively analyzed the clinical characteristics, preoperative evaluations, surgical procedures, and final pathological diagnoses of patients who underwent TLH for AEH. We evaluated EC incidence in patients with preoperative AEH diagnosis and discussed how to detect EC before surgery and treat AEH during laparoscopic surgery.

  Patients and Methods 

A total of 57 patients who underwent TLH for AEH in our hospitals between 2013 and 2020 were enrolled. All clinicopathological data, including age, body mass index, parity, menopausal status, endometrial thickness, serum CA125, endometrial sampling method, preoperative imaging (magnetic resonance imaging [MRI] or computed tomography [CT]), surgical procedures, pathological diagnoses, and other pathological features (adenomyosis, endometriosis, and myoma), were retrospectively extracted from clinical records. The thickness of the endometrium was evaluated using MRI or transvaginal ultrasonography. Endometrial sampling was performed by dilation and curettage (D&C) under general anesthesia or suction biopsy with pipette without anesthesia in an outpatient setting. Hysteroscopic endometrial sampling was not performed. Basically, bilateral salpingo-oophorectomy (BSO) was recommended at the time of TLH for AEH in our hospitals because the coexistence of EC with AEH is relatively frequent and no consensus exists on ovarian conservation at hysterectomy for AEH. However, bilateral salpingectomy (BS) was permitted for those who were premenopausal or had osteoporosis and cardiovascular disease in consideration of mortality benefits. Pelvic lymph node biopsy (PLNB) was performed at the time of TLH for AEH in some hospitals to avoid additional surgery to search for pelvic lymph node metastases when the final diagnosis was EC. This study was approved by the institutional review boards of all hospitals involved. All statistical analyses were performed with EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan),[9] which is for R. More precisely, it is a modified version of R commander designed to add statistical functions frequently used in biostatistics. Fisher's exact test and Mann–Whitney U-test were used to evaluate the association between the final pathological diagnosis and clinical characteristics. Statistical analyses were two-sided, and a P < 0.05 was considered statistically significant.

  Results 

The clinical characteristics, preoperative evaluation method (endometrial sampling and diagnostic imaging), and surgical procedures are shown in [Table 1]. Fifty patients (88%) underwent D&C and 55 (96%) underwent MRI before surgery; however, 20 patients (35%) were finally diagnosed with EC after hysterectomy. There was no statistically significant difference in clinical characteristics and preoperative evaluation methods between the AEH and EC (final diagnosis) groups. However, the rate of postmenopausal status tended to be higher in patients with EC (50%) than in patients with AEH (27%) (P = 0.145; [Table 1]).

Table 1: Details of 57 patients with a preoperative diagnosis of atypical endometrial hyperplasia (AEH)

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Of 20 patients with EC, 16 and four were finally diagnosed with stage IA and stage IB EC, respectively (International Federation of Gynecology and Obstetrics; FIGO staging system 2008) [Table 2] and [Table 3]. For all patients, histological examination revealed grade 1 endometrioid carcinoma. In all patients with stage IA EC, serum CA125 was not elevated; endometrial thickness was <11 mm in nine patients and ≥11 mm in seven patients (44%). Of the four patients diagnosed with stage IB EC after surgery, two underwent contrast-enhanced MRI. Although none were found to have myometrial invasion by contrast-enhanced MRI, both of these patients had adenomyosis: one ([Table 3], No. 1) had a cervical myoma and the other ([Table 3], No. 2) had a double uterus. One patient ([Table 3], No. 3) underwent additional pelvic lymphadenectomy for restaging and did not receive adjuvant chemotherapy. Two patients ([Table 3], No. 2 and 4) did not undergo restaging surgery but received adjuvant chemotherapy (paclitaxel/carboplatin). No recurrence was observed in any patient with EC (median follow-up: 33 months [range: 2.1–82]).

Table 3: Details of four patients diagnosed as stage IB EC after surgery

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Uterine manipulators were used in all patients. Tubal sealing was performed before inserting the manipulator in 38 patients, including 12 patients with EC (nine with stage IA EC and three with stage IB EC), but not in seven patients with stage IA EC and one patient with stage IB EC. In contrast, the uterus was retrieved intraperitoneally using a cellophane bag in 17 patients, including four patients with EC (three patients with stage IA EC and one with stage IB EC).

  Discussion 

In this retrospective review of 57 patients who were diagnosed with AEH preoperatively and underwent TLH at our hospitals, 35% (20/57) were diagnosed with EC postoperatively. This frequency was comparable to that reported in previous studies (27%–52%).[1],[2],[3],[4],[5],[6],[7],[8] Failure to completely distinguish EC from AEH before hysterectomy may be attributed to endometrial sampling not being highly accurate. A retrospective study of 881 patients with EC showed that the diagnostic accuracy of endometrial sampling was 87%, especially 80% for grade 1 endometrioid carcinoma, with 15% of grade 1 endometrioid carcinoma being underdiagnosed as AEH.[10] Although endometrial curettage was recommended for the detection of EC, the rate of unrecognized cancer in AEH diagnosed by curettage was 27%–32.7%.[11],[12],[13],[14] Mostly consistent with these previous reports, 34% (17/50) patients diagnosed with AEH by curettage had unrecognized cancer in this study. Suction biopsy with pipette is also recommended for EC and AEH diagnosis,[15],[16],[17] but this method is less accurate for an endometrial thickness of <5 mm[18] or when the disease is confined to polyps or small areas of the endometrium.[19] In this study, the accuracy of aspirating pipettes in diagnosing AEH was 57% (4/7), which was not significantly lower than that of D&C (66%, 33/50) [P = 0.687; [Table 1]]. In recent years, some studies have suggested that hysteroscopic endometrial resection may be useful to reduce the risk of undiagnosed EC.[11],[20],[21] Although hysteroscopic endometrial resection for EC is associated with the risk of intraperitoneal spread of malignant cells,[22],[23],[24],[25] it does not affect the prognosis in early EC.[23],[26] Further studies are required to confirm the usefulness and safety of diagnostic hysteroscopy for AEH.

There is a possibility that AEH diagnosed by endometrial sampling coexists with EC, suggesting that surgical methods for EC should be considered when performing hysterectomy for AEH. On the other hand, the surgical procedures recommended for ECs depend on each stage. Based on the evidence from randomized trials and a systematic review of the Cochrane database, the National Comprehensive Cancer Network guidelines recommend minimally invasive surgery for early EC confined to the uterus.[27],[28] In contrast, the Japanese guidelines approve it only for low-risk EC (stage IA with endometrioid carcinoma Grade 1 or 2) and recommend laparotomy (comprising hysterectomy, BSO, and lymphadenectomy) for EC with stage IB or greater.[29] Moreover, even when performing laparoscopic surgery for stage IA EC and for benign disease, several differences exist in surgical techniques. First, ovarian metastasis was reported to be 5% of stage I EC[30] and BSO should be discussed. Reportedly, the coexistence of EC with AEH was more frequent in patients aged >50 years,[14] which is not surprising as EC is more common in older woman,[13],[31] indicating that BSO may be considered for patients with AEH who are postmenopausal or >50 years. Second, sentinel lymph node mapping or lymph node biopsy may be considered because of the risk of lymph node metastasis. Reportedly, 2%–6% of patients with EC who were preoperatively diagnosed with AEH had the risk of lymph node metastasis and required additional lymphadenectomy.[2],[32] In addition, a recent study demonstrated the usefulness of sentinel lymph node mapping for AEH with possible EC.[33] Third, intraperitoneal cancer spillage during surgery should be avoided. The following methods have been suggested to prevent tumor dissemination: clipping or cauterization of the  Fallopian tube More Detailss before manipulator insertion,[34] avoiding using manipulator,[35] retrieving the uterus intraperitoneally using a cellophane bag,[36] and pelvic lavage at the end of the surgery.[37]

A prospective cohort study reported that 10.6% (13/123) of patients with EC who were diagnosed with AEH before hysterectomy had more than 50% of myometrial invasion.[8] In the present study, 20% (4/20) of patients with EC diagnosed with AEH had stage IB EC. These incidences are not low, and it is important to differentiate stage IB EC from AEH preoperatively to select the appropriate surgical method. Therefore, we additionally investigated the association between clinicopathological findings and final diagnoses (stage IB EC and AEH/stage IA EC) [Table 4]. Although there were no statistically significant differences in the clinical characteristics of patients between the EC and AEH groups [Table 1], the median age, menopausal status, and the presence of adenomyosis differed significantly between the stage IB EC and other groups. The stage IB EC group had a significantly higher median age (P = 0.022; [Table 4]) as well as a significantly higher proportion of postmenopausal patients (P = 0.012; [Table 4]) and patients with adenomyosis (P = 0.012; [Table 4]). Multivariate analysis was not performed in this study owing to the small number of patients with stage IB EC, but it implied that postmenopausal patients with AEH and adenomyosis might upstage to stage IB EC. A previous study reported that the risk of EC was higher in postmenopausal patients with adenomyosis[38] and that the evaluation of myometrial invasion using MRI was difficult in patients with EC with adenomyosis.[39],[40] The combination of T2-weighted imaging, diffusion-weighted imaging, and dynamic contrast-enhanced MRI was suggested to be the most accurate protocol for estimating myometrial invasion of EC.[41],[42] On the other hand, some studies reported the difficulty in assessing myometrial invasion by MRI in cases with large polypoid tumor, leiomyoma, adenomyosis, congenital anomalies, and small uterus.[39],[40] Considering the risk of postoperative upstaging to stage IB EC, contrast-enhanced MRI may be recommended in AEHs with such disease for evaluating myometrial invasion. However, detecting deep myometrial invasion may also be difficult in such cases even by contrast-enhanced MRI and careful perioperative management is required.

Table 4: Association between clinicopathological findings and final diagnoses (stage IB EC and AEH/stage IA EC)

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There are several limitations to this study. First, this was a retrospective study. Second, the sample size was small. Further prospective or large studies are required to examine the characteristics of patients with EC underdiagnosed with AEH before surgery.

In conclusion, 35% of patients who underwent TLH with a preoperative diagnosis of AEH were diagnosed with EC postoperatively. There was a risk of upstaging to stage IB EC, especially in postmenopausal patients with adenomyosis. A highly accurate endometrial sampling and contrast-enhanced MRI are recommended for AEH, although the preoperative examination cannot completely detect the risk of EC with AEH. Surgical techniques for AEH are required to prevent cancer spillage in consideration of its coexistence, such as tubal sealing before manipulator insertion or avoiding the use of manipulator.

Acknowledgment

We gratefully acknowledge the cooperation of the participating hospitals affiliated with the Department of OB/GYN in The Jikei University School of Medicine. We also thank Enago (www.enago.jp) for English language edition.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 

  References 
1.Dunton CJ, Baak JP, Palazzo JP, van Diest PJ, McHugh M, Widra EA. Use of computerized morphometric analyses of endometrial hyperplasias in the prediction of coexistent cancer. Am J Obstet Gynecol 1996;174:1518-21.  
    2.Costales AB, Schmeler KM, Broaddus R, Soliman PT, Westin SN, Ramirez PT, et al. Clinically significant endometrial cancer risk following a diagnosis of complex atypical hyperplasia. Gynecol Oncol 2014;135:451-4.  
    3.Valenzuela P, Sanz JM, Keller J. Atypical endometrial hyperplasia: Grounds for possible misdiagnosis of endometrial adenocarcinoma. Gynecol Obstet Invest 2003;56:163-7.  
    4.Shutter J, Wright TC Jr. Prevalence of underlying adenocarcinoma in women with atypical endometrial hyperplasia. Int J Gynecol Pathol 2005;24:313-8.  
    5.Doherty MT, Sanni OB, Coleman HG, Cardwell CR, McCluggage WG, Quinn D, et al. Concurrent and future risk of endometrial cancer in women with endometrial hyperplasia: A systematic review and meta-analysis. PLoS One 2020;15:e0232231.  
    6.Rakha E, Wong SC, Soomro I, Chaudry Z, Sharma A, Deen S, et al. Clinical outcome of atypical endometrial hyperplasia diagnosed on an endometrial biopsy: Institutional experience and review of literature. Am J Surg Pathol 2012;36:1683-90.  
    7.Vetter MH, Smith B, Benedict J, Hade EM, Bixel K, Copeland LJ, et al. Preoperative predictors of endometrial cancer at time of hysterectomy for endometrial intraepithelial neoplasia or complex atypical hyperplasia. Am J Obstet Gynecol 2020;222:60.e1-60.e7.  
    8.Trimble CL, Kauderer J, Zaino R, Silverberg S, Lim PC, Burke JJ 2nd, et al. Concurrent endometrial carcinoma in women with a biopsy diagnosis of atypical endometrial hyperplasia: A Gynecologic Oncology Group study. Cancer 2006;106:812-9.  
    9.Kanda Y. Investigation of the freely available easy-to-use software 'EZR' for medical statistics. Bone Marrow Transplant 2013;48:452-8.  
    10.Jobo T. Endometrial cytology and biopsy in endometrial carcinoma diagnosis: Advantages and disadvantage. J Jpn Soc Clin Cytol 2008;47:330-6.  
    11.Bourdel N, Chauvet P, Tognazza E, Pereira B, Botchorishvili R, Canis M. Sampling in atypical endometrial hyperplasia: Which method results in the lowest underestimation of endometrial cancer? A systematic review and meta-analysis. J Minim Invasive Gynecol 2016;23:692-701.  
    12.Leitao MM Jr., Han G, Lee LX, Abu-Rustum NR, Brown CL, Chi DS, et al. Complex atypical hyperplasia of the uterus: Characteristics and prediction of underlying carcinoma risk. Am J Obstet Gynecol 2010;203: 6.e1-6.  
    13.Suh-Burgmann E, Hung YY, Armstrong MA. Complex atypical endometrial hyperplasia: The risk of unrecognized adenocarcinoma and value of preoperative dilation and curettage. Obstet Gynecol 2009;114:523-9.  
    14.Zhang C, Wang EY, Liu F, Sung CJ, Quddus MR, Ou J, et al. Routine histologic features in complex atypical hyperplasia can predict the presence of endometrial carcinoma: A clinicopathological study of 222 cases. Hum Pathol 2018;80:40-6.  
    15.Huang GS, Gebb JS, Einstein MH, Shahabi S, Novetsky AP, Goldberg GL. Accuracy of preoperative endometrial sampling for the detection of high-grade endometrial tumors. Am J Obstet Gynecol 2007;196:5.e1-5.  
    16.Machado F, Moreno J, Carazo M, León J, Fiol G, Serna R. Accuracy of endometrial biopsy with the Cornier pipelle for diagnosis of endometrial cancer and atypical hyperplasia. Eur J Gynaecol Oncol 2003;24:279-81.  
    17.Piriyev E, Mellin W, Römer T. Comparison of aspirating pipettes and hysteroscopy with curettage. Arch Gynecol Obstet 2020;301:1485-92.  
    18.Elsandabesee D, Greenwood P. The performance of Pipelle endometrial sampling in a dedicated postmenopausal bleeding clinic. J Obstet Gynaecol 2005;25:32-4.  
    19.Guido RS, Kanbour-Shakir A, Rulin MC, Christopherson WA. Pipelle endometrial sampling. Sensitivity in the detection of endometrial cancer. J Reprod Med 1995;40:553-5.  
    20.Oda K, Koga K, Hirata T, Maruyama M, Ikemura M, Osuga Y, et al. Risk of endometrial cancer in patients with a preoperative diagnosis of atypical endometrial hyperplasia treated with total laparoscopic hysterectomy. Gynecol Minim Invasive Ther 2016;5:69-73.  
    21.Giannella L, Delli Carpini G, Sopracordevole F, Papiccio M, Serri M, Giorda G, et al. Atypical endometrial hyperplasia and unexpected cancers at final histology: A study on endometrial sampling methods and risk factors. Diagnostics (Basel) 2020;10:E474.  
    22.Polyzos NP, Mauri D, Tsioras S, Messini CI, Valachis A, Messinis IE. Intraperitoneal dissemination of endometrial cancer cells after hysteroscopy: A systematic review and meta-analysis. Int J Gynecol Cancer 2010;20:261-7.  
    23.Chang YN, Zhang Y, Wang YJ, Wang LP, Duan H. Effect of hysteroscopy on the peritoneal dissemination of endometrial cancer cells: A meta-analysis. Fertil Steril 2011;96:957-61.  
    24.Obermair A, Geramou M, Gucer F, Denison U, Graf AH, Kapshammer E, et al. Does hysteroscopy facilitate tumor cell dissemination? Incidence of peritoneal cytology from patients with early stage endometrial carcinoma following dilatation and curettage (D & C) versus hysteroscopy and D & C. Cancer 2000;88:139-43.  
    25.Stachowicz N, Mazurek D, Łoziński T, Czekierdowski A. Diagnostic hysteroscopy and the risk of malignant cells intraabdominal spread in women with endometrial cancer. Ginekol Pol 2017;88:562-7.  
    26.Ben-Arie A, Tamir S, Dubnik S, Gemer O, Ben Shushan A, Dgani R, et al. Does hysteroscopy affect prognosis in apparent early-stage endometrial cancer? Int J Gynecol Cancer 2008;18:813-9.  
    27.Janda M, Gebski V, Davies LC, Forder P, Brand A, Hogg R, et al. Effect of total laparoscopic hysterectomy vs. total abdominal hysterectomy on disease-free survival among women with stage I endometrial cancer: A randomized clinical trial. JAMA 2017;317:1224-33.  
    28.Walker JL, Piedmonte MR, Spirtos NM, Eisenkop SM, Schlaerth JB, Mannel RS, et al. Recurrence and survival after random assignment to laparoscopy versus laparotomy for comprehensive surgical staging of uterine cancer: Gynecologic Oncology Group LAP2 Study. J Clin Oncol 2012;30:695-700.  
    29.Yamagami W, Mikami M, Nagase S, Tabata T, Kobayashi Y, Kaneuchi M, et al. Japan Society of Gynecologic Oncology 2018 guidelines for treatment of uterine body neoplasms. J Gynecol Oncol 2020;31:e18.  
    30.Takeshima N, Hirai Y, Yano K, Tanaka N, Yamauchi K, Hasumi K. Ovarian metastasis in endometrial carcinoma. Gynecol Oncol 1998;70:183-7.  
    31.Cramer DW. The epidemiology of endometrial and ovarian cancer. Hematol Oncol Clin North Am 2012;26:1-12.  
    32.Shalowitz DI, Goodwin A, Schoenbachler N. Does surgical treatment of atypical endometrial hyperplasia require referral to a gynecologic oncologist? Am J Obstet Gynecol 2019;220:460-4.  
    33.Touhami O, Grégoire J, Renaud MC, Sebastianelli A, Grondin K, Plante M. The utility of sentinel lymph node mapping in the management of endometrial atypical hyperplasia. Gynecol Oncol 2018;148:485-90.  
    34.Lee M, Nam EJ, Kim S, Kim JH, Kim YT, Kim SW. Two-port access laparoscopic surgery in gynecologic oncology. Int J Gynecol Cancer 2013;23:935-42.  
    35.Padilla-Iserte P, Lago V, Tauste C, Díaz-Feijoo B, Gil-Moreno A, Oliver R, et al. Impact of uterine manipulator on oncological outcome in endometrial cancer surgery. Am J Obstet Gynecol 2021;224:65.e1-65.e11.  
    36.Wang PH, Yen MS, Yuan CC, Chao KC, Ng HT, Lee WL, et al. Port site metastasis after laparoscopic-assisted vaginal hysterectomy for endometrial cancer: Possible mechanisms and prevention. Gynecol Oncol 1997;66:151-5.  
    37.Shinohara S, Sakamoto I, Numata M, Ikegami A, Teramoto K. Risk of spilling cancer cells during total laparoscopic hysterectomy in low-risk endometrial cancer. Gynecol Minim Invasive Ther 2017;6:113-5.  
    38.Koshiyama M, Morita Y, Fujii H, Kobashi Y, Yoshida M. Gynecologic malignancies accompanied by benign hormone-dependent diseases. Menopause 2001;8:149-50.  
    39.Kinkel K. Pitfalls in staging uterine neoplasm with imaging: A review. Abdom Imaging 2006;31:164-73.  
    40.Scoutt LM, McCarthy SM, Flynn SD, Lange RC, Long F, Smith RC, et al. Clinical stage I endometrial carcinoma: Pitfalls in preoperative assessment with MR imaging. Work in progress. Radiology 1995;194:567-72.  
    41.Andreano A, Rechichi G, Rebora P, Sironi S, Valsecchi MG, Galimberti S. MR diffusion imaging for preoperative staging of myometrial invasion in patients with endometrial cancer: A systematic review and meta-analysis. Eur Radiol 2014;24:1327-38.  
    42.Nougaret S, Horta M, Sala E, Lakhman Y, Thomassin-Naggara I, Kido A, et al. Endometrial cancer MRI staging: Updated Guidelines of the European Society of Urogenital Radiology. Eur Radiol 2019;29:792-805.  
    

 
 

  [Table 1], [Table 2], [Table 3], [Table 4]