Obstetrics & Gynecology:
Coexisting Ovarian Malignancy in Young Women With Endometrial Cancer
Walsh, Christine MD1,2,3; Holschneider, Christine MD2; Hoang, Yen MD1; Tieu, Khai MD1; Karlan, Beth MD1; Cass, Ilana MD1
From the 1Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, UCLA and Cedars-Sinai Medical Centers, Los Angeles, California; 2Division of Gynecologic Oncology, Olive View-UCLA Medical Center, Los Angeles, California; and 3Division of Gynecologic Oncology, Kaiser Permanente, Los Angeles, California.
See related editorial on page 680.
Corresponding author: Ilana Cass, MD, Division of Gynecologic Oncology, Cedars-Sinai Medical Center, 8700 Beverly Boulevard #160W, Los Angeles, CA 90048; e-mail: firstname.lastname@example.org.
OBJECTIVE: In premenopausal women with endometrial cancer, ovarian preservation may be a consideration. Our objective was to examine the occurrence of coexisting ovarian malignancy and to identify predictors of adnexal involvement.
METHODS: With institutional review board approval, a retrospective chart review was conducted of young women with endometrial cancer identified at 4 affiliated institutions from 1996 to 2004.
RESULTS: Among 102 young women (aged 24–45 years) who underwent hysterectomy for endometrial cancer, 26 (25%) were found to have coexisting epithelial ovarian tumors: 23 were classified as synchronous primaries, and 3 as metastases. Ovarian cancer histology was endometrioid in 92% of cases. Among the 26 cases of coexisting ovarian involvement, 12 (46%) had grade 1 endometrial cancer on preoperative biopsy, 4 (15%) had normal preoperative imaging of the adnexa, and 4 (15%) had benign-appearing ovaries at the time of intraoperative assessment. On final pathology, 18 of 26 cases (69%) occurred in patients with grade 1 endometrial cancers, and 15 (58%) occurred with inner myometrial invasion. Our study further highlights the risk of conservative management with 1 case of ovarian cancer diagnosed 9 months after hysterectomy with ovarian conservation for a stage IA, grade 1 endometrial cancer and a case of advanced endometrial cancer metastatic to the ovaries developing 3 years after successful resolution of a grade 1 endometrial cancer treated with megestrol acetate (Megace).
CONCLUSION: Careful preoperative and intraoperative assessment of the adnexa is mandatory in young women with endometrial cancer. Those who desire ovarian preservation should be counseled regarding the high rate of coexisting ovarian malignancy.
LEVEL OF EVIDENCE: II-3
The diagnosis of endometrial cancer in a young, premenopausal woman may present the patient and her physician with the question of conservative management or ovarian preservation. Standard treatment includes hysterectomy and bilateral salpingo-oophorectomy (BSO) and results in an abrupt loss of fertility as well as surgical menopause with its attendant symptoms. The option of conservative treatment with progestins, usually in the context of fertility preservation, has been advocated as a safe alternative by a number of groups.1–7 However, there are also reports of a higher incidence of ovarian malignancy in this young subset of women who may be considering uterine or ovarian preservation, with a range of 5 to 29% reported in the literature.8–11
Knowledge of the potential risk for a coexisting ovarian malignancy has important implications for counseling and management of young patients with endometrial cancer. Our objectives in this study were to determine the frequency of coexisting ovarian malignancies in young women with endometrial cancer and to identify predictors for coexisting ovarian malignancy that might assist with clinical decision making.
MATERIALS AND METHODS
Institutional review board approval was obtained at Cedars-Sinai Medical Center, University of California Los Angeles Medical Center, Olive View-UCLA, and Kaiser-Sunset Medical Center to perform this study. Patients aged 45 years or younger with a histologic diagnosis of endometrial cancer treated with hysterectomy between 1996 and 2004 were identified through a search of pathology and gynecologic oncology databases and gynecologic oncology clinic records. A single investigator (C.W.) reviewed all pathology reports to identify eligible patients. Patients with type 2 endometrial cancer (uterine papillary serous carcinoma or clear cell carcinoma), advanced stage (stage 4) endometrial cancer, or both were excluded from the analysis, because these patients would be unlikely candidates for conservative treatment.
Pathology specimens were reviewed by a gynecologic pathologist at the time of original diagnosis, and ovarian malignancy was classified as synchronously arising or metastatic based upon features of the malignancies at the 2 sites.12 Approximately one half (54%) of the cases with adnexal involvement were available for re-review by a gynecologic pathologist, who confirmed the presence of malignancy in the ovary in all cases. A diagnosis of synchronously arising tumors was assigned based upon superficial or no myometrial invasion, low grade and stage of the endometrial tumor, low grade and stage of the ovarian tumor, dissimilar grades between the uterine and ovarian sites, or dissimilar tumor histologies. Metastasis from the endometrium to the ovary was characterized by deep myometrial invasion, lymph–vascular space invasion, high-grade histologies, the pattern of tumor in the adnexa, and the pattern of extra-pelvic tumor metastases. However, the distinction between synchronous and metastatic disease was limited by the uncertainties of assignment by pathologic criteria alone. Information regarding patient age, body mass index, medical and family histories, reproductive history, preoperative and intraoperative evaluation, use of adjuvant treatment, and follow-up were abstracted from the medical record.
One hundred two young patients, aged 45 years or younger, underwent hysterectomy for type 1 endometrial cancer. Table 1 reviews their clinical and reproductive characteristics. The majority of patients were overweight, with a body mass index of greater than 25. A significant proportion of patients had some reproductive abnormality, with either irregular menses, history of polycystic ovarian syndrome, or infertility. It is striking that in this young population, 11% and 15% of patients carried a diagnosis of diabetes or hypertension, respectively. One half of the patients had a diagnosis of cancer in a first or second-degree relative, but no patient had a family history that met the Amsterdam II criteria for hereditary nonpolyposis colorectal cancer syndrome.13 Before hysterectomy, 26 (25%) patients were treated with hormones for a range of 1–48 months. At the time of hysterectomy, 16 (16%) patients chose ovarian preservation. The majority of uterine tumors were early stage, low grade, endometrioid adenocarcinomas.
Among the 102 women who had a hysterectomy for endometrial cancer, 26 (25%) had coexisting ovarian malignancies. Table 2 demonstrates the pathologic characteristics of the endometrial and ovarian tumors in all 26 patients, including 1 patient who had a subsequent diagnosis of ovarian malignancy 9 months after hysterectomy with ovarian preservation (case S3). The remaining 25 patients were diagnosed at the time of initial surgical exploration with hysterectomy and BSO.
All ovarian tumors were of epithelial origin. There were no granulosa cell tumors. With the exception of 1 patient with a mucinous ovarian cancer (case S16), all of the patients had endometrioid or adenosquamous histology of the ovary (Table 2). Of note, 18 of the 26 cases (69%) occurred in patients with grade 1 endometrial cancer and 15 (58%) occurred in patients with less than 50% myometrial invasion (stage 1A or 1B endometrial cancer). In the first 23 cases (S1–S23), pathologic findings were suggestive for synchronous endometrial and ovarian primaries. The remaining 3 cases (M1–M3), were characterized as metastases from the endometrial tumor to the adnexa.
Table 3 illustrates the preoperative endometrial sampling, imaging, and intraoperative findings among young women with endometrial cancer (26 with and 76 without adnexal involvement). Traditional factors associated with low-risk disease such as low-grade did not reliably predict absence of adnexal pathology. Among 62 patients with a grade 1 tumor on preoperative endometrial sampling, 12 (19%) were ultimately found to have malignant adnexal pathology. Alternatively, among 26 patients with malignant adnexal involvement, 12 (46%) had grade 1 tumor on preoperative endometrial sampling.
Among the 26 patients with confirmed adnexal malignancy, 14 patients had preoperative imaging with pelvic ultrasound, computed tomography, magnetic resonance imaging, or a combination of modalities. Ten of the 14 (71%) had abnormal imaging of the adnexa, with masses ranging from 2.8 cm to 14 cm in size. Four patients (29%) had benign imaging findings of the adnexa: the ovaries appeared normal in 2 cases and contained small (less than 2 cm) physiologic-appearing cysts in the other 2 cases. Stated differently, 4 of 46 (9%) of patients with normal imaging of the adnexa were ultimately found to have adnexal malignancy.
Information regarding intraoperative adnexal findings was available for 21 of the 26 patients with adnexal involvement. Ovarian masses ranging in size from 3 cm to 12 cm were present in 14 (67%), surface excrescences were present in 3 (14%), and no gross abnormalities were found in 4 (19%). In 3 of these 4 cases, the operative reports commented on slightly cystic but otherwise normal-appearing ovaries. Final pathologic examination of the specimens revealed these ovaries to harbor a 0.8-cm metastasis, a 0.1-cm synchronous ovarian tumor, and a 2.5-cm endometrioid ovarian cancer. In the fourth case, the operative report commented on benign-appearing ovaries, and final pathology revealed a 4.5-cm endometrioid ovarian adenocarcinoma arising in endometriosis.
Twenty-six patients underwent hormonal treatment for endometrial cancer for a range of 1 to 48 months before ultimate surgical management. There were four cases (15%) of ovarian cancer diagnosed among this cohort. In the first case (Table 2, case M1), a 43 year-old patient had an initial diagnosis of grade 1 endometrioid adenocarcinoma on an endometrial biopsy and was successfully treated with megestrol acetate (Megace, Bristol-Myers Squibb, Princeton, NJ) 240 mg each day. Results of a follow-up biopsy 7 months later were negative, and she was changed to oral contraceptive pills. Her endometrial cancer recurred 41 months later and was notable for metastases to both ovaries and extension to the parametria, cervical stroma, and outer myometrium at the time of surgical treatment. Two additional cases (M2, M3) were found to have endometrial cancer metastases to the ovaries after unsuccessful hormonal treatment for 2 and 5 months. In the fourth case (S3), a 37 year-old patient underwent hormonal treatment for 7 months before hysterectomy with ovarian conservation for a stage IA, grade 1 endometrial cancer. During a subsequent infertility workup with a plan for egg aspiration and surrogate gestational carrier, she was found to have a 4-cm ovarian cyst. She underwent a second staging surgery 9 months after hysterectomy and was found to have a stage IC, grade 1 endometrioid ovarian cancer.
Overall, 16 patients had ovarian preservation at the time of hysterectomy for endometrial cancer. All had stage IA or IB endometrioid endometrial cancers and normal intraoperative evaluation of the adnexa except for the finding of polycystic ovaries in 2 cases. During a median follow-up time of 13 months (range 1 to 50 months), 3 of the 16 patients developed adnexal abnormalities requiring surgical removal, including case S3 reported above. The other 2 patients had pelvic masses detected during follow-up and underwent BSO 40 months and 46 months after hysterectomy. Pathology revealed benign cysts including bilateral cystadenofibromas in the first patient and a cystadenofibroma and corpus luteum in the second patient. The remaining 14 patients had not developed any adnexal pathology during follow-up.
An additional case that deserves mention is S18. This patient was diagnosed with a stage 2A, grade 1 endometrial cancer with a synchronous stage 1C, grade 1 endometrioid adenocarcinoma of the right ovary at the age of 35. Six years previously, she had been diagnosed with a stage IC endometrioid adenocarcinoma of the left ovary that was 13 cm in size. At the time, she was conservatively managed with a left salpingo-oophorectomy followed by no adjuvant therapy and a negative second look surgery.
Adjuvant treatment was administered to 21 of the 26 patients (81%) with coexisting ovarian and endometrial malignancies (Table 4). There were 5 recurrences and 1 case of progression during adjuvant therapy. A subsequent ovarian cancer diagnosis and a vaginal recurrence were both successfully salvaged with surgical treatment. Two recurrences to the lymph nodes were also managed surgically and a peritoneal recurrence was successfully treated with salvage chemotherapy. The case of progression was treated with chemotherapy. Over a median follow-up time of 34 months (range 3–103 months), 22 patients had no evidence of disease, and 4 patients were alive with disease and undergoing treatment.
In young women with a diagnosis of endometrial cancer, preservation of ovarian function is a complex, controversial issue. We found coexisting ovarian malignancies in 25% of our cohort of women aged 45 years or younger with type 1 endometrial cancer. This is within the range reported by other investigators8–11 and underscores the importance of careful adnexal assessment in the management of these young patients.
When confronted with the question of conservative nonsurgical management, ovarian preservation, or both in a young woman with endometrial cancer, it is important to counsel the patient about the risk of ovarian pathology and the lack of absolutely reliable preoperative or intraoperative predictors to guide decision-making. Candidates for fertility preservation with progestin treatment are restricted to those with low-grade endometrial histology. In our study, carcinoma of the adnexa was found in 19% who met this criterion. Additionally, a patient who successfully resolved her endometrial cancer on megestrol acetate recurred more than 3 years later with advanced disease that had metastasized to the ovaries.
Our tools for preoperative detection of ovarian malignancy are relatively insensitive and of limited value for preoperative counseling. Of the patients with negative preoperative imaging of the adnexa, 9% (4 of 46) were subsequently found to have a coexisting ovarian malignancy. Even intraoperative assessment of ovarian pathology is fallible, and 4 patients with benign-appearing ovaries at the time of surgery were found to have tumor in the adnexa on final pathologic examination. The presence of occult malignancy harbored in grossly normal-appearing ovaries in this population of young women has been reported by other authors.10 Additionally, normal adnexal findings at the time of hysterectomy do not protect the patient from developing a subsequent ovarian cancer, as was seen in 1 of our patients who chose ovarian preservation.
Ovarian tumors coexisting with endometrial malignancy have been generally regarded as synchronous primaries rather than metastases from one site to another based on the observation of a more favorable clinical prognosis9,14–27 as well as the pathologic appearance of the malignancy at the 2 sites.12 Several molecular studies have supported the hypothesis of independent origins by demonstrating different patterns of X chromosome inactivation and dissimilar mutations in PTEN, p53, or K-ras.28–30 However, a recent analysis based on loss of heterozygosity patterns reported a mere 53% concordance rate between the genetic and histopathologic diagnoses for dual site cancers, highlighting our difficulty in accurately making the distinction.31 Despite the majority of our cases being classified as synchronous primaries, the vast majority received adjuvant chemotherapy, further underscoring the uncertainty of the diagnosis or the optimal treatment. It was not the primary objective of our study to differentiate between synchronously arising tumors and ovarian metastases, but rather to determine the rate of any type of adnexal involvement in young patients with endometrial cancer.
Nevertheless, this phenomenon of synchronously arising malignancies of the female genital tract seems to be more commonly seen in premenopausal women than postmenopausal women.10 The occurrence of multiple malignancies decades earlier than expected raises the question of genetic susceptibility. In our study, we did not find any family histories that were clearly suggestive of an inherited genetic syndrome. However, the unusual characteristics of this cohort, including the high incidence of concordant endometrioid histology24,32 and the young age of onset of malignancy warrant further investigation. In the general population, endometrioid histology accounts for 16–24% of the epithelial ovarian carcinomas.23,33 In our study, 96% of ovarian tumors found concurrently with type 1 endometrial cancers were endometrioid or adenosquamous. In the literature, figures as high as 88% endometrioid ovarian histology in simultaneously detected endometrial and ovarian carcinomas are reported.32 No stimulating factor has yet been described to account for the effect, although estrogens,34 androgens,10 and endometriosis35,36 have been hypothesized as contributing factors.
The cause of the simultaneously arising neoplasms has yet to be elucidated. It has been suggested that embryologically similar tissues, such as those of the female genital tract, may be subject to the same carcinogenic or hormonal stimuli and thereby develop synchronous neoplasms.37–39 Interestingly, in our case series, we describe a 29-year-old patient diagnosed with stage IC endometrioid adenocarcinoma of the ovary with a subsequent diagnosis of stage 2A, grade 1 endometrial cancer with a synchronously arising stage IC, grade 1 endometrioid adenocarcinoma of the remaining ovary 6 years later. This case may illustrate a persistent carcinogenic effect and risk of future development of an endometrioid adenocarcinoma of preserved ovaries or endometrium.
Based on our data, we would recommend a cautious approach to ovarian preservation in young patients with endometrial cancer. The high incidence of coexisting malignancy in the ovaries and the young age of diagnosis suggest an increased susceptibility of the reproductive organs to carcinogenic transformation. This elevated risk may reflect a different underlying biology that is at play in the reproductive tracts of young women who develop endometrial cancer. We would suggest the need for a heightened awareness of the risk of concurrent adnexal malignancy in these young patients. Others have suggested the use of laparoscopy to rule out adnexal pathology before embarking on conservative hormonal treatment.40 If a BSO is performed, careful intraoperative evaluation and possible frozen section may minimize the possibility of delayed detection of adnexal malignancy. If the ovaries are preserved at the time of hysterectomy, patients may need continued postoperative surveillance of the retained adnexa. At the minimum, careful assessment of the adnexa by some method is warranted in all young patients with endometrial cancer.
1. Randall TC, Kurman RJ. Progestin treatment of atypical hyperplasia and well-differentiated carcinoma of the endometrium in women under age 40. Obstet Gynecol 1997;90:434–40.
2. Ramirez PT, Frumovitz M, Bodurka DC, Sun CC, Levenback C. Hormonal therapy for the management of grade 1 endometrial adenocarcinoma: a literature review. Gynecol Oncol 2004;95:133–8.
3. Niwa K, Tagami K, Lian Z, Onogi K, Mori H, Tamaya T. Outcome of fertility-preserving treatment in young women with endometrial carcinomas. BJOG 2005;112:317–20.
4. Nakao Y, Nomiyama M, Kojima K, Matsumoto Y, Yamasaki F, Iwasaka T. Successful pregnancies in 2 infertile patients with endometrial adenocarcinoma. Gynecol Obstet Invest 2004;58:68–71.
5. Lowe MP, Cooper BC, Sood AK, Davis WA, Syrop CH, Sorosky JI. Implementation of assisted reproductive technologies following conservative management of FIGO grade I endometrial adenocarcinoma and/or complex hyperplasia with atypia. Gynecol Oncol 2003;91:569–72.
6. Gotlieb WH, Beiner ME, Shalmon B, Korach Y, Segal Y, Zmira N, et al. Outcome of fertility-sparing treatment with progestins in young patients with endometrial cancer. Obstet Gynecol 2003;102:718–25.
7. Emons G, Heyl W. Hormonal treatment of endometrial cancer. J Cancer Res Clin Oncol 2000;126:619–23.
8. Crissman JD, Azoury RS, Barnes AE, Schellhas HF. Endometrial carcinoma in women 40 years of age or younger. Obstet Gynecol 1981;57:699–704.
9. Gitsch G, Hanzal E, Jensen D, Hacker NF. Endometrial cancer in premenopausal women 45 years and younger. Obstet Gynecol 1995;85:504–8.
10. Evans-Metcalf ER, Brooks SE, Reale FR, Baker SP. Profile of women 45 years of age and younger with endometrial cancer. Obstet Gynecol 1998;91:349–54.
11. Duska LR, Garrett A, Rueda BR, Haas J, Chang Y, Fuller AF. Endometrial cancer in women 40 years old or younger. Gynecol Oncol 2001;83:388–93.
12. Ulbright TM, Roth LM. Metastatic and independent cancers of the endometrium and ovary: a clinicopathologic study of 34 cases. Hum Pathol 1985;16:28–34.
13. Vasen HF, Watson P, Mecklin JP, Lynch HT. New clinical criteria for hereditary nonpolyposis colorectal cancer (HNPCC, Lynch syndrome) proposed by the International Collaborative group on HNPCC. Gastroenterology 1999;116:1453–6.
14. McGee W. Carcinoma of the endometrium in women under forty years of age; report of three cases. Obstet Gynecol 1958;11:388–90.
15. Gallup DG, Stock RJ. Adenocarcinoma of the endometrium in women 40 years of age or younger. Obstet Gynecol 1984;64:417–20.
16. Geisler HE, Huber CP, Rogers S. Carcinoma of the endometrium in premenopausal women. Am J Obstet Gynecol 1969;104:657–63.
17. Kempson RL, Pokorny GE. Adenocarcinoma of the endometrium in women aged forty and younger. Cancer 1968;21:650–62.
18. Peterson EP. Endometrial carcinoma in young women: a clinical profile. Obstet Gynecol 1968;31:702–7.
19. Rose PG, Herterick EE, Boutselis JG, Moeshberger M, Sachs L. Multiple primary gynecologic neoplasms. Am J Obstet Gynecol 1987;157:261–7.
20. Dockerty MB. Primary and secondary ovarian adeno-acanthoma. Surg Gynecol Obstet 1954;99:392–400.
21. Zaino RJ, Unger ER, Whitney C. Synchronous carcinomas of the uterine corpus and ovary. Gynecol Oncol 1984;19:329–35.
22. Axelrod JH, Fruchter R, Boyce JG. Multiple primaries among gynecologic malignancies. Gynecol Oncol 1984;18:359–72.
23. Czernobilsky B, Silverman BB, Mikuta JJ. Endometrioid carcinoma of the ovary: a clinicopathologic study of 75 cases. Cancer 1970;26:1141–52.
24. Eifel P, Hendrickson M, Ross J, Ballon S, Martinez A, Kempson R. Simultaneous presentation of carcinoma involving the ovary and the uterine corpus. Cancer 1982;50:163–70.
25. Matlock DL, Salem FA, Charles EH, Savage EW. Synchronous multiple primary neoplasms of the upper female genital tract. Gynecol Oncol 1982;13:271–7.
26. Piura B, Glezerman M. Synchronous carcinomas of endometrium and ovary. Gynecol Oncol 1989;33:261–4.
27. Eisner RF, Nieberg RK, Berek JS. Synchronous primary neoplasms of the female reproductive tract. Gynecol Oncol 1989;33:335–9.
28. Fujita M, Enomoto T, Wada H, Inoue M, Okudaira Y, Shroyer KR. Application of clonal analysis: differential diagnosis for synchronous primary ovarian and endometrial cancers and metastatic cancer. Am J Clin Pathol 1996;105:350–9.
29. Lin WM, Forgacs E, Warshal DP, Yeh IT, Martin JS, Ashfaq R, et al. Loss of heterozygosity and mutational analysis of the PTEN/MMAC1 gene in synchronous endometrial and ovarian carcinomas. Clin Cancer Res 1998;4:2577–83.
30. Caduff RF, Svoboda-Newman SM, Bartos RE, Ferguson AW, Frank TS. Comparative analysis of histologic homologues of endometrial and ovarian carcinoma. Am J Surg Pathol 1998;22:319–26.
31. Brinkmann D, Ryan A, Ayhan A, McCluggage WG, Feakins R, Santibanez-Koref MF, et al. A molecular genetic and statistical approach for the diagnosis of dual-site cancers. J Natl Cancer Inst 2004;96:1441–6.
32. Zaino R, Whitney C, Brady MF, DeGeest K, Burger RA, Buller RE. Simultaneously detected endometrial and ovarian carcinomas—a prospective clinicopathologic study of 74 cases: a gynecologic oncology group study. Gynecol Oncol 2001;83:355–62.
33. Long ME, Taylor HC Jr. Endometrioid carcinoma of the ovary. Am J Obstet Gynecol 1964;90:936–50.
34. Silverman BB, O’Neill RT, Mikuta JJ. Multiple malignant tumors associated with primary carcinoma of the ovary. Surg Gynecol Obstet 1972;134:243–8.
35. Choo YC, Naylor B. Multiple primary neoplasms of the ovary and uterus. Int J Gynaecol Obstet 1982;20:327–34.
36. Cummins PA, Fox H, Langley FA. An electron-microscopic study of the endometrioid adenocarcinoma of the ovary and a comparison of its fine structure with that of normal endometrium and of adenocarcinoma of the endometrium. J Pathol 1974;113:165–73.
37. Woodruff JD, Julian CG. Multiple malignancy in the upper genital canal. Am J Obstet Gynecol 1969;103:810–22.
38. Woodruff JD, Solomon D, Sullivant H. Multifocal disease in the upper genital canal. Obstet Gynecol 1985;65:695–8.
39. Lauchlan SC. The secondary Mullerian system. Obstet Gynecol Surv 1972;27:133–46.
40. Morice P, Fourchotte V, Sideris L, Gariel C, Duvillard P, Castaigne D. A need for laparoscopic evaluation of patients with endometrial carcinoma selected for conservative treatment. Gynecol Oncol 2005;96:245–8.
This article has been cited 37 time(s).
Human Reproduction UpdateAutotransplantation of cryopreserved ovarian tissue in cancer survivors and the risk of reintroducing malignancy: a systematic reviewHuman Reproduction Update
Gynecologic OncologyFertility preserving treatments for endometrial cancer: The unanswered questionsGynecologic Oncology
Journal of Ovarian ResearchSimultaneous early ovarian and endometrial cancer treated conservatively with spontaneous pregnancyJournal of Ovarian Research
Gynecologic and Obstetric InvestigationControversies of the Hormonal Conservative Treatment of Endometrial CancerGynecologic and Obstetric Investigation
Fertility and SterilitySafety of ovarian preservation in young patients with early-stage endometrial cancer: a retrospective study and meta-analysisFertility and Sterility
European Review for Medical and Pharmacological Sciences
Fertility-sparing treatment of endometrial cancer precursors among young women: a reproductive point of view
European Review for Medical and Pharmacological Sciences, 16():
Reproductive issues in the gynecologic cancer patient
Oncology-New York, 21(5):
Clinical & Translational OncologyConservative management of patients with early endometrial carcinoma: A systematic reviewClinical & Translational Oncology
Gynecologic OncologyYoung patients with endometrial cancer: How many could be eligible for fertility-sparing treatment?Gynecologic Oncology
HistopathologySynchronous tumours of the female genital tractHistopathology
American Journal of Surgical Pathology
Endometrial Carcinomas in Women Aged 40 Years and Younger: Tumors Associated With Loss of DNA Mismatch Repair Proteins Comprise a Distinct Clinicopathologic Subset
American Journal of Surgical Pathology, 33():
Cervical Signet-Ring Cell Carcinoma Presenting as a Synchronous Primary Carcinoma With Uterine Adenocarcinoma
Military Medicine, 174(2):
Journal of Clinical OncologySafety of Ovarian Preservation in Premenopausal Women With Endometrial CancerJournal of Clinical Oncology
Gynecologic OncologyOvarian preservation and staging in reproductive-age endometrial cancer patientsGynecologic Oncology
Journal of Gynecologic OncologyPremenopausal early-stage endometrial carcinoma patients with low CA-125 levels and low tumor grade may undergo ovary-saving surgeryJournal of Gynecologic Oncology
Archives of Pathology & Laboratory Medicine
Population-based analysis of pathologic data - A new approach to the investigation of uterine endometrial and ovarian endometrioid carcinomas
Archives of Pathology & Laboratory Medicine, 131(9):
Fertility and SterilityStage I ovarian carcinoma: different clinical pathologic patternsFertility and Sterility
Fertility and SterilityOutcome of in vitro fertilization treatment in infertile women conservatively treated for endometrial adenocarcinomaFertility and Sterility
Gynecologic OncologyA review of the challenges faced in the conservative treatment of young women with endometrial carcinoma and risk of ovarian cancerGynecologic Oncology
Gynecologic and Obstetric InvestigationFertility-Sparing in Endometrial CancerGynecologic and Obstetric Investigation
Gynecologic OncologyYoung patients with endometrial carcinoma selected for conservative treatment: A need for vigilance for synchronous ovarian carcinomas, case report and literature reviewGynecologic Oncology
Pathology Research and PracticeCoexisting endometrial and ovarian carcinomas: A retrospective clinicopathological studyPathology Research and Practice
Gynecologic OncologyFeasibility of ovarian preservation in patients with early stage endometrial carcinomaGynecologic Oncology
Gynecologic OncologyUse of gene expression profiles to stage concurrent endometrioid tumors of the endometrium and ovaryGynecologic Oncology
Clinical Cancer ResearchMolecular, pathologic, and clinical features of early-onset endometrial cancer: Identifying presumptive lynch syndrome patientsClinical Cancer Research
Gynecologic OncologyOvarian preservation during the surgical treatment of early stage endometrial cancer: A nation-wide study conducted by the Korean Gynecologic Oncology GroupGynecologic Oncology
Mayo Clinic Proceedings
Current issues in the management of endometrial cancer
Mayo Clinic Proceedings, 83(1):
International Journal of Gynecology & ObstetricsSynchronous early-stage endometrial and ovarian cancerInternational Journal of Gynecology & Obstetrics
Seminars in OncologyManagement of Early-Stage Endometrial CancerSeminars in Oncology
OnkologeSpecial cases of endometrial carcinoma. Fertility retention and prevention in high-risk patientsOnkologe
Journal of Clinical OncologyMulticenter phase II study of fertility-sparing treatment with medroxyprogesterone acetate for endometrial carcinoma and atypical hyperplasia in young womenJournal of Clinical Oncology
Gynecological EndocrinologyThe fertility-sparing treatment in patients with endometrial atypical hyperplasia and early endometrial cancer: A debated therapeutic optionGynecological Endocrinology
European Journal of Obstetrics & Gynecology and Reproductive BiologyEndometrial cancer: molecular and therapeutic aspectsEuropean Journal of Obstetrics & Gynecology and Reproductive Biology
Current Opinion in Obstetrics and GynecologyEndometrial cancer and fertilityCurrent Opinion in Obstetrics and Gynecology
Obstetrics & GynecologyEndometrial Cancer With Concurrent Ovarian Malignancy: Assessing the RisksObstetrics & Gynecology
International Journal of Gynecological CancerConservative Treatment With Progestin and Pregnancy Outcomes in Endometrial CancerInternational Journal of Gynecological Cancer
© 2005 by The American College of Obstetricians and Gynecologists.