Safety of Fertility-Sparing Surgery in Primary Mucinous Carcinoma of the Ovary

Jung-Yun Lee; Yu Ri Jo; Tae Hun Kim; Hee Seung Kim; Min A Kim; Jae Weon Kim; Noh Hyun Park; Yong-Sang Song

doi:10.4143/crt.2014.004

Articles

Page Path: HOME > Cancer Res Treat > Volume 47(2); 2015 > Article

Original Article Safety of Fertility-Sparing Surgery in Primary Mucinous Carcinoma of the Ovary: Jung-Yun Lee, MD¹, Yu Ri Jo, MD¹, Tae Hun Kim, MD¹, Hee Seung Kim, MD¹, Min A Kim, MD, PhD², Jae Weon Kim, MD, PhD¹, Noh Hyun Park, MD, PhD¹, Yong-Sang Song, MD, PhD^1,3,4,; Cancer Research and Treatment : Official Journal of Korean Cancer Association 2015;47(2):290-297.
DOI: https://doi.org/10.4143/crt.2014.004
Published online: August 29, 2014

¹Department of Obstetrics and Gynecology, Seoul National University College of Medicine, Seoul, Korea

²Department of Pathology, Seoul National University College of Medicine, Seoul, Korea

³Cancer Research Institute, Seoul National University College of Medicine, Seoul, Korea

⁴Major in Biomodulation, World Class University, Seoul National University, Seoul, Korea

Correspondence: Yong-Sang Song, MD, PhD Department of Obstetrics and Gynecology, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul 110-744, Korea
Tel: 82-2-2072-2822 Fax: 82-2-762-3599 E-mail: yssong@snu.ac.kr

• Received: January 5, 2014 • Accepted: February 5, 2014

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

12,459 Views
107 Download
35 Web of Science
29 Crossref
39 Scopus

prev next

Full Article

Download PDF

Abstract
Introduction
Materials and Methods
Results
Discussion
Conclusion
NOTES
REFERENCES

Abstract

Purpose
The aim of this study is to evaluate the safety of fertility-sparing surgery as the treatment for patients with primary mucinous epithelial ovarian cancer.
Materials and Methods
A retrospective study of patients with mucinous ovarian cancer between 1991 and 2010 was performed. The demographics and survival outcomes were compared between patients who underwent fertility-sparing surgery and those who underwent radical surgery.
Results
A total of 110 patients underwent primary surgery. At the time of surgery, tumors appeared to be grossly confined to the ovaries in 90 patients, and evidence of metastasis was definite in 20 patients. Of the 90 patients with tumors that appeared to be grossly confined to the ovaries at surgical exploration, 35 (38.9%) underwent fertility-sparing surgery. The Kaplan-Meier curve and the log rank test showed no difference in either recurrence-free survival (p=0.792) or disease-specific survival (p=0.706) between the two groups. Furthermore, there was no significant difference in recurrence-free survival (p=0.126) or disease-specific survival (p=0.377) between the two groups, even when the analysis was limited to women below the age of 40. In a multivariate Cox model, fertility-sparing surgery had no effect on either recurrence-free survival (recurrence hazard ratio [HR], 1.20; 95% confidence interval [CI], 0.25 to 5.71) or disease-specific survival (death HR, 0.88; 95% CI, 0.17 to 4.60).
Conclusion
Fertility-sparing surgery in primary mucinous cancer grossly confined to the ovaries may be a safe option and one not associated with an increase in recurrence or mortality.
Key words: Mucinous adenocarcinoma, Ovarian epithelial cancer, Fertility-sparing surgery, Survival

Introduction

Epithelial ovarian cancer is the most lethal of the gynecologic cancers. Approximately 20% of all epithelial ovarian cancer are diagnosed at an early stage, and thus high survival rates have been reported for patients whose disease was identified at this stage [1]. Moreover, approximately 10% of all epithelial ovarian cancer occurs in women under the age of 40 years [2]. The safety of fertility-sparing surgery for women of childbearing age with early-stage disease has been evaluated over the past two decades [3-11]. The current guidelines recommend fertility-sparing surgery only in selected cases of early-stage ovarian cancer [12].

Primary mucinous carcinoma of the ovary accounts for 7% to 14% of all invasive epithelial ovarian cancers [13]. When compared to high-grade serous carcinoma, mucinous carcinoma has distinct presentation, clinical course, and response to therapy [14]. Moreover mucinous carcinoma is usually confined to the ovary at surgery, and the prognosis is favorable when found at an early stage [15]. For mucinous tumors apparently confined to the ovary, some studies have reported that complete surgical staging is unnecessary due to a low risk of upstaging [16,17]. Despite the infrequency of this subtype, previous studies have shown that about 27% of patients with stage I epithelial ovarian cancer have mucinous histology [18,19]. In Korea, mucinous carcinoma is the most common histologic subtype of stage I epithelial ovarian cancer [16]. Because early-stage mucinous carcinoma is usually found in young women [7-11], fertility preservation is a matter of great interest in considering mucinous tumors than for other histologic subtypes. However, the safety of fertility-sparing surgery in mucinous histology has not yet been determined.

In this study, we compare the long-term oncologic outcomes of fertility-sparing surgery with those of radical surgery in patients with apparent early-stage mucinous carcinoma.

Materials and Methods

1. Patients

After receiving approval from the Institutional Review Board, we reviewed all patients with primary mucinous carcinoma of the ovary diagnosed at Seoul National University Hospital between January 1991 and December 2010. A gynecologic oncology pathologist evaluated all cases. Patients with borderline malignancies or with metastatic mucinous ovarian carcinomas from other primary sites were excluded. Histological diagnosis was established according to the World Health Organization (WHO) classification.

Clinical and pathologic variables, such as age, International Federation of Gynecology and Obstetrics (FIGO) stage, year of diagnosis, grade, adjuvant chemotherapy, surgical procedure, and date of last contact or date of recurrence/death, were collected. In addition, we gathered information on the cause and date of death from death certificates obtained from the Korean National Statistical Office.

2. Treatment methods

Fertility-sparing surgery was performed if patients of childbearing age had a strong desire to retain fertility. These women were informed of the possible risks and benefits of fertility-sparing surgery and signed a consent form during a preoperative counseling session. Patients in the fertility-sparing surgery group underwent unilateral salpingo-oophorectomy on the side of the ovarian tumor with surgical exploration (cytology of peritoneal washing or ascites, careful palpation and inspection of the peritoneal cavity). Surgical staging procedures, such as peritoneal biopsy of suspicious lesions or random biopsy, appendectomy, omentectomy, and lymphadenectomy, were optional and conducted at the surgeon’s discretion. Otherwise, patients were categorized as being in the radical surgery group.

Adjuvant chemotherapy is based on the pathologic findings of the surgical specimen. Patients with stage IAG3 or IBG3, or any grades of IC, were treated with three to six courses of platinum-based chemotherapy. Two patients did not receive adjuvant chemotherapy despite indication.

3. Statistical analysis

Disease-specific survival was defined as the time from surgery to the date of death due to ovarian cancer. Recurrence-free survival was defined as the time from surgery to the date of recurrence.

The differences between clinical and demographic characteristics of the fertility-sparing surgery and radical surgery groups were compared with Student’s t-test for continuous variables and chi-square test or Fisher’s exact test for categorical variables. The recurrence-free and disease-specific survival curves were estimated using the Kaplan-Meier method, and the differences in survival between the groups were compared using the log rank test. Cox proportional hazards models were developed to examine the survival. In Cox proportional hazards analyses, the recurrence and death hazard ratios (HRs) were modeled and patients who underwent fertility preservation were compared with those who did not. All analyses were performed using STATA ver. 11.0 (StataCorp, College Station, TX). All p-values are two-sided.

Results

1. Patient characteristics

In total, 110 patients with mucinous epithelial ovarian cancer were identified in our cancer registry, all of which had undergone primary surgery. At the time of surgery, 90 patients (81.8%) had tumors grossly confined to the ovaries, and 20 patients (18.2%) had definite evidence of metastasis. Of the 90 patients with tumors grossly confined to the ovaries, 35 patients (38.9%) underwent fertility-sparing surgery based on the surgeon’s decision.

The baseline characteristics are shown in Table 1. The mean age at diagnosis was 28.6 years in the fertility-sparing surgery group and 50.3 years in the radical surgery group (p < 0.001). With the exception of age, the clinical characteristics were similar for both groups, including stage, year of diagnosis, adjuvant chemotherapy, tumor grade, and recurrence rate.

2. Upstaging after surgical staging

Table 2 shows the procedures performed at the time of surgical exploration and cases of microscopic metastasis after additional biopsies. Surgical staging led to upstaging for four patients who were identified as having invasive cancer following a peritoneal biopsy of a suspicious lesion or adhesion site. However, there were not any cases with upstaging occurrence based on random peritoneal biopsies without suspicious lesions. In addition, a positive peritoneal washing cytology was identified in eight patients. Among these patients, ovarian surface involvement or spontaneous rupture had already been identified in three cases, intraoperative rupture occurred in two patients, and invasive cancer was found following peritoneal biopsy in one patient. Therefore, only two patients were upstaged based solely on washing cytology, both of which were in the fertility-sparing surgery group. There was no case of upstaging following lymphadenectomy, appendectomy, omentectomy, or hysterectomy. Moreover, of the 49 patients who had tumors that were unilateral and confined to the ovary at the time of surgery in the radical surgery group, no tumor was identified on the opposite ovary following bilateral salpingooophorectomy.

3. Survival analysis

The median follow-up duration was 104 months (range, 8.0 to 231.6 months). The Kaplan-Meier curves and the log rank test showed no difference in either recurrence-free survival (p=0.792) or disease-specific survival (p=0.706) between patients who underwent fertility-sparing surgery and radical surgery (Fig. 1). Five-year disease-specific survival was 91.3% for those who had fertility-sparing surgery, compared with 86.4% for patients who underwent radical surgery. In addition, 10-year disease-specific survival was 81.4% for those who had fertility-sparing surgery, compared with 81.8% for patients who underwent radical surgery.

Of the 90 patients with tumors that appeared to be grossly confined to the ovaries upon surgical exploration, 15 (16.7%) eventually experienced disease recurrence, including six of the 35 patients (17.1%) who underwent fertility-sparing surgery and nine of the 55 patients (16.4%) who underwent radical surgery (p=0.923). Contralateral adnexal recurrence was suspected in just one of the patients with recurrence in the fertility-sparing surgery group, based on imaging study findings. Only two of the 15 patients who experienced recurrence went on to live without the disease.

A subgroup analysis was performed with women below the age of 40; there were 32 patients in the fertility-sparing surgery group and 11 in the radical surgery group. Even when the analysis was confined to women less than 40 years old, Kaplan-Meier curves and the log rank test showed no difference in either recurrence-free survival (p=0.126) or disease-specific survival (p=0.377) between the two groups (Fig. 2).

Cox proportional hazards analysis was performed to adjust for the baseline characteristics (Table 3). Fertility-sparing surgery had no effect on either recurrence-free survival (HR, 1.20; 95% confidence interval [CI], 0.25 to 5.71) or disease-specific survival (HR, 0.88; 95% CI, 0.17 to 4.60). Stage was the most important prognostic factor for recurrence and survival in our cohort. This finding did not change when the analysis was confined to women younger than 40. The surgical procedure was not an independent prognostic factor for either recurrence-free survival (HR, 0.22; 95% CI, 0.04 to 1.24) or disease-specific survival (HR, 0.52; 95% CI, 0.09 to 3.11) in patients below the age of 40.

Discussion

This study highlights the safety of fertility-sparing surgery in cases of mucinous epithelial ovarian cancer when tumors appear to be grossly confined to the ovaries. We compared the oncologic outcomes of patients who underwent fertilitysparing and radical surgery using long-term follow-up data. In addition, the risk of upstaging is minimal in patients with early-stage mucinous ovarian cancer when no suspicious lesions on the peritoneum are found during careful intraoperative exploration.

Previous studies have reported the outcomes of fertilitysparing surgery in women with early-stage epithelial ovarian cancer [3-11]. The preservation of the female reproductive organ is one of the key issues for young women with epithelial ovarian cancer, and in particular for nulliparous women. However, the criteria for guaranteeing the safety of fertilitysparing surgery in early-stage ovarian cancer have not been identified thus far. Although the current guidelines recommend that fertility-sparing surgery may be considered in selected cases, it is not clear what these ‘selected cases’ are [12]. Most studies propose that fertility-sparing surgery can be performed on all young women with stage IA grade 1 ovarian cancer [20]. In many of the above-mentioned series, fertility-sparing surgery was also performed on invasive ovarian cancer patients with unfavorable grades, as well as on patients with disease not confined to one ovary [7,8,10,11,21]. Although the recurrence rate remains low even for these patients, the data has limitations due to the retrospective nature of this study and the small sample size.

Recent studies have demonstrated that epithelial ovarian cancer is not a single disease but is composed of a diverse group of tumors. Based on distinctive morphologic and molecular genetic features, a dualistic model that classifies various types of ovarian cancer into two groups (type I and type II) was proposed by Kurman and Shih [22]. Type I tumors are clinically indolent and usually present with low-grade carcinoma, including low-grade serous, low-grade endometrioid, and mucinous carcinoma. Mucinous carcinoma is indolent and has an excellent prognosis when identified at an early stage [23]. By contrast, advanced-stage mucinous ovarian cancer has a poor prognosis due to its resistance to platinum-based chemotherapy [24]. In particular, mucinous invasive ovarian cancer is a different disease entity and has distinct characteristics compared to highgrade serous carcinoma. Therefore, these favorable histologic subtypes should be distinguished from others.

In patients with mucinous ovarian cancer grossly confined to the ovaries, the risk of upstaging after surgical staging procedure has been reported to be minimal [16,17]. In addition, these histological subtypes are commonly found in younger women. As a result, fertility preservation is an important consideration in this disease subset. Of the 90 patients in our cohort with tumors grossly confined to the ovaries, only six cases were upstaged following surgical staging, and there were no cases of upstaging due to microscopic metastasis following omentectomy, appendectomy, or lymphadenectomy. This finding was in accordance to those of previous studies. Recently, a number of studies have reported that occult lymph node metastasis was not found in any patients with apparent early-stage mucinous epithelial ovarian cancer [16,17]. Cho et al. [16] reported that out of 85 patients with stage I mucinous epithelial ovarian cancers, only five were upstaged due to positive peritoneal cytology. Schmeler et al. [17] demonstrated that 13 out of 93 patients with mucinous tumors grossly confined to the ovary were upstaged based on additional biopsies at the time of surgery. Moreover, they reported no significant difference in survival between the group that underwent lymphadenectomy and the group that did not.

When considering previously described indolent aspects of early-stage mucinous adenocarcinoma, fertility-sparing surgery may be an acceptable option for younger women. However, concerns surrounding suboptimal surgery remain. One major concern with fertility-sparing surgery is the very small or microscopic foci involvement of the normal-looking uterus and contralateral ovary. Previous studies have shown that the risk of contralateral ovary involvement during surgery and recurrence in the contralateral residual ovary is low. Considering the 118 normal-appearing ovaries of epithelial ovarian cancer patients, Benjamin et al. [25] reported that only three patients (2.5%) had microscopic involvement in the contralateral ovary. Moreover, of the 209 patients treated conservatively, 14 patients (6.7%) experienced recurrence in the contralateral ovary [20]. Our results suggest more promising findings in mucinous histological subtypes. No cases of upstaging due to microscopic metastasis were identified in our cohort after hysterectomy. Of the patients with tumors confined to one ovary at surgical exploration in the radical surgery group, 49 underwent bilateral salpingo-oophorectomy, where no tumor was identified on the contralateral ovary. Moreover, of the 35 patients who underwent fertility-sparing surgery, only one experienced recurrence in the contralateral ovary. As a result, preservation of the uterus and contralateral ovary should be considered in patients with mucinous tumors confined grossly to one ovary.

Our study is limited by retrospective data collection, a long study period, small sample size, and possible referral bias. Moreover, varying surgical treatment types were used at the clinician’s discretion. Finally, it is unclear whether the lack of significant differences in recurrence and survival between patients who underwent fertility-sparing surgery and those who had radical surgery is attributable to our small sample size. However, only a small proportion of patients with invasive epithelial ovarian cancer underwent fertility-sparing surgery. In addition, no prospective study on the fertility-sparing issue in invasive epithelial ovarian cancer has been designed, and such a study is unlikely to perform a randomized controlled trial in the near future, due particularly to ethical problems and the anticipated difficulty in patient recruitment. Given these circumstances, our retrospective analysis opens up a discussion of the possibility that fertility-sparing surgery may be safe in mucinous histology.

Conclusion

In conclusion, our findings demonstrate that fertility-sparing surgery does not appear to have an adverse impact on the recurrence and survival rates in patients with early-stage mucinous ovarian carcinoma. This study has useful implications for physicians counseling patients who want to preserve their fertility. To validate our results, further largescale studies considering a sufficient number of patients with mucinous histology are required.

NOTES

Conflict of interest relevant to this article was not reported.

Acknowledgements

This work was supported by WCU (World Class University) program (R31-10056) through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology.

Fig. 1.

Recurrence-free survival (A) and disease-specific survival (B) in all patients with tumors grossly confined to the ovaries.

Fig. 2.

Recurrence-free survival (A) and disease-specific survival (B) in all patients under the age of 40 with tumors grossly confined to the ovaries.

Table 1.

Clinical and demographic characteristics

	Fertility-sparing surgery		p-value
	Yes (n=35)	No (n=55)	p-value
Age (yr)	28.6 ±10.1	50.3±14.0	< 0.001
Stage			0.496
IA	21 (60)	34 (61.8)
IB	0 (0)	1 (1.8)
IC	13 (37.1)	17 (30.9)
IIA	0 (0)	1 (1.8)
IIB	0 (0)	2 (3.6)
IIC	1 (2.9)	0 (0)
Year of diagnosis			0.067
1991-2000	15 (42.9)	18 (32.7)
2001-2005	13 (37.1)	13 (23.6)
2006-2010	7 (20.0)	24 (43.6)
Adjuvant chemotherapy			0.498
Yes	14 (40.0)	26 (47.3)
Conventional platinum-based	5 (14.3)	9 (16.4)
Taxane plus platinum	9 (25.7)	17 (30.9)
No	21 (60.0)	29 (52.7)
Grade			0.479
1	27 (77.1)	34 (61.8)
2	5 (14.3)	15 (27.3)
3	1 (2.9)	2 (3.6)
NA	2 (5.7)	4 (7.3)
Recurrence (%)			0.923
Yes	6 (17.1)	9 (16.4)
No	29 (82.9)	46 (83.6)

Values are presented as mean±standard deviation or number (%). NA, not available.

Table 2.

Procedures performed during surgical staging and cases of microscopic metastasis after surgery (cases of metastasis/cases of surgery performed)

	Fertility-sparing surgery
	Yes (n=35)	No (n=55)
Hysterectomy	0/0	0/55
Contralateral oophorectomy	0/0	0/49^a)
Peritoneal biopsy	1/7	3/20
Appendectomy	0/9	0/41
Omentectomy	0/12	0/45
Lymphadenectomy	0/2	0/26
Cytology	6/35	2/55

^a) Among patients who had tumors grossly confined to unilateral ovary at the time of surgery.

Table 3.

Cox proportional hazards model of factors associated with recurrence and disease-specific survival for primary mucinous cancer grossly confined to the ovaries

	Recurrence HR (95% CI)	Death HR (95% CI)
FSS
No	Reference	Reference
Yes	1.20 (0.25-5.71)	0.88 (0.17-4.60)
Age (yr)
< 40	Reference	Reference
≥ 40	2.08 (0.38-11.55)	1.04 (0.18-6.08)
Stage
IA or IB	Reference	Reference
IC	1.98 (0.46-8.61)	1.56 (0.35-7.03)
II	28.99 (2.72-308.91)	11.47 (1.16-113.17)
Year of diagnosis
1991-2000	Reference	Reference
2001-2005	0.53 (0.12-2.31)	0.24 (0.04-1.56)
2006-2010	0.14 (0.01-1.33)	0.29 (0.04-2.17)
Adjuvant chemotherapy
No	Reference	Reference
Yes	2.24 (0.48-10.46)	1.86 (0.39-8.83)
Grade
1	Reference	Reference
2	1.35 (0.27-6.78)	1.40 (0.25-7.98)
3	3.09 (0.25-37.76)	9.26 (0.60-141.82)

HR, hazard ratio; CI, confidence interval; FSS, fertility-sparing surgery.

REFERENCES

1. Young RC, Decker DG, Wharton JT, Piver MS, Sindelar WF, Edwards BK, et al. Staging laparotomy in early ovarian cancer. JAMA. 1983;250:3072–6. Article PubMed
2. Heintz AP, Odicino F, Maisonneuve P, Quinn MA, Benedet JL, Creasman WT, et al. Carcinoma of the ovary. FIGO 26th Annual Report on the Results of Treatment in Gynecological Cancer. Int J Gynaecol Obstet. 2006;95 Suppl 1:S161–92.
3. Borgfeldt C, Iosif C, Masback A. Fertility-sparing surgery and outcome in fertile women with ovarian borderline tumors and epithelial invasive ovarian cancer. Eur J Obstet Gynecol Reprod Biol. 2007;134:110–4. Article PubMed
4. Fruscio R, Corso S, Ceppi L, Garavaglia D, Garbi A, Floriani I, et al. Conservative management of early-stage epithelial ovarian cancer: results of a large retrospective series. Ann Oncol. 2013;24:138–44. Article PubMed
5. Kajiyama H, Shibata K, Mizuno M, Nawa A, Mizuno K, Matsuzawa K, et al. Fertility-sparing surgery in young women with mucinous adenocarcinoma of the ovary. Gynecol Oncol. 2011;122:334–8. Article PubMed
6. Kwon YS, Hahn HS, Kim TJ, Lee IH, Lim KT, Lee KH, et al. Fertility preservation in patients with early epithelial ovarian cancer. J Gynecol Oncol. 2009;20:44–7. Article PubMed PMC
7. Morice P, Leblanc E, Rey A, Baron M, Querleu D, Blanchot J, et al. Conservative treatment in epithelial ovarian cancer: results of a multicentre study of the GCCLCC (Groupe des Chirurgiens de Centre de Lutte Contre le Cancer) and SFOG (Societe Francaise d'Oncologie Gynecologique). Hum Reprod. 2005;20:1379–85. Article PubMed
8. Park JY, Kim DY, Suh DS, Kim JH, Kim YM, Kim YT, et al. Outcomes of fertility-sparing surgery for invasive epithelial ovarian cancer: oncologic safety and reproductive outcomes. Gynecol Oncol. 2008;110:345–53. Article PubMed
9. Satoh T, Hatae M, Watanabe Y, Yaegashi N, Ishiko O, Kodama S, et al. Outcomes of fertility-sparing surgery for stage I epithelial ovarian cancer: a proposal for patient selection. J Clin Oncol. 2010;28:1727–32. Article PubMed
10. Schilder JM, Thompson AM, DePriest PD, Ueland FR, Cibull ML, Kryscio RJ, et al. Outcome of reproductive age women with stage IA or IC invasive epithelial ovarian cancer treated with fertility-sparing therapy. Gynecol Oncol. 2002;87:1–7. Article PubMed
11. Zanetta G, Chiari S, Rota S, Bratina G, Maneo A, Torri V, et al. Conservative surgery for stage I ovarian carcinoma in women of childbearing age. Br J Obstet Gynaecol. 1997;104:1030–5. Article PubMed
12. National Comprehensive Cancer Center. Ovarian cancer clinical practice guidelines in oncology (v.I.2010) [Internet]. Fort Washington: National Comprehensive Cancer Network; 2010. [cited 2013 Feb 4]. Available from: http://www.nccn.org
13. McGuire V, Jesser CA, Whittemore AS. Survival among U.S. women with invasive epithelial ovarian cancer. Gynecol Oncol. 2002;84:399–403. Article PubMed
14. Hess V, A'Hern R, Nasiri N, King DM, Blake PR, Barton DP, et al. Mucinous epithelial ovarian cancer: a separate entity requiring specific treatment. J Clin Oncol. 2004;22:1040–4. Article PubMed
15. Mizuno M, Kikkawa F, Shibata K, Kajiyama H, Suzuki T, Ino K, et al. Long-term prognosis of stage I ovarian carcinoma. Prognostic importance of intraoperative rupture. Oncology. 2003;65:29–36. Article
16. Cho YH, Kim DY, Kim JH, Kim YM, Kim KR, Kim YT, et al. Is complete surgical staging necessary in patients with stage I mucinous epithelial ovarian tumors? Gynecol Oncol. 2006;103:878–82. Article PubMed
17. Schmeler KM, Tao X, Frumovitz M, Deavers MT, Sun CC, Sood AK, et al. Prevalence of lymph node metastasis in primary mucinous carcinoma of the ovary. Obstet Gynecol. 2010;116(2 Pt 1):269–73. Article PubMed PMC
18. Kajiyama H, Shibata K, Mizuno M, Umezu T, Suzuki S, Nawa A, et al. Long-term survival of young women receiving fertility-sparing surgery for ovarian cancer in comparison with those undergoing radical surgery. Br J Cancer. 2011;105:1288–94. Article PubMed PMC
19. Vergote I, De Brabanter J, Fyles A, Bertelsen K, Einhorn N, Sevelda P, et al. Prognostic importance of degree of differentiation and cyst rupture in stage I invasive epithelial ovarian carcinoma. Lancet. 2001;357:176–82. Article PubMed
20. Menczer J. Conservative fertility-sparing surgical treatment of invasive epithelial ovarian cancer: when is it acceptable? Isr Med Assoc J. 2013;15:116–20. PubMed
21. Raspagliesi F, Fontanelli R, Paladini D, di Re EM. Conservative surgery in high-risk epithelial ovarian carcinoma. J Am Coll Surg. 1997;185:457–60. Article PubMed
22. Kurman RJ, Shih Ie M. The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol. 2010;34:433–43. Article PubMed PMC
23. Harrison ML, Jameson C, Gore ME. Mucinous ovarian cancer. Int J Gynecol Cancer. 2008;18:209–14. Article PubMed
24. Karabuk E, Kose MF, Hizli D, Taskin S, Karadag B, Turan T, et al. Comparison of advanced stage mucinous epithelial ovarian cancer and serous epithelial ovarian cancer with regard to chemosensitivity and survival outcome: a matched case-control study. J Gynecol Oncol. 2013;24:160–6. Article PubMed PMC
25. Benjamin I, Morgan MA, Rubin SC. Occult bilateral involvement in stage I epithelial ovarian cancer. Gynecol Oncol. 1999;72:288–91. Article PubMed

Figure & Data

REFERENCES

Citations

Citations to this article as recorded by

Safety of fertility-sparing surgery in young women with stage I endometrioid epithelial and mucinous ovarian cancer: A population-based analysis
Jing Li, Huimin Qiao, Yunyun Liu, Chunxian Huang, Aoshuang Cheng, Zhongqiu Lin, Lijuan Wang, Huaiwu Lu
European Journal of Surgical Oncology.2024; 50(1): 107276. CrossRef
Mucinous ovarian carcinoma: A survey of practice in Australia and New Zealand
Niveditha Rajadevan, Ariane Flinkier, Hugo Saunders, Yeh Chen Lee, Clare Scott, Pearly Khaw, Prue Allan, Claire Davies, John Andrews, Michelle Wilson, Janine M Lombard, Michelle Harrison, Heshani Nesfield, Anna DeFazio, Tarek Meniawy, Kylie L Gorringe
Australian and New Zealand Journal of Obstetrics and Gynaecology.2024; 64(4): 319. CrossRef
Evaluation of Outcomes of Mucinous Ovarian Cancer Treated at a Tertiary Care Cancer Hospital in Pakistan
Syed Abdul Mannan Hamdani, Musa Azhar, Abdul Wahab, Tahira Yasmeen, Neelam Siddiqui
South Asian Journal of Cancer.2023; 12(01): 081. CrossRef
Update on Prognostic and Predictive Markers in Mucinous Ovarian Cancer
Fulvio Borella, Marco Mitidieri, Stefano Cosma, Chiara Benedetto, Luca Bertero, Stefano Fucina, Isabelle Ray-Coquard, Annalisa Carapezzi, Domenico Ferraioli
Cancers.2023; 15(4): 1172. CrossRef
Safety of fertility sparing management in invasive mucinous ovarian carcinoma
Soyoun Rachel Kim, Ainhoa Madariaga, Liat Hogen, Danielle Vicus, Allan Covens, Carlos Parra-Herran, Stephanie Lheureux, Lilian T. Gien
Gynecologic Oncology.2023; 174: 129. CrossRef
Rare Epithelial Ovarian Cancers: Low Grade Serous and Mucinous Carcinomas
Olivia Craig, Abhimanyu Nigam, Genevieve V. Dall, Kylie Gorringe
Cold Spring Harbor Perspectives in Medicine.2023; 13(9): a038190. CrossRef
Oncological and Reproductive Outcomes After Fertility-Sparing Surgery for Stage I Mucinous Ovarian Carcinoma
Wei Lin, Dongyan Cao, Xiaohua Shi, Yan You, Jiaxin Yang, Keng Shen
Frontiers in Oncology.2022;[Epub] CrossRef
Surgical treatment for clinical early-stage expansile and infiltrative mucinous ovarian cancer: can staging surgeries safely be omitted?
Marc D. Algera, Willemien J. van Driel, Koen K. van de Vijver, Roy F.P.M. Kruitwagen, Christianne A.R. Lok
Current Opinion in Oncology.2022; 34(5): 497. CrossRef
Primary mucinous ovarian cancer: options for surgery and chemotherapy
Katherine C Kurnit, Michael Frumovitz
International Journal of Gynecologic Cancer.2022; 32(11): 1455. CrossRef
Outcomes after Fertility-sparing Surgery for Women with Ovarian Cancer: A Systematic Review of the Literature
Alexandra Bercow, Roni Nitecki, Paula C. Brady, J.Alejandro Rauh-Hain
Journal of Minimally Invasive Gynecology.2021; 28(3): 527. CrossRef
Fertility preserving surgery in carcinoma ovary: a single institution experience
T. Subramanyeshwar Rao, KVVN Raju, Vikas Gupta, R. Rajagopalan Iyer
Indian Journal of Gynecologic Oncology.2021;[Epub] CrossRef
Fertility-Sparing Surgery in Gynecologic Cancer: A Systematic Review
Teska Schuurman, Sanne Zilver, Sanne Samuels, Winnie Schats, Frédéric Amant, Nienke van Trommel, Christianne Lok
Cancers.2021; 13(5): 1008. CrossRef
Fertility preservation in rare ovarian tumors
Anca Chelariu-Raicu, Lauren P Cobb, David M Gershenson
International Journal of Gynecologic Cancer.2021; 31(3): 432. CrossRef
Oncologic outcomes of uterine preservation for pre-menopausal patients with stage II epithelial ovarian carcinoma
Dimitrios Nasioudis, Lakeisha Mulugeta-Gordon, Erin McMinn, Maureen Byrne, Emily M Ko, Lori Cory, Ashley F Haggerty, Nawar A Latif
International Journal of Gynecologic Cancer.2021; 31(3): 480. CrossRef
Fertility-Sparing Surgery for Ovarian Cancer
Geoffroy Canlorbe, Nathalie Chabbert-Buffet, Catherine Uzan
Journal of Clinical Medicine.2021; 10(18): 4235. CrossRef
Emerging molecular alterations leading to histology-specific targeted therapies in ovarian cancer beyond PARP inhibitors
M. Bartoletti, L. Musacchio, G. Giannone, V. Tuninetti, A. Bergamini, G. Scambia, D. Lorusso, G. Valabrega, G. Mangili, F. Puglisi, S. Pignata
Cancer Treatment Reviews.2021; 101: 102298. CrossRef
Options for the Treatment of Mucinous Ovarian Carcinoma
Olivia Craig, Carolina Salazar, Kylie L. Gorringe
Current Treatment Options in Oncology.2021;[Epub] CrossRef
Fertility sparing surgery vs radical surgery for epithelial ovarian cancer: a meta-analysis of overall survival and disease-free survival
Denghua Liu, Jing Cai, Aiwei Gao, Zehua Wang, Liqiong Cai
BMC Cancer.2020;[Epub] CrossRef
Fertility‐sparing treatment for early‐stage epithelial ovarian cancer: Contemporary oncologic, reproductive and endocrinologic perspectives
Rachel S. Mandelbaum, Maximilian Klar, Tsuyoshi Takiuchi, Liat Bainvoll, Shinya Matsuzaki, Richard J. Paulson, Koji Matsuo
Journal of Obstetrics and Gynaecology Research.2020; 46(8): 1263. CrossRef
Impact of uterus‐preserving surgery on Stage I primary mucinous epithelial ovarian carcinoma: A multi‐institutional study with propensity score‐weighted analysis
Masato Yoshihara, Hiroaki Kajiyama, Satoshi Tamauchi, Shohei Iyoshi, Akira Yokoi, Shiro Suzuki, Michiyasu Kawai, Tetsuro Nagasaka, Kunihiko Takahashi, Shigeyuki Matsui, Fumitaka Kikkawa
International Journal of Gynecology & Obstetrics.2020; 150(2): 177. CrossRef
Tumeurs épithéliales de l’ovaire : préservation de la fertilité. Article rédigé sur la base de la recommandation nationale de bonnes pratiques cliniques en cancérologie intitulée « Conduites à tenir initiales devant des patientes atteintes d’un cancer épi
C. Uzan, B. Courbiere, N. Chabbert-Buffet
Gynécologie Obstétrique Fertilité & Sénologie .2019; 47(2): 180. CrossRef
Mucinous Ovarian Carcinoma
Dan L. Longo, Philippe Morice, Sebastien Gouy, Alexandra Leary
New England Journal of Medicine.2019; 380(13): 1256. CrossRef
Early stage mucinous ovarian cancer: A review
Erin K. Crane, Jubilee Brown
Gynecologic Oncology.2018; 149(3): 598. CrossRef
Results of Fertility-Sparing Surgery for Expansile and Infiltrative Mucinous Ovarian Cancers
Sebastien Gouy, Marine Saidani, Amandine Maulard, Slim Bach-Hamba, Enrica Bentivegna, Alexandra Leary, Patricia Pautier, Mojgan Devouassoux-Shisheboran, Catherine Genestie, Philippe Morice
The Oncologist.2018; 23(3): 324. CrossRef
Assisted reproductive techniques after fertility-sparing treatments in gynaecological cancers
Ignacio Zapardiel, Maria Cruz, Maria D. Diestro, Antonio Requena, Juan A. Garcia-Velasco
Human Reproduction Update.2016; 22(3): 281. CrossRef
Fertility-Sparing Surgery in Epithelial Ovarian Cancer
Enrica Bentivegna, Philippe Morice, Catherine Uzan, Sebastien Gouy
Future Oncology.2016; 12(3): 389. CrossRef
Mucinous ovarian cancer: A therapeutic review
Wen Xu, Jack Rush, Kirsty Rickett, Jermaine I.G. Coward
Critical Reviews in Oncology/Hematology.2016; 102: 26. CrossRef
Long-term results of fertility-sparing treatment compared with standard radical surgery for early-stage epithelial ovarian cancer
Robert Fruscio, Lorenzo Ceppi, Silvia Corso, Francesca Galli, Tiziana Dell'Anna, Federica Dell'Orto, Daniela Giuliani, Annalisa Garbi, Stefania Chiari, Costantino Mangioni, Rodolfo Milani, Irene Floriani, Nicoletta Colombo, Cristina Maria Bonazzi
British Journal of Cancer.2016; 115(6): 641. CrossRef
Fertility-sparing surgery in epithelial ovarian cancer: a systematic review of oncological issues
E. Bentivegna, S. Gouy, A. Maulard, P. Pautier, A. Leary, N. Colombo, P. Morice
Annals of Oncology.2016; 27(11): 1994. CrossRef

PubReader
ePub Link

Cite

CITE: export Copy Download Format; Close

Download Citation

Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.

Format:

RIS — For EndNote, ProCite, RefWorks, and most other reference management software
BibTeX — For JabRef, BibDesk, and other BibTeX-specific software

Include:

Citation for the content below
Citation and abstract for the content below

Safety of Fertility-Sparing Surgery in Primary Mucinous Carcinoma of the Ovary

Cancer Res Treat. 2015;47(2):290-305. Published online August 29, 2014

DOI: https://doi.org/10.4143/crt.2014.004

XML Download

Figure

Safety of Fertility-Sparing Surgery in Primary Mucinous Carcinoma of the Ovary

Fig. 1. Recurrence-free survival (A) and disease-specific survival (B) in all patients with tumors grossly confined to the ovaries.

Fig. 2. Recurrence-free survival (A) and disease-specific survival (B) in all patients under the age of 40 with tumors grossly confined to the ovaries.

Fig. 1.

Fig. 2.

Safety of Fertility-Sparing Surgery in Primary Mucinous Carcinoma of the Ovary

	Fertility-sparing surgery		p-value
	Yes (n=35)	No (n=55)	p-value
Age (yr)	28.6 ±10.1	50.3±14.0	< 0.001
Stage			0.496
IA	21 (60)	34 (61.8)
IB	0 (0)	1 (1.8)
IC	13 (37.1)	17 (30.9)
IIA	0 (0)	1 (1.8)
IIB	0 (0)	2 (3.6)
IIC	1 (2.9)	0 (0)
Year of diagnosis			0.067
1991-2000	15 (42.9)	18 (32.7)
2001-2005	13 (37.1)	13 (23.6)
2006-2010	7 (20.0)	24 (43.6)
Adjuvant chemotherapy			0.498
Yes	14 (40.0)	26 (47.3)
Conventional platinum-based	5 (14.3)	9 (16.4)
Taxane plus platinum	9 (25.7)	17 (30.9)
No	21 (60.0)	29 (52.7)
Grade			0.479
1	27 (77.1)	34 (61.8)
2	5 (14.3)	15 (27.3)
3	1 (2.9)	2 (3.6)
NA	2 (5.7)	4 (7.3)
Recurrence (%)			0.923
Yes	6 (17.1)	9 (16.4)
No	29 (82.9)	46 (83.6)

	Fertility-sparing surgery
	Yes (n=35)	No (n=55)
Hysterectomy	0/0	0/55
Contralateral oophorectomy	0/0	0/49^a)
Peritoneal biopsy	1/7	3/20
Appendectomy	0/9	0/41
Omentectomy	0/12	0/45
Lymphadenectomy	0/2	0/26
Cytology	6/35	2/55

	Recurrence HR (95% CI)	Death HR (95% CI)
FSS
No	Reference	Reference
Yes	1.20 (0.25-5.71)	0.88 (0.17-4.60)
Age (yr)
< 40	Reference	Reference
≥ 40	2.08 (0.38-11.55)	1.04 (0.18-6.08)
Stage
IA or IB	Reference	Reference
IC	1.98 (0.46-8.61)	1.56 (0.35-7.03)
II	28.99 (2.72-308.91)	11.47 (1.16-113.17)
Year of diagnosis
1991-2000	Reference	Reference
2001-2005	0.53 (0.12-2.31)	0.24 (0.04-1.56)
2006-2010	0.14 (0.01-1.33)	0.29 (0.04-2.17)
Adjuvant chemotherapy
No	Reference	Reference
Yes	2.24 (0.48-10.46)	1.86 (0.39-8.83)
Grade
1	Reference	Reference
2	1.35 (0.27-6.78)	1.40 (0.25-7.98)
3	3.09 (0.25-37.76)	9.26 (0.60-141.82)

Table 1. Clinical and demographic characteristics

Values are presented as mean±standard deviation or number (%). NA, not available.

Table 2. Procedures performed during surgical staging and cases of microscopic metastasis after surgery (cases of metastasis/cases of surgery performed)

Among patients who had tumors grossly confined to unilateral ovary at the time of surgery.

Table 3. Cox proportional hazards model of factors associated with recurrence and disease-specific survival for primary mucinous cancer grossly confined to the ovaries

HR, hazard ratio; CI, confidence interval; FSS, fertility-sparing surgery.