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10.1245/ASO.2006.12.024
Annals of Surgical Oncology 13:565-571 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Recurrence After Cystectomy for Borderline Ovarian Tumors: Results of a French Multicenter Study

Christophe Poncelet, MD, PhD1,2, Raffaèle Fauvet, MD1, Joëlle Boccara, MD1 and Emile Daraï, MD, PhD1

1 Service de Gynécologie-Obstétrique, Hôpital Tenon, AP-HP, 4 Rue de la Chine, CancerEst, UFR Saint-Antoine, 75020 Paris VI, France
2 UFR SMBH Léonard De Vinci, Université Paris XIII, 93017 Bobigny Cedex, Paris, France

Correspondence: Address correspondence and reprint requests to: Emile Daraï, MD, PhD; E-mail: emile.darai{at}tnn.ap-hop-paris.fr.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Fertility-sparing surgery for borderline ovarian tumors (BOT) is feasible and effective and does not seem to have a negative effect on survival. Specific data on the effect of cystectomy, and notably on recurrence, are lacking.

Methods: This was a French retrospective multicenter study of 313 women with stage I BOT treated from 1990 to 2000 in 13 specialized gynecological units and 1 cancer center. Diagnosis and staging were based on International Federation of Gynecology and Obstetrics (1989) criteria. Surgery consisted of cystectomy, unilateral salpingo-oophorectomy (USO), or bilateral salpingo-oophorectomy (BSO).

Results: After cystectomy, persistent BOT and benign ovarian cysts on the operated ovary were observed in 15% and 65% of patients, respectively. Mean follow-up did not differ among patients receiving the three types of surgery. The recurrences after cystectomy, USO, and BSO treatment were 30.3%, 11%, and 1.7%, respectively (P < .0001). Recurrences were more frequent after cystectomy than after USO (P = .0001) and BSO (P = .0001) and when intraoperative cyst rupture occurred (P = .04).

Conclusions: These results suggest that cystectomy for BOT is associated with a high risk of intraoperative cyst rupture and of recurrence compared with USO or BSO.

Key Words: Borderline ovarian tumors • Recurrence • Cystectomy • Persistent tumor • Salpingo-oophorectomy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Accepted as a distinct diagnostic category by the International Federation of Gynecology and Obstetrics1 and the World Health Organization2 in the early 1970s, borderline ovarian tumors (BOTs) account for 10% to 20% of all ovarian epithelial tumors.3 Guidelines for surgical treatment of BOTs are similar to those for ovarian cancer and include peritoneal washing, hysterectomy with bilateral salpingo-oophorectomy (BSO), omentectomy, and multiple peritoneal biopsies.4,5

One third of BOTs are diagnosed before the age of 40 years and possibly warrant conservative fertility-sparing surgery.3,6–14 Tazelaar et al.15 were the first to report the use of salpingo-oophorectomy for BOTs, and several small studies subsequently confirmed the feasibility of this strategy.3,11,14,16–19 Recurrence rates after conservative treatment were as high as 30%, depending on the histological type and the form of conservative surgery, but overall survival did not seem to be negatively affected.8,16–22

In a preliminary series of 35 cases, Lim-Tan et al.16 noted ipsilateral persistence or recurrence rates of 8% after laparotomic cystectomy for serous borderline tumors. Morice et al.14 emphasized the lack of large series and long-term follow-up data (>5 years) on cystectomy for BOTs. The indications of cystectomy in this setting are therefore controversial because of the risk of relapse and potential progression to frankly invasive carcinoma.14,21 The aims of this retrospective multicenter study of BOTs were (1) to determine the persistence rate of ovarian lesions after initial cystectomy and (2) to compare the number of recurrences after cystectomy, unilateral salpingo-oophorectomy (USO), or BSO.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From January to December 2001, we conducted a retrospective multicenter study of 360 women treated for BOTs between 1990 and 2000 in 13 specialized gynecological units and 1 cancer center. Gynecological units were chosen according to oncological activity and the agreement of the person in charge of the department. Data were obtained from hospital records, physicians, and direct contact with the patients. All the charts were reviewed on site and in their entirety by R.F. and J.B. In accordance with the French laws, no ethical review board approval was necessary for this retrospective study.

The histological type was established by reviewing hematoxylin and eosin–stained slides, as recommended by International Federation of Gynecology and Obstetrics, by a trained pathologist masked to outcome.4 The following histological criteria were used to identify borderline tumors: (1) stratification of the epithelial lining of the papillae, with microscopic papillary projections or tufts arising from the epithelial lining of the papillae; (2) nuclear atypia; (3) mitotic activity; (4) intracystic clusters of free-floating cells; and (5) absence of stromal invasion. Margins of resection were assessed.

Surgical treatment was considered conservative when at least one ovary and the uterus were conserved. Conservative treatment consisted of unilateral cystectomy or USO. The initial operation was considered to be a complete staging operation when all peritoneal surfaces were carefully inspected and peritoneal washing, multiple random or oriented biopsies, and infracolonic omentectomy were performed. Systematic appendectomy was also a criterion for complete staging of mucinous borderline tumors. The initial operation was considered an incomplete staging operation in all other cases, independently of the radical or conservative nature of treatment.

Disease was staged as recommended by the International Federation of Gynecology and Obstetrics.4 Restaging operations were surgical procedures performed after initial incomplete staging, whatever the initial disease stage, when the interval between the initial and restaging operation was <6 months and adjuvant therapy was given. The restaging operation was either laparotomic orlaparoscopic, depending on the participating center.

We compared three groups of women according to the type of surgical treatment. Women who underwent cystectomy, USO, and BSO composed the cystectomy, USO, and BSO groups, respectively. Only women with stage I disease were included, and women who underwent both cystectomy and USO were excluded. Therefore, the study population consisted of 313 women (Fig. 1Go).


Figure 1
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  		FIG. 1. Distribution of the study population. After restaging operation, 33 women underwent a cystectomy, 100 women underwent an unilateral salpingo-oophorectomy (USO), and 180 women underwent a bilateral salpingo-oophorectomy (BSO).

 
The {chi}2 test and Student’s t-test were used to compare noncontinuous and continuous variables. P values <.05 were considered significant. Recurrence probabilities were calculated by using the product-limit method of Kaplan and Meier, and life curves were compared with the log-rank test.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Among 360 women with borderline tumors, 313 had stage I disease after initial or restaging surgery; the other 47 women were excluded from the study (Fig. 1Go). All restaging operations were performed within 3 months after the initial operation. Initial surgery consisted of cystectomy, USO, and BSO in 53, 96, and 164 women, respectively (Fig. 1Go).

Surgical Management of BOTs
Staging was complete in 1 (1.9%), 16 (16.7%), and 72 women (43.9%) in the cystectomy, USO, and BSO groups, respectively (Table 1Go). The rate of complete staging was lower in the cystectomy group than in the USO and BSO groups (P < .0001) and was also lower in the USO group than in the BSO group (P < .001). Among the 129 women with mucinous BOT, 69 women had a prior appendectomy, and 14 underwent this procedure during BOT surgical treatment.


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  		TABLE 1. Initial surgery for women with borderline ovarian tumors undergoing cystectomy, unilateral salpingo-oophorectomy (USO), and bilateral salpingo-oophorectomy (BSO)
 
The intraoperative cyst rupture rate was higher in the laparoscopic (58%) than in the laparotomic (41.5%) groups (P = .02). The intraoperative cyst rupture rate was higher in the cystectomy group than in the USO and BSO groups (P = .001). It was higher in the cystectomy group than in the USO group (P = .02) and higher in the USO group than in the BSO group (P = .02). The rate of intraoperative rupture and the occurrence of recurrence in the laparoscopic and laparotomic groups according to cystectomy, USO, and BSO are given in Table 2Go.


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  		TABLE 2. Intraoperative cyst rupture or recurrence occurrence according to the surgical route
 
Persistence of BOTs After Initial Cystectomy
In the cystectomy group, 33 women (62.3%) had no additional operations and had assumed stage I disease. Twenty women (37.7%) underwent restaging, of whom 16 (30.2%) underwent USO and 4 (7.5%) underwent BSO (Fig. 1Go). A residual ipsilateral ovarian lesion was diagnosed after restaging in 16 patients (80%): 3 women (15%) had a persistent BOT, and 13 women (65%) had benign ovarian cysts of the same pathologic type as the initial BOT.

Persistence of BOTs After Initial USO
In the USO group, 84 women (87.5%) had no additional operations and had assumed stage I disease. The other 12 women (12.5%) underwent restaging (always BSO; Fig. 1Go). After restaging, one woman (8.3%) was found to have a contralateral benign serous ovarian cyst of the same pathologic type as the initial BOT.

Epidemiological Characteristics of Women With BOTs After Restaging
The mean age was higher in the BSO group than in the cystectomy group (P < .0001) and the USO group (P < .0001; Table 3Go). The mean age was lower in the cystectomy group than in the USO group (P < .03). The mean parity was higher in the BSO group than in the cystectomy group (P < .0001) and the USO group (P < .0001). The mean parity was also higher in the USO group than in the cystectomy group (P < .03).


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  		TABLE 3. Characteristics of women with borderline ovarian tumors, including women who underwent a restaging operation after initial cystectomy, unilateral salpingo-oophorectomy (USO), or bilateral salpingo-oophorectomy (BSO)
 
A difference in the mean tumor size was observed between the groups (P = .01). Mean tumor size was larger in the BSO group than in the cystectomy group (P < .02). No difference in the pathological type of BOTs was found among the groups.

Recurrence After Surgery for BOTs
No difference in mean follow-up was found among the groups (Table 3Go). The median follow-up was 19 months (range, 6–243 months). The number of recurrences did not differ according to the histological type. No difference in the mean time to recurrence was observed among the groups (Table 3Go). There were no recurrences on the trocar incision site when a laparoscopic treatment was performed. No patient died of tumor progression.

Recurrences were more frequently observed in women with intraoperative cyst rupture (11 of 74; 14.9%) than in women without intraoperative cyst rupture (4 of 77; 5.2%; P = .04; Fig. 2Go). After restaging, 10 (30.3%) of the 33 women in the cystectomy group had a recurrence. The recurrence affected the ipsilateral ovary in nine cases and the contralateral ovary in one case. Eleven (11%) of the 100 women in the USO group and 3 (1.7%) of the 180 women in the BSO group had a recurrence. The recurrence rate was higher in the cystectomy group than in the USO and BSO groups (P < .0001). The recurrence rate was higher in the cystectomy group than in the USO group (P = .0008) and higher in the USO group than in the BSO group (P = .002; Fig. 3Go). No difference in recurrences was noted between women with serous and mucinous BOTs (P = .88).


Figure 2
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  		FIG. 2. Percentage of women without recurrence with (dotted line) and without (unbroken line) intraoperative cyst rupture (P < .04).

 

Figure 3
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  		FIG. 3. Percentage of women without recurrence according to the final surgical treatment (BSO, bilateral salpingo-oophorectomy; USO, unilateral salpingo-oophorectomy; or cystectomy).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this large retrospective study of women with BOTs, those who underwent cystectomy had a higher rate of intraoperative cyst rupture and more recurrences than those who underwent USO or BSO. Conservative surgery, particularly cystectomy, is controversial in women with BOTs because of the high risk of recurrence.14–16,23 In our series, 16.9% of women underwent cystectomy, and nearly one third of these women had a recurrence. Our results are in keeping with previous studies, in which recurrence rates after cystectomy ranged from 12% to 58%.6,13–16,24 The vast majority of recurrences affected the ipsilateral ovary, thus casting doubt on the legitimacy of this surgical option. One possible explanation for our relatively high rate of cystectomy is that tumors were often diagnosed as benign, and intraoperative histological analysis was rarely performed. Furthermore, these women tended to be younger and to have low parity. After final histological analysis, only 37.7% of women who underwent initial cystectomy had a restaging operation. One potential explanation is that BOTs are considered to behave in a benign fashion.25 Nevertheless, our findings should encourage surgeons to request frozen sections on tumors even in young women to perform adequate initial treatment. Moreover, comprehensive restaging is controversial because of its minor effect on clinical management and outcome.26–28 Trimble and Trimble29 recommended a case-by-case approach, taking into account the adequacy of initial surgery, the tumor subtype, and adjuvant therapy. In contrast to previous studies that showed little effect of restaging after initial USO or BSO treatment, our data raise the issue of restaging operations in women who undergo initial cystectomy.28,30 In a multivariate analysis, Trope et al.22 found that the main independent prognostic factor for disease-free and long-term survival was the International Federation of Gynecology and Obstetrics stage.

Little evidence has been provided for persistence or recurrence after cystectomy for BOTs. In a series of 35 patients with serous borderline tumors, Lim-Tan et al.16 reported a persistence rate of 8%. The rate of BOT persistence after cystectomy was 15% in our study, thus suggesting that cystectomy was inadequate. Moreover, we found a benign cystadenoma of the same histological type as the initial tumor in 65% of cases.

The main objective of conservative treatment for women with BOTs is to spare fertility without negatively affecting overall and disease-free survival.6,11,13–16 In our previous study,31 fertility rates did not differ between women who underwent USO and those who underwent cystectomy. In this study, we found that the number of recurrences was higher after cystectomy than after USO. This suggests that cystectomy should be considered only for women with one ovary or with bilateral tumors who wish to preserve their childbearing potential.

This is the largest published study of cystectomy for stage I BOTs. Cystectomy was associated with a higher rate of intraoperative cyst rupture than was USO or BSO. The rate of rupture was higher in the laparoscopic group compared with the laparotomic group. However, this difference was not related to the route of operation, but to the type of treatment. Indeed, a higher rate of cystectomy was performed by laparoscopy. Our rate of cyst rupture was higher than that observed by Havrilesky et al.32 (25%) for benign ovarian tumors. There are few data on intraoperative cyst rupture in the specific setting of borderline tumors. In our previous study, cyst rupture was observed in 14 (41%) of 34 cases, 13 of which involved laparoscopic procedures.24 The risks associated with intraoperative cyst rupture were well documented in women with frankly malignant tumors: rupture negatively affected both disease-free and overall survival.33 No equivalent data are available for intraoperative rupture of BOTs. Our high rate of intraoperative cyst rupture during laparoscopy may explain the higher number of recurrences than that observed by Lim-Tan et al.16 In our preliminary study, two of the four recurrences occurred in women who had intraoperative cyst rupture.24

This study was multicentric and retrospective and did not include systematic restaging. Moreover, the limited follow-up and the incomplete intraoperative data could potentially induce bias. However, the results suggest that intraoperative cyst rupture is associated with an increase in recurrence. This, together with the higher risk of recurrence after cystectomy than after USO, raises the issue of restaging operation including ipsilateral salpingo-oophorectomy, especially after cyst rupture.14,30,31

Conservative management of BOTs is an acceptable option for women who wish to preserve their fertility. However, our data show that cystectomy is associated with an increase of recurrence. Patients with BOTs who have been treated with ovarian cystectomy should be fully informed of the risk of relapse.


   ACKNOWLEDGMENTS
 
The authors thank the following individuals for supplying materials for this study: Prof. Philippe Descamps, Centre Hospitalier Universitaire Angers, Angers, France; Dr. Eric Fondrinier, Centre de Recherche et de Lutte Contre le Cancer Paul Papin Angers, Angers, France; Dr. Philippe Pillot, Centre Hospitalier Général Le Mans, Le Mans, France; Prof. Denis Querleu, Centre Hospitalier Universitaire Lille, Lille, France; Prof. Bernard Blanc, Centre Hospitalier Universitaire Marseille, Marseille, France; Prof. Hervé Fernandez, Centres Hospitaliers Universitaires Paris, Hôpital Béclère, Clamart, France; Prof. Patrick Madelenat, Hôpital Bichat, Paris, France; Prof. Charles Chapron, Hôpital Cochin, Paris, France; Prof. Jean Blondon and Prof. Yves Darbois, Hôpital de la Pitié-Salpétrière, Paris, France; Prof. Jacques Milliez, Hôpital Saint-Antoine, Paris, France; and Prof. Serge Uzan, Hôpital Tenon, Paris, France.

Received for publication December 29, 2004. Accepted for publication October 12, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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