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1996 > Gynécologie > Cancer de l'ovaire  Telecharger le PDF

Epithelial ovarian carcinoma of low malignant potential

E. Darai , E Meneux , C Renolleau , É. Sebban , J. Benifla , P. Madelenat , P Morice , J Teboul , G Pennehouat et J. Gugliemina

In 1929, Taylor [1] reported a series of patients with ovarian epithelial tumors that appeared malignant but behaved in a relatively benign manner.This concept was not immediately accepted. In 1971, the International Federation of Gynaecology and Obstetrics (Figo) [2] included in the classification system the ovarian carcinoma of low malignant potential. The World Health Organisation (Who) followed with a similar categorization in 1973 [3].Approximatively 15 % of epithelial ovarian malignancies are tumors of low malignant potential (or borderline) [4]. Compared to frankly malignant carcinoma of the ovary [5], patients have been reported to be younger, to exhibit a relatively benign clinical course. A higher percentage of borderline are discovered as stage I disease.

This report retrospectively reviews the treatment and outcome of 34 patients with epithelial ovarian carcinoma of low malignant potential with particular emphasis on 25 patients who had a laparoscopic management.

Materials and Methods

From January 1986 up to December 1994, 34 patients with 40 epithelial ovarian carcinomas of low malignancy were diagnosed and treated in the gynecologic service BICHAT-CLAUDE BERNARD Hospital Paris - France.

The histologic criteria include stratification of the epithelial lining of the papillae with formation of microscopic papillary projections or tufts arising from the epithelial lining of the papillae, nuclear atypicality, mitotic activity, intracystic clusters of free floating cells, and the absence of stromal invasion.

Microscopic sections from each of the 40 tumors were blindly reviewed by one of the authors to ensure accuracy of diagnosis. Follow-up on each patient was determined from hospital records, contact with referming physicians, and letters to patients. On the basis of the records, all patients had their original Figo stage confirmed. Particular emphasis was placed on whether there were sonographic examinations, tumors markers and laparoscopic treatment.


Thirty four patients were identified who met the strict histologic criteria for tumors of low malignant potential. The mean age of the patients at diagnosis was 46,4 with a range of 22 - 72 years. The largest group (11 patients) were in their forties (Fig 1), eight patients(18,6 %) were nulligravida, 2 (5,8 %) were pregnant at diagnosis and 10 (29,4 %) were menopausal. Twenty six patients (76,5 %) had never used oral contraceptive pill and ten (29,4 %) had previous ovarian surgery.

The patients reported the presence of asymptomatic mass [12], pain [8], bleeding [1], sonographic examination [8], during laparoscopy [5]. The symptomatology was not available in one case.Table 1 shows the distribution of 29 patients with 31 tumors according to sonographic caracteristics. Three of 7 patients with unilocular anechogene had vegetations at sonographic control.

Nineteen patients (55,8 %) had pretreatment serum CA 125 determinations, seventeen (50 %) pretreatment serum CA 199 and nineteen (55,8 %) pretreatment ACE. The abnormal markers levels were 7/19 (4 serous tumors, 3 mucinous tumors), 4/17 (one serous tumor,3 mucinous tumors) and 0/19 respectively. Twenty patients (58,8 %) had serous tumors and the remaining 14 (41,2 %) had mucinous tumors. Six of the twenty serous lesions were bilateral. Table 2 shows the distribution of patients in relation with histologic diagnosis and stage of disease.

The mean size of the mucinous tumors was larger than that of the serous tumors ; 117 mm (range 20 - 350) in the mucinous versus 93 mm (range 15 - 250) in the serous.Surgical management was reviewed. Nine patients (26,4 %) had first laparotomic management in 8 cases for clinical presomption of frankly ovarian carcinoma and in one case for size mass of 350 mm. Seven patients had hysterectomy and bilateral salpingo-oophorectomy, one patient had unilateral salpingo-oophorectomy and another one had hysterectomy and unilateral cystectomy. Twenty five patients (73,6 %) had first laparoscopic management. Seven patients had laparoconversion, in five cases for failure of the procedure (three bowel adhesions, two hemorages) and in 2 cases for presomption of frankly ovarian malignant carcinoma. Among these 7 patients, two had hysterectomy and bilateral salpingo-oophorectomy, and 5 women had conservative management (3 unilateral salpingo-oophorectomy and 2 cystectomies). One patient had an ovarian biopsy with subsequent laparotomic hysterectomy with bilateral salpingo-oophorectomy and omuntectomy three days later.

Seventeen patients had exclusive laparoscopic management, six patients had cystectomy, seven patients had unilateral salpingo-oophorectomy, and other four bilateral salpingo-oophorectomy of which one with laparoscopic hysterectomy.

Peritoneal cytology was performed in 16 cases and was positive in one case. This patient had a radical treatment without recurrence. Two recurrences occurred in the group of negative cytology.

Per operative rupture of the cyst occurred in 14 cases (41,1 %) 13 during laparoscopy and one during laparotomy. Two recurrences occurred in the per operative rupture cyst group. Table 3 shows the subsequent treatment and outcome of the 34 patients.Four patients had developped recurrent disease, two on ipsilateral ovary after cystectomy and two controlateral, one after cystectomy and the second after salpingo-oophorectomy.

Ten patients had laparoscopic second look. All were negative. The mean follow-up was 44 months (range12 - 96). Thirty three patients were alive without disease and another one died of intercurrent disease.


In the present study, 91 % of the tumors of low malignant potential were diagnosed as stage I disease and ten patients were under forty years. At sonographic examination 67.7 % of tumor appear as multilocular, seven (22.5 %) are unilocular smooth sonolucent. 35 % of the patients had preoperative abnormal marker level CA 19.9 or CA 125 but ACE was always normal.

The relative frequency of low malignant potential tumors in young women in the reproductive age group and the excellent prognosis associated with stage I tumors have led to more conservative surgery approaches despite a reported 5 - 10 % frequency of microscopic tumor in a grossly normal appearing controlateral ovary [6].

Lim Tan [7] reported an ipsilateral persistence or recurrence rate of 8 % per ovary and 100 % survival in a group of 35 patients with serous borderline tumors subjected to cystectomy alone. Julian and Woodruff [8] reported 100 % survival rate in 15 patients with stage I borderline serous ovarian tumors who underwent unilateral adnexal removal but did not report the local reccurence rate. As Tazelaar [9], we report in stage I borderline tumors, three recurrences (37.5 %) after cystectomies (two in ipsi lateral ovary and one in controlateral ovary) and only one recurrence (9 %) after unilateral salpingo-oophorectomy. As there appears to be a higher local recurrence rate following cystectomy alone. As salvage therapy appears to be effective, but is critically dependent upon close, intense follow-up to allow early discovery of a recurrence.

As Lim Tan [7] our study suggests that cystectomy alone is insuffisant therapy in the multilocular cysts. In fact, all of the recurrences occurred in this group. The laparoscopic management of borderline tumors is associated with higher rate of peroperatively rupture. In the study two recurrences occurred in the group of rupture cysts. Katzenstein [10] suggests that the rupture of the tumor did not affect survival. The apparent high curability of recurrent disease (the patients have remained free of disease after additional treatment) and the observation that total abdominal hysterectomy and bilateral salpingo-oophorectomy will not always be curative suggest that conservative therapy is justifiable especially in young women.

In spite of three recurrences after laparoscopic management of borderline tumors, it appears that the rate is similar to the laparotomic conservative surgery and could be proposed in the young women.


[1] Taylor H.C. : Malignant and semimalignant tumors of the ovary. Surg. Gynecol. Obstet. 1929 ; 48 : 702.

[2] International Federation Of Gynaecology and Obstetrics : Classification and staging of malignant tumors in the female pelvis. Acta Obstet. Gynecol. Scand. 1971 ; 50 : 1.

[3] Serov S.F. ; Scully R.E. ; Sobin L.H. : International histological classification of tumors,no. 9. Histological typing of ovarian tumors. Geneva. World Health Organization, 1973.

[4] Barnhill D. ; Heller P. ; Brzozowski P. ; Advani H. ; Gallup D. ; Park R. : Epithelial ovarian carcinoma of low malignant potential. Obstet. Gynecol. 1985 ; 65 : 53 - 58.

[5] Fort MG., Pierce VK., Saigo PE., Hoskins WJ., Lewis JL. : Evidence for the efficacy of adjuvant therapy in epithelial ovarian tumors of low malignant potential. Gynecol. Oncol. 1989 ; 32 : 269 - 272.

[6] Williams T.J. ; Dockerty M.B. : Status of the contralateral ovary in encapsulated low grade malignant tumors of the ovary. Surg. Gynecol. Obstet. 1976 ; 143 : 763.

[7] Lim Tan S. K. ; Cajogas H.E. ; Scully R.E. : Ovarian cystectomy for serous borderline tumors : a follow up study of 35 cases. Obstet. Gynecol. 1988 ; 72 : 775 - 780.

[8] Julian C.G. ; Woodruff J.D. : The biologic behavior of low grade papillary serous carcinoma of the ovary. Obstet. Gynecol. 1972 ; 40 : 860.

[9] Tazelaar H.D. ; Bostwick D.G. ; Ballon S.C. et al. : Conservative treatment of borderline ovarian tumors. Obstet. Gynecol. 1985 ; 66 : 417.

[10] Katzenstein A.A. ; Mazur M.T. ; Morgan T.E. et al. : Proliferative serous tumors of the ovary. Histologic features and prognosis. Am. J. Surg. Pathol. 1978 ; 2 : 339.

University Hospital Bichat Claude Bernard - Paris - France. Department of Gynaecology, Department of Pathology