Epithelial ovarian carcinoma of low malignant potential
E. DARAI* MD, J. TEBOUL* MD, F. WALKER**, J.-L. BENIFLA* MD,E. MENEUX*
MD, J.-N. GUGLIELMINA* MD, G. PENNEHOUAT* MD,C. RENOLLEAU* MD, E. SEBBAN* MD et P.
In 1929, Taylor  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)  included in the classification system the ovarian carcinoma of low malignant
potential. The World Health Organisation (Who) followed with a similar categorization in
1973 .Approximatively 15 % of epithelial ovarian malignancies are tumors of low
malignant potential (or borderline) . Compared to frankly malignant carcinoma of the
ovary , 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
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 , pain , bleeding ,
sonographic examination , during laparoscopy . 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
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 .
Lim Tan  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  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 , 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  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  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
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.
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E. DARAI* MD, J. TEBOUL* MD, F. WALKER**, J.-L. BENIFLA* MD,E. MENEUX* MD, J.-N.
GUGLIELMINA* MD, G. PENNEHOUAT* MD,C. RENOLLEAU* MD, E. SEBBAN* MD et P. MADELENAT* PhD
University Hospital Bichat Claude Bernard - Paris - France.
* Department of Gynaecology- P. MADELENAT, PhD.
** Department of Pathology - F. POTET, PhD.
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