1. Arch Gynecol Obstet (2011) 284:731–735
DOI 10.1007/s00404-010-1713-9
123
GYNECOLOGIC ONCOLOGY
Ten years experience in the management of borderline ovarian
tumors at Tom Baker Cancer Centre
Nisrin AnWnan · Khalid Sait · Prafull Ghatage ·
Jill Nation · Pam Chu
Received: 22 July 2010 / Accepted: 28 September 2010 / Published online: 21 October 2010
© Springer-Verlag 2010
Abstract
Objective The aim of this study was to review the clinical
outcomes of patients with borderline ovarian tumors
(BOTs) at Tom Baker Cancer Centre (TBCC) and to assess
the value of surgical staging.
Methods This retrospective study included 138 patients
treated for BOTs at TBCC between January 1994 and
December 2005. Patients were divided into two groups:
group I with complete surgical staging (n = 89) and group
II with incomplete surgical staging (n = 49). This popula-
tion-based study identiWed patients using the Alberta Can-
cer Registry. Charts were reviewed by a single person. Data
extracted included demographic information and prognos-
tic factors such as age, histological type, laterality of the
cyst, presence of microinvasion, and the type of surgical
procedure. Data were extracted and entered into a study
database for analysis. Overall survival and overall recur-
rence-free survival of both groups were calculated using the
Kaplan–Meier method. Risk factors for recurrence were
analyzed using Cox regression analysis.
Results A total of 138 patients were enrolled, with a mean
age of 46 years. The median follow-up time was 37 months.
The most common histological type of BOT was the serous
type found in 70 (50.7%) patients. Microinvasion was
identiWed in four (2.9%) patients. Twelve patients were
found to have implants as result of the staging procedure;
two of them were invasive implants and both required
chemotherapy. Forty-three (31%) patients had conservative
surgery and 95 (68.8%) patients had non-conservative sur-
gery. Nine (6.5%) patients experienced recurrence: Wve
(5.6%) patients in group I versus four (8.2%) patients in
group II. The presence of microinvasion is the risk factor
for recurrence (P = 0.013).
Conclusions The indications for restaging surgery remain
controversial, as there was no diVerence in recurrence rates
observed between the study groups. However, surgical
staging is important for identifying invasive extraovarian
implants that need to be treated with chemotherapy. For
patients who have conservative surgery, close- and long-
term follow-up is required.
Keywords Borderline ovarian tumor · Recurrence ·
Survival
Introduction
Borderline ovarian tumors (BOTs) account for 10–20% of
ovarian epithelial tumors [1, 2], with the highest frequency
of these tumors occurring in women with a desire to pre-
serve fertility [1]. The need for complete surgical staging of
BOTs is controversial; the frequency of upstaging of the
tumor when a comprehensive staging procedure is per-
formed ranges from 12 to 47% [3, 4]. The overall risk of
recurrence after conservative surgery for a BOT ranges
from 7 to 30% [5] and recurrences typically show border-
line histology [6]. The rates of recurrence following both
conservative and complete surgical procedures for BOTs
have been reported to range between 9 and 11.6%. Disease-
free and overall survival rates for the two approaches did
N. AnWnan (&) · P. Ghatage · J. Nation · P. Chu
Department of Gynecology Oncology,
Tom Baker Cancer Centre, 3330 Hospital Drive NW,
Calgary, AB T2N 4N1, Canada
e-mail: Dr_nisreen2001@yahoo.com
K. Sait
Department of Obstetrics and Gynecology,
King Abdulaziz University Hospital,
Jeddah, Saudi Arabia

2. 732 Arch Gynecol Obstet (2011) 284:731–735
123
not signiWcantly diVer [7]. There has been no randomized
controlled trial that has evaluated the role of surgical stag-
ing of BOTs. The aim of this study was to review our clini-
cal experience with BOTs and to assess the value of
surgical staging.
Materials and methods
This is a retrospective study of women treated for BOTs
between January 1995 and December 2005 at Tom Baker
Cancer Centre (TBCC). This population-based study identi-
Wed all Southern Alberta patients with a BOT during this
time period. Most of the information related to the cases
was obtained using an electronic cancer registry. A chart
review was performed by a single person when the elec-
tronic data were incomplete. The data extracted included
demographic information and prognostic factors such as
age, histological type, laterality of the cyst, presence of
microinvasion, type of surgical procedure (conservative vs.
non-conservative surgery), and whether the patient had
undergone complete or incomplete surgical staging.
The histological criteria used for the diagnosis of BOTs
were according to Scully et al. [8] and included (1) stratiW-
cation of the epithelial lining, (2) the presence of micro-
scopic papillary projections, (3) nuclear atypia; and 4) the
absence of stromal invasion. At the time of diagnosis, gyne-
cological pathologists reviewed the pathology from all of
the patients at the gynecology tumor board.
We followed the FIGO 1987 guidelines [9] for com-
plete surgical staging that are used for ovarian malignan-
cies; they include careful inspection of all peritoneal
surfaces and peritoneal washing, infracolic omentectomy,
multiple peritoneal biopsies, and pelvic and para-aortic
lymphadenectomy [9]. Incomplete staging was deWned as
the lack of at least one of the above-mentioned proce-
dures.
Surgical treatment of a BOT consisted either of conser-
vative surgery (preserving the uterus and salvaging at least
one ovary) or non-conservative surgery (bilateral salpingo-
oophorectomy with or without hysterectomy).
Inclusion criteria
All patients diagnosed with a BOT were included. Patients
with invasive implants found on Wnal pathology were also
included.
Exclusion criteria
All patients diagnosed with invasive disease on Wnal
pathology or patients who developed other malignancies
during follow up were excluded.
Study groups
Patients with BOTs were divided into two groups: group I
complete surgical staging and group II incomplete surgical
staging.
Statistical analysis
Statistical analysis was performed using the statistical
package of social science version, 10 (SPSS). Qualitative
data were presented in the form of numbers and percent-
ages. Chi-square test was used for comparison of qualita-
tive data, Yates correction was used when appropriate.
Overall survival (OS) and recurrence-free survival (RFS) of
both groups were calculated using log-rank test. Cox
regression was used to identify the risk factor for recur-
rence.
Results
One hundred and thirty-eight patients who met the inclu-
sion criteria were included in this study. The median age of
the patients at the time of diagnosis was 46 years (range
16–80 years), and the median follow-up time was
37 months (range 39–154 months). The total numbers of
patients in group 1 and group 2 were 89 (64.4%), 49
(35.6%), respectively.
The most common histological type of tumor was the
serous type, which was found in 70 (50.7%) patients; 45
(32.6%) patients had mucinous type tumors. Microinvasion
was identiWed in four (2.9%) cases (Table 1). Only one
patient (0.7%) found to have micro papillary pattern.
Complete surgical staging was performed in 89 (64.4%)
patients (group I); 12 (13.5%) had conservative surgery,
while 77 of these patients (86.5%) had non-conservative
surgery (Table 2).
Table 1 Characteristics of 138 patients according to treatment group
Group I complete staging, Group II incomplete staging
Group I
(n = 89)
Group II
(n = 49)
SigniWcance
(P)
Age (year) 47.2 § 14.22 44.22 § 15.07 0.21
Histological type
Serous 52 (58.4%) 18 (36.7%) <0.001
Mucinous 19 (21.3%) 26 (53.1%)
Other 18 (20.2%) 5 (10.2%) 0.55
Microinvasion 3 (3.4%) 1 (2%)
Conservative surgery 12 (13.5%) 31 (63.2%) <0.001
Non-conservative
surgery
77 (86.5%) 18 (36.7%) <0.001
Frozen section 69 (77.5%) 24 (48.9%) 0.006

3. Arch Gynecol Obstet (2011) 284:731–735 733
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In group I, 63 (70.8%) patients had an initial full staging
operation, while 26 (29.2%) of them underwent a second
laparotomy for a restaging procedure (Table 3). Following
the initial staging procedure, tumors in 29 (46%) patients
were upstaged (Table 3), the numbers and percentages of
patients with Stages I, II, and III disease were 57 (64%), 13
(14.6%), and 19 (21.3%), respectively.
The total number of implants identiWed during the initial
staging procedure was 12 (8.6%); non-invasive implants
were found in 10 (15.9%) patients, consisting of 6 in the
peritoneum and 4 in the pelvic lymph nodes; 2 (3.2%)
patients were found to have separate invasive implants in
the peritoneum and in a pelvic lymph node. Both patients
received adjuvant chemotherapy in the form of paclitaxel
(Taxol) and carboplatinum for six cycles. Neither patient
experienced recurrence or died. Among patients who had
the restaging procedure (n = 26), upstaging of tumors was
found in 14 (53.8%) cases (Table 3). No invasive implants
were detected.
A total of nine (6.5%) patients experienced recurrence of
the disease for both groups (Table 4). Their average age
was 50 years (range 38–80 years), and the median time
until recurrence was 32 months (range 4–88 months). Five
(5.6%) patients in group I and four (8.2%) patients in group
II experienced recurrence. Table 5 shows details of the
patients who developed a recurrence. The pathology in
seven (77.7%) patients revealed a serous type of tumor.
All patients with a recurrence were treated with a second
radical surgery; three patients required adjuvant chemother-
apy in the form of carboplatinum and paclitaxel (Taxol).
The Wrst patient was 54-year-old woman treated initially
with total abdominal hysterectomy and bilateral salpingo-
oophorectomy (TAHBSO). Four years later, she developed
a pelvic recurrence, and she underwent a second laparot-
omy followed by chemotherapy for this invasive recur-
rence. The second patient was a 38-year-old woman
diagnosed with a stage Ia endometrioid BOT. She under-
went initial radical surgery, but 3 years later, she developed
a recurrence with invasive adenocarcinoma at the vaginal
vault. She was treated with a second debulking surgery fol-
lowed by six cycles of carboplatinum and paclitaxel
(Taxol).
The overall survival (OS) rate in groups I, II were
(100%) and (98.2%), respectively (P = 0.56; Fig. 1). No
statistically signiWcant diVerence in RFS rates existed
between group I (94.3%) and group II (91.8%) at this time
point (P = 0.53; Fig. 2).
A cox model for RFS showed the presence of microinva-
sion is the risk factor for recurrence P = 0.013,
Exp(B) = 57.7, CI (2.32–1398), other variables (age, site of
tumor, histopathology) were non-signiWcant for recurrence.
Discussion
The usual treatment for an apparently early stage BOT is
hysterectomy with bilateral salpingo-oophorectomy. How-
ever, conservative surgery is performed in young patients
with surgical staging if they wish to maintain their fertility
[10]. It is estimated that the rate of recurrence after conser-
vative surgery is between 0 and 20% and is especially
higher in patients who undergo cystectomy. In our series,
conservative surgery was performed in 43 (31%) patients,
with 38 (27.5%) patients treated with unilateral salpingo-
oophorectomy. Five patients who underwent conservative
surgery developed a recurrence, but only three patients had
bilateral adnexal masses; their initial surgery was unilateral
salpingo-oophorectomy and cystectomy of the contralateral
ovary. Only two patients had a cystectomy as conservative
surgery. Neither of them had staging procedures, and no
recurrences were reported in these patients.
Although conservative surgery can be performed in a
patient with a stage II, III, or IV BOT who has not com-
pleted childbearing, resection of extraovarian macroscopic
and microscopic disease with preservation of fertility is
important to achieve a good outcome [11, 12]. The need for
Table 2 Breakdown of operations performed for BOTs
BOTs borderline ovarian tumors, THBSO total hysterectomy and bilat-
eral salpingo-oophorectomy, USO unilateral salpingo-oophorectomy
Type of surgery Group I
(n = 89)
Group II
(n = 49)
SigniWcance
(P)
Non-conservative 77 (86.5%) 18 (36.7%) <0.001
Conservative 12 (13.5%) 31 (63.2%) <0.001
Cystectomy 0 2 (4.1%) 0.12
USO, cystectomy 0 3 (6.1%) 0.042
USO 12 (13.5%) 26 (53.1%) <0.001
Table 3 Upstaging after initial staging and restaging procedures and
presence of invasive implants
P = 0.60
Type of surgery Patient no. Upstaging Presence of
invasive implants
Initial full staging 63 (70.8%) 29 (46%) 2 (3.2%)
Restaging 26 (29.2%) 14 (53.8%) 0
Table 4 Recurrence in groups I and II according to the type of surgery
Group I
(n = 89)
Group I
(n = 49)
SigniWcance
(P)
Complete 3 (3.3%) 1 (2%) 0.55
Conservative 2 (2.2%) 3 (6.1%) 0.23

4. 734 Arch Gynecol Obstet (2011) 284:731–735
123
complete surgical staging is controversial [10, 13–15],
especially in the absence of gross extraovarian disease, as
no signiWcant diVerences in outcome measures of recur-
rence and mortality between staged and unstaged patients
have been observed [4, 16–18]. In our study, staging did
not inXuence overall rates of recurrence and survival.
Restaging of patients who are referred after a diagnosis
of BOT may not change their overall prognosis, especially
if they have undergone an initial comprehensive staging
procedure with an upstaging rate between 12 and 47% [3,
4]. In 26 (18.8%) patients who underwent a second surgery
for restaging, the rate of upstaging was 53.8%.
Stromal microinvasion with ovarian BOTs usually asso-
ciated with favorable outcome [19], certain patients with
microinvasion may be at higher risk for recurrence as inva-
sive disease [20].
The low prognostic utility of lymph node sampling was
illustrated in a meta-analysis of 97 studies that included
more than 4,000 patients with BOTs. The authors reported
98% survival in women with lymph node involvement (the
incidence of pelvic lymph node involvement was 1.7%)
[21]. We report Wve (3.6%) patients with pelvic lymph node
involvement. One patient received chemotherapy for an
invasive implant. None of the patients developed a recur-
rence or died.
Our policy at TBCC for the management of BOTs is as
follows: if the patient is referred for an ovarian mass and
frozen section shows a BOT, oophorectomy and a full stag-
ing procedure are usually performed if the patient wants to
preserve her fertility. However, if she has completed her
family, then complete surgery with a staging procedure will
Table 5 Details of patients who developed a recurrence
TAH total abdominal hysterectomy, USO unilateral salpingo-oophorectomy, TAHBSO total abdominal hysterectomy and bilateral salpingo-
oophorectomy, BSO bilateral salpingo-oophorectomy
a
Previous hysterectomy
b
Presence of microinvasion
Age (years) Initial surgery Formal staging Pathology Treatment for recurrence
38 USO No Serous TAH, USO
45 USO Yes Serous TAH, USO
54 TAHBSO Yes Serous Debulking + chemotherapy
80 BSO No Mucinous Debulking
30 USO No Serous Debulking + chemotherapy
36 USO, cystectomya
Yes Serous Debulking
53 USO No Serous Debulking
41 USO Yes Serous Debulking
38 TAH, USO Yes Endometrioidb
Debulking + chemotherapy
Fig. 1 Kaplan–Meier survival curves showing overall survival of pa-
tients with borderline ovarian tumors who underwent complete staging
(group I) versus incomplete staging (group II) (P = 0.56)
Log Rank test P= 0.56
Duration of survival (months)
96847260483624120
CumSurvival
1.00
.99
.98
.97
.96
.95
.94
.93
GROUPS
2
1
Fig. 2 Kaplan–Meier survival curves showing overall recurrence-free
survival of patients with borderline ovarian tumors who underwent
complete staging (group I) versus incomplete staging (group II)
(P = 0.53)
Log Rank test P=0.53
Duration of free recurrance
96847260483624120
CumSurvival
1.00
.99
.98
.97
.96
.95
.94
.93
.92
.91
.90
GROUP
2
1

5. Arch Gynecol Obstet (2011) 284:731–735 735
123
be carried out. In a patient who is referred to us with a diag-
nosis of BOT after conservative surgery, close follow-up is
needed if she wishes to preserve her fertility. Otherwise,
she will be counseled to undergo total hysterectomy and a
staging procedure. Chemotherapy is considered if the Wnal
pathology shows invasive implants.
In conclusion, the indications for restaging surgery
remain controversial, as no diVerence in recurrence rates
was observed between the two study groups. However, sur-
gical staging is important for identifying invasive extrao-
varian implants that can adversely aVect the prognosis. For
patients who have not had conservative surgery or staging,
close- and long-term follow-up is needed. A randomized
controlled trial that addresses the need for surgical staging
of BOTs is warranted.
ConXict of interest None.
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