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Hung-Yaw Chang*, Hao Lin, Chan-Chao Changchien, Shiuh-Young Chang

Department of Obstetrics and Gynecology, Chang Gung Memorial Hospital, Kaohsiung, Taiwan.

Objective: Ovarian tumors of borderline malignancy are not as aggressive as, and tend to occur in younger
patients than, their invasive counterparts. We retrospectively reviewed our experience to assess the safety of
conservative management of patients with limited disease.
Materials and Methods: The clinical and pathologic records of 57 patients with ovarian borderline malignant
tumors from 1988 to 1998 were identified from the database of the Chang Gung Memorial Hospital, Taiwan.
The International Federation of Gynecology and Obstetrics staging was retrospectively assigned, follow-up
information was obtained, and clinicopathologic correlations were made.
Results: Forty-three of the 57 patients (75.4%) were at stage Ia, six (10.5%) were at stage Ib, seven (12.3%)
were at stage Ic, and only one (1.8%) was at stage IIIc. Forty-three patients (75.4%) had mucinous cystadenoma
of borderline malignancy, while 14 (24.6%) had the serous type. Twenty-eight patients (49.1%) underwent
total abdominal hysterectomy and bilateral salpingo-oophorectomy or bilateral oophorectomy. Twenty-four
patients (42.1%) were treated with unilateral oophorectomy or unilateral salpingo-oophorectomy. Two patients
(3.5%) underwent debulking surgery. Five patients (8.8%) underwent enucleation of the ovarian tumor. Five
patients (8.8%) received chemotherapy after surgery. The median follow-up period was 44 months, and no
recurrence was found.
Conclusions: Conservative procedures appear to be warranted in young patients with clinically localized disease,
which might preserve fertility and decrease surgical morbidity. [Taiwanese J Obstet Gynecol 2004;43(1):16–19]

Key Words: conservative treatment, ovarian borderline malignancy, ovarian cancer

Introduction longer survival. In addition, the mean age of occurrence

of borderline tumors is nearly 10 years younger than
Ovarian tumors of borderline malignancy (low malignant that of invasive tumors [2]. In view of their biologically
potential) constitute approximately 10–15% of ovarian less aggressive behavior or low malignant potential,
carcinomas [1]. The majority of borderline ovarian conservative treatments have been attempted recently
tumors are of the serous or mucinous histologic type. in order to preserve fertility and avoid morbidity [3,4].
Compared with frankly invasive ovarian tumors, According to a survey of the Society of Gynecologic
borderline ovarian tumors behave more indolently and Oncologists (SGO), 97% of respondents advocated
are characterized by an earlier stage at presentation and surgical staging as surgical management for borderline
ovarian tumors [5]. Diversity exists in the surgical
management of borderline ovarian tumors between
conservative treatment and complete surgical staging.
*Correspondence to: Dr. Hung-Yaw Chang, Department of Obste- In an effort to provide more information about the
trics and Gynecology, Chang Gung Memorial Hospital, 123 appropriateness of conservative surgical management
Ta-Pei Road, Niaosung, Kaohsiung, Taiwan. in early ovarian borderline malignancies, we conducted
a retrospective, 10-year review of patients with borderline
Received: February 25, 2003
Revised: July 18, 2003 tumors to study the clinical characteristics of patients
Accepted: October 2, 2003 and their outcomes.

16 Taiwanese J Obstet Gynecol • March 2004 • Vol 43 • No 1

Management of Ovarian Borderline Malignancy

Materials and Methods Histopathologic type

All 57 patients had either serous or mucinous borderline
Fifty-seven patients with a diagnosis of borderline ovarian tumors of the ovary. Forty-three of the 57 patients
tumor who were seen at Chang Gung Memorial Hospital, (75.4%) had mucinous borderline ovarian tumors and
Taiwan, from 1988 to 1998, were identified using the 14 (24.6%) had serous borderline tumors. In seven
database of the institution and that of the Department patients, the tumors, which ruptured during surgery,
of Pathology. Detailed information regarding patient were staged Ic. Six patients’ bilateral ovarian borderline
age, blood type, initial symptoms, serum level of tumor tumors (three mucinous and three serous) were staged
markers, treatment, and follow-up were extracted from Ib. One patient had extra-ovarian disease with omental
the medical records. The diagnosis of borderline tumors metastasis, staged IIIc.
of the ovary was defined by published histologic criteria Fifty-three of the 57 patients had frozen sections
[6,7]. Based on the surgical notes and pathologic reports, taken. Diagnoses of borderline tumors by frozen and
tumor stage was defined using International Federation permanent pathology were consistent in 77.3% of cases.
of Gynecology and Obstetrics criteria [8]. Twelve patients were under-diagnosed to have benign
lesions by frozen section.
The mean overall diameter was 17.2 cm (range, 3–
Results 50 cm) for serous and 18.8 cm for mucinous tumors.
Patient characteristics
CA-125 values
The age at presentation ranged from 17 to 80 years,
Preoperative CA-125 values were available in 42 of
with 70.2% of patients being premenopausal. The mean
57 patients. CA-125 values were more than 35 IU/mL
age was similar in the serous (43.6 years) and mucinous
in 50% of mucinous tumors (mean, 88.0 IU/mL) as
groups (43.7 years). Patients had a mean age at
opposed to 75% of serous tumors (mean, 95.4 IU/mL).
menarche of 14.6 years (range, 12–18 years). The mean
number of gestations was 3.12 (range, 0–10), and 15
Adjuvant therapy
(26.3%) patients were nulligravida.
Five of the 57 patients received adjuvant systemic
All 57 patients had undergone pelvic surgery, and no
chemotherapy using a regimen of cisplatin, adriamycin
diagnosis of borderline tumor had been made before
and cyclophosphamide for 3 to 5 cycles. We performed
the operation. The mean and median follow-up times
physical examination, serum CA-125 test, and pelvic
were 44.9 and 44.0 months, respectively.
ultrasound examination during follow-up, but found
Presenting symptoms no recurrence in any of the 57 patients.
Low abdominal pain and a palpable pelvic mass led the
presenting symptoms in 41 patients (71.9%). Three pa-
tients (5.3%) presented with dysmenorrhea, six (10.5%) Discussion
with abdominal distension due to ascites or tumor
mass, and three (5.3%) with postmenopausal bleeding Borderline tumors of the ovary tend to occur at a
for 1 to 4 months. Two patients (3.5%) came for help younger age than their invasive counterparts [9]. In the
due to primary infertility, and one patient (1.8%) was current study, the mean age at diagnosis was 43.7 years,
diagnosed during pregnancy. with 70.2% of patients presenting prior to menopause,
and 42.1% of patients presenting prior to the age of 40
Surgical treatment
All 57 patients had their primary surgery without grossly
detected residual disease. The types of primary surgical Table 1. Primary surgical procedures for ovarian
procedures are shown in Table 1. Peritoneal washings borderline tumors
were performed in 12 patients: only two had atypical Stage
cells, while the other 10 were negative for malignant Ia Ib Ic IIIc
cells. Nine patients underwent omentectomy and all
were negative for tumors. Pelvic and para-aortic lymph Cystectomy 15 0 0 0
nodes were sampled in two patients, none of which Unilateral oophorectomy 21 0 3 0
Bilateral oophorectomy 11 1 0 0
showed tumor invasion. Most patients did not receive
Abdominal total hysterectomy +
complete staging work-up when the tumor was confined
bilateral oophorectomy 16 5 4 1
to the ovaries, and palpation of the pelvic lymph node (+ staging procedures)
and omentum was negative.

Taiwanese J Obstet Gynecol • March 2004 • Vol 43 • No 1 17

H.Y. Chang, et al

years. The mean age at diagnosis is less than in some Table 2. Incidence of recurrence after conservative
other series [10,11], with no difference in the age of and aggressive treatment and staging procedures
patients with mucinous or serous types of tumors.
Case Number Recurrence
Unlike previous studies [7,10,12], mucinous borderline
tumors (75.4%) were more common than serous Conservative treatment* 29 0
borderline tumors (24.6%) in our study. This may have Aggressive treatment† and
staging procedures‡ 28 0
been due to the early stage of the tumors in our series,
as serous borderline tumors are more often found in *Conservative treatment included cystectomy and unilateral oophorectomy
advanced disease [7,10,12]. with or without salpingectomy; †aggressive treatment included total abdominal
CA-125 was elevated in 57% (24/42) of patients. hysterectomy and bilateral oophorectomy with or without salpingectomy;

staging procedures included omentectomy, pelvic or para-aortic lymph node
Preoperatively, serous tumors of borderline malignancy sampling, and peritoneal biospy.
were associated with elevated CA-125 levels in 75% of
patients compared with 50% of patients with mucinous
tumors. A previous study also found that a higher
proportion of serous tumors was associated with those who underwent radical surgery and staging pro-
elevated CA-125 (75% serous, 30% mucinous) [13]. cedures (Table 2). Thus, our experience may indicate
Primary surgical treatment of borderline tumors that complete surgical staging with radical procedures
follows the guidelines for invasive carcinomas, and may not be necessary in patients with limited borderline
includes total abdominal hysterectomy, bilateral ovarian tumors without palpable pelvic lymph nodes or
salpingo-oophorectomy, omentectomy, and peritoneal omental tumors. The prognosis for patients with
washing. In advanced stages, tumor debulking is per- borderline ovarian tumors without nodal involvement is
formed, but lymph node sampling has not been part of excellent. Routine lymphadenectomy should not be
the standard procedure. In young fertile women with performed in patients with early stage disease [20,21].
early stage tumors, limited surgery with fertility pre- However, the follow-up period in our study is not long
servation has been performed. The surgical approach enough, and a longer duration of follow-up would be
now tends to be less aggressive for early stage tumors. required to make such a conclusion.
Borderline ovarian tumors behave more indolently The management of borderline ovarian tumors is
than frankly invasive ovarian tumors. Patients with still evolving. The main suggestion for patients with
borderline tumors are characterized by a younger age at borderline tumors is that they should not be managed
diagnosis, an earlier stage at presentation, and longer with an overly aggressive approach [23]. Continued ad-
survival [14–16]. In recent times, less radical surgery has vances in the application of molecular genetic analysis
been used more often in limited disease of borderline may help to identify tumors which are likely to contain
tumors not only because of the desire to preserve fertility, areas of malignant transformation from those likely
but also for the lower morbidity that can be achieved to have aggressive behavior. Individualized treatment
without radical operation and staging. In this series, no based on these analyses can minimize over-treatment of
recurrence was found with or without radical operation these diseases [24].
and staging. Recurrence was reported in 10–15% of
early stage borderline ovarian tumors in a previous
study [17,22]. However, a low recurrence rate (2.5%) References
for stage I borderline ovarian tumors has been reported
1. Barakat RR. Borderline tumors of the ovary. Obstet Gynecol
in another series [16]. Late recurrence may occur, but
Clin North Am 1994;21:93–105.
the interval between initial treatment and recurrence
2. Kennedy AW, Hart WR. Ovarian papillary serous tumors of
was 6 to 36 months in one series [19]. low malignant potential (serous borderline tumors). A long-
According to a survey among members of the SGO, term follow-up study, including patients with microinvasion,
97% of respondents advocated surgical staging [5]. In lymph node metastasis, and transformation to invasive serous
our study, complete staging procedures were performed carcinoma. Cancer 1996;78:278–86.
in two patients, 12 patients had washings, nine had 3. Kurman RJ, Trimble CL. The behavior of serous tumors of low
omentectomy, and two had pelvic para-aortic lymph malignant potential: are they ever malignant? Int J Gynecol
Pathol 1993;12:120–7.
node sampling. All of the previous staging surveys re-
4. Casey AC, Bell DA, Lage JM, Fuller AF, Nikrui N, Rice LW.
vealed negative findings. None of the other patients had Epithelial ovarian tumors of borderline malignancy: long-
staging work-up except for complete tumor excision. term follow-up. Gynecol Oncol 1993;50:316–22.
Survival and recurrence did not differ between those 5. Menzin AW, Gal D, Lovecchio JL. Contemporary surgical
patients who underwent conservative treatment and management of borderline ovarian tumors: a survey of the

18 Taiwanese J Obstet Gynecol • March 2004 • Vol 43 • No 1

Management of Ovarian Borderline Malignancy

Society of Gynecologic Oncologists. Gynecol Oncol 2000;78: 15. Kliman L, Rome RM, Fortune DW. Low malignant potential
7–9. tumors of the ovary: a study of 76 cases. Obstet Gynecol 1986;
6. Hart WR, Norris HJ. Borderline and malignant mucinous 68:338–44.
tumors of the ovary. Histologic criteria and clinical behavior. 16. Leake JF, Currie JL, Rosenshein NB, Woodruff JD. Long-term
Cancer 1973;31:1031–45. follow-up of serous ovarian tumors of low malignant potential.
7. Bostwick DG, Tazelaar HD, Ballon SC, Hendrickson MR, Gynecol Oncol 1992;47:150–8.
Kempson RL. Ovarian epithelial tumors of borderline 17. Morris RT, Gershenson DM, Silva EG, Follen M, Morris M,
malignancy. A clinical and pathologic study of 109 cases. Wharton JT. Outcome and reproductive function after
Cancer 1986;58:2052–65. conservative surgery for borderline ovarian tumors. Obstet
8. Changes in definitions of clinical staging for carcinoma of the Gynecol 2000;95:541–7.
cervix and ovary: International Federation of Gynecology and 18. Tazelaar HD, Bostwick DG, Ballon SC, Hendrickson MR,
Obstetrics. Am J Obstet Gynecol 1987;156:263–4. Kempson RL. Conservative treatment of borderline ovarian
9. Hopkins MP, Kumar NB, Morley GW. An assessment of tumors. Obstet Gynecol 1985;66:417–22.
pathologic features and treatment modalities in ovarian 19. Chow SN, Chen CD, Chen YP, Hsieh CY. Borderline malignant
tumors of low malignant potential. Obstet Gynecol 1987;70: tumors of the ovary: study of prognostic factors. J Formos Med
923–9. Assoc 1996;95:851–6.
10. Kaern J, Trope CG, Abeler VM. A retrospective study of 20. Camatte S, Morice P, Atallah D, et al. Lymph node disorders
370 borderline tumors of the ovary treated at the Norwegian and prognostic value of nodal involvement in patients treated
Radium Hospital from 1970 to 1982. A review of clinico- for a borderline ovarian tumor: an analysis of a series of 42
pathologic features and treatment modalities. Cancer 1993; lymphadenectomies. J Am Coll Surg 2002;195:332–8.
71:1810–20. 21. Lee KR, Scully RE. Mucinous tumors of the ovary: a clinico-
11. Kuoppala T, Heinola M, Aine R, Isola J, Heinonen PK. Serous pathologic study of 196 borderline tumors (of intestinal
and mucinous borderline tumors of the ovary: a clinico- type) and carcinomas, including an evaluation of 11 cases
pathologic and DNA-ploidy study of 102 cases. Int J Gynecol with ‘pseudomyxoma peritonei’. Am J Surg Pathol 2000;24:
Cancer 1996;6:302–8. 1447–64.
12. Russell P, Merkur H. Proliferating ovarian “epithelial” tumours: 22. Trope C, Kaern J. Management of borderline tumors of the
a clinico-pathological analysis of 144 cases. Aust NZ J Obstet ovary: state of the art. Semin Oncol 1998;25:372–80.
Gynaecol 1979;19:45–51. 23. Link CJ Jr, Reed E, Sarosy G, Kohn EC. Borderline ovarian
13. Gotlieb WH, Soriano D, Achiron R, et al. CA 125 measurement tumors. Am J Med 1996;101:217–25.
and ultrasonography in borderline tumors of the ovary. Am J 24. Zheng J, Wan M, Zweizig S, Velicescu M, Yu MC, Dubeau L.
Obstet Gynecol 2000;183:541–6. Histologically benign or low-grade malignant tumors adja-
14. Barnhill D, Heller P, Brzozowski P, Advani H, Gallup D, Park cent to high-grade ovarian carcinomas contain molecular
R. Epithelial ovarian carcinoma of low malignant potential. characteristics of high-grade carcinomas. Cancer Res 1993;
Obstet Gynecol 1985;65:53–9. 53:4138–42.

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