YGYNO-975853; No.

of pages: 5; 4C:
Gynecologic Oncology xxx (2015) xxx–xxx

Contents lists available at ScienceDirect

Gynecologic Oncology

journal homepage: www.elsevier.com/locate/ygyno

Outcomes of pediatric and adolescent girls with malignant ovarian germ

cell tumors
Jeong-Yeol Park ⁎, Dae-Yeon Kim, Dae-Shik Suh, Jong-Hyeok Kim, Yong-Man Kim,
Young-Tak Kim, Joo-Hyun Nam
Department of Obstetrics and Gynecology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Republic of Korea

H I G H L I G H T S

• Oncologic and reproductive outcomes were evaluated in 42 pediatric and young adolescent girls with malignant ovarian germ cell tumor.
• All patients received uniform treatment consisting of fertility-sparing, complete cytoreductive surgery with or without BEP chemotherapy.
• Survival outcomes were excellent and reproductive outcomes were favorable, regardless of histologic type or FIGO stage.

a r t i c l e i n f o a b s t r a c t

Article history: Objective. To analyze the oncologic and reproductive outcomes of pediatric and young adolescents with
Received 17 January 2015 malignant ovarian germ cell tumors (MOGCTs).
Accepted 25 March 2015 Methods. Pediatric or young adolescent girls aged 16 years or under with MOGCT were eligible for this study.
Available online xxxx Results. Forty-two pediatric or adolescent girls with MOGCT met the inclusion criteria. The median age was
12 years (range, 6–16 years) and 29 patients were premenarchal. The most common histologic type was imma-
Keywords:
ture teratoma, and 30 patients (54.3%) had stage I MOGCT. All patients underwent fertility-sparing surgery,
Malignant ovarian germ cell tumor
Children
which was defined as the preservation of at least one adnexa and the uterus. No patient had residual disease
Adolescent after surgery. Thirteen patients had tumor spillage, two patients had a positive peritoneal cytology, and two pa-
Ovary tients had lymph node metastasis. After surgery, 31 patients received adjuvant chemotherapy with bleomyocin,
etoposide, and cisplatin (BEP) (median, 4 cycles; range, 1–6 cycles). After a median follow-up time of 93 months
(range, 22–217 months), six patients had a recurrence of the disease, and one patient died. The 5-year disease-
free and overall survival rates were 85% and 97%, respectively. Among the surviving 41 patients, seven were
premenarchal, 30 had regular menstruation, and three had irregular menstruation. No patient had premature
ovarian failure.
Conclusion. All patients received uniform treatment consisting of fertility-sparing complete cytoreductive
surgery followed by BEP chemotherapy. Regardless of histologic type and FIGO stage, the oncologic outcomes
were excellent and the reproductive outcomes were favorable.
© 2015 Elsevier Inc. All rights reserved.

1. Introduction
Malignant ovarian germ cell tumors (MOGCTs) are rare malignant
tumors that account for about 5% of all ovarian malignancies [1–3],
and they usually occur in young females with a peak of incidence be-
tween 16 and 20 years of age [4]. MOGCTs consist of several different
histologic types, but all are derived from primordial germ cells of the
ovary. The most common histologic type is dysgerminoma followed
⁎ Corresponding author at: Department of Obstetrics and Gynecology, University of
Ulsan College of Medicine, Asan Medical Center, #388-1 Poongnap-2 dong, Songpa-gu,
Seoul, 138-736, Republic of Korea. Tel.: +82 2 3010 3646; fax: +82 2 476 7331.
E-mail address: catgut1-0@hanmail.net (J.-Y. Park).
by immature teratoma and yolk sac tumor, which together comprise
over 90% of all MOGCTs [5]. Choriocarcinoma, embryonal carcinoma,
and polyembryoma comprise the remaining 5–10% of MGOCTs [6].
Sometimes, a mixed type MOGCT is diagnosed, with dysterminoma
and yolk sac tumor being the most common combination [7].
Because MOGCT is a relatively rare malignancy, few clinical trials
have been done to guide standard treatment. Its incidence is only
about one-tenth of that of malignant testicular germ cell tumor. Treat-
ment modalities for MOGCT are mostly based on those of testicular can-
cer. The survival outcome of MOGCT was dramatically improved when
platinum-based chemotherapy for testicular cancer was applied to
treat patients with MOGCT [8,9]. Treatment outcomes are usually re-
ported only for older adolescent and young adult patients, because

http://dx.doi.org/10.1016/j.ygyno.2015.03.054
0090-8258/© 2015 Elsevier Inc. All rights reserved.

Please cite this article as: Park J-Y, et al, Outcomes of pediatric and adolescent girls with malignant ovarian germ cell tumors, Gynecol Oncol
(2015), http://dx.doi.org/10.1016/j.ygyno.2015.03.054
2 J.-Y. Park et al. / Gynecologic Oncology xxx (2015) xxx–xxx

MOGCTs are rare in children and young adolescents. MOGCTs account Table 1
for less than 1% of all childhood malignant tumors and only about 20% Demographic and clinicopathologic characteristics of patients (n = 42).

of MOGCTs are diagnosed in premenarchal girls [10]. Characteristics N %

The aim of this study was to analyze the oncologic and reproductive Age Median (range), years 12 (6–16)
outcomes of children and young adolescents with MOGCT. ≤10 years 13 31
N10 years 29 69
Histology Dysgerminoma 9 21.4
2. Materials and methods Immature teratoma 19 45.3
Grade 1 5
After obtaining the approval of the Institutional Review Board of Grade 2 9
Grade 3 5
Asan Medical Center (AMC, Seoul, Korea), we searched for patients
Yolk sac tumor 3 7.1
who met the following inclusion criteria: 1) age ≤ 16 years, 2) histolog- Mixed 11 26.2
ically proven MOGCT, 3) patients who were treated and followed-up at FIGO stage IA 21 50
AMC between 1996 and 2011. Demographic data were gathered from IB 1 2.4
the patients' medical records, including age, menarche, co-morbid IC 8 19
IIC 3 7.1
medical disease, and history of surgery; clinicopathologic data in- IIIA 3 7.1
cluding presenting symptoms, tumor markers, surgery, adjuvant IIIB 2 4.8
therapies, complications, histologic types, and grade and stage of IIIC 3 7.1
tumor; and follow-up data including recurrence, the pattern of re- IV 1 2.4
CA 125a Median (range), U/mL 49.7 (6.2–1700)
currence, treatment at recurrence, death, menstruation, menopause,
Not elevated 10 23.8
and pregnancy. A telephone interview was also performed to ascer- Elevated 16 38.1
tain the reproductive outcomes of patients. Histologic types of Not checked 16 38.1
MOGCT were classified according to the World Health Organization AFPb Median (range), ng/mL 10.6 (0.63–616,000)
(WHO) classification and the stage was determined according to Not elevated 19 45.3
Elevated 20 47.6
the revised version (2014) of the International Federation of Gyne- Not checked 3 7.1
cology and Obstetrics (FIGO) staging system [11–13]. The histologic b-hCGc Median (range), mIU/mL 1.0 (0.1–12,000)
grade of immature teratoma was determined according to the Norris Not elevated 24 57.1
classification [14]. Disease-free survival time was calculated as the Elevated 5 11.9
Not checked 13 31
time interval in months from the date of diagnosis to the date of
recurrence or censoring. Overall survival time was calculated as the FIGO, the International Federation of Obstetrics and Gynecology; CA 125, cancer antigen
125; AFP, alpha fetoprotein; b-hCG, beta-human chorionic gonadotropin.
time interval in months from the date of diagnosis to the date of a
Reference range: 0–35 U/mL.
death from the disease or the last follow-up. Survival curves were b
Reference range: 0–20 ng/mL.
calculated using the Kaplan–Meier method and the differences in c
Reference range: 0–3 mIU/mL.
survival rate were compared using log-rank test in SPSS software
(version 21.0; IBM, Armonk, NY). P b 0.05 was regarded as a statisti-
peritoneal cytology, two patients had a positive cytology. Two patients
cally significant difference.
had lymph node metastasis.
After surgery, 31 patients received adjuvant chemotherapy with
3. Results bleomyocin, etoposide, and cisplatin (BEP). The median number of che-
motherapy cycles was four (range, 1–6). In general, all patients exclud-
Between 1996 and 2011, 42 pediatric or adolescent girls with ing stage IA MOGCT received adjuvant chemotherapy. One patient with
MOGCTs met the inclusion criteria for this study. The demographic stage IV MGOCT due to malignant pleural effusion also underwnent
and clinicopathologic characteristics of patients are listed in Table 1. cytoreductive surgery followed by adjuvant chemotherapy. After a me-
The median age at diagnosis was 12 years (range, 6–16 years) and 29 dian follow-up time of 93 months (range, 22–217 months), six patients
patients were premenarchal. Thirty nine patients presented with a pal- had disease recurrence. All patients with recurrent disease received BEP
pable abdominal mass with or without abdominal pain, two patients chemotherapy with or without secondary surgery. Four patients
presented with torsion of the ovarian mass, and one patient presented showed complete response, one patient showed partial response, and
with rupture of the ovarian mass. The most common histologic type one patient died of disease due to disease progression. Table 3 shows
was immature teratoma followed by mixed MOGCT, dysgerminoma, the characteristics of patients with recurrent disease. Of the 30 patients
and yolk sac tumor. Most patients had FIGO stage I MOGCT. Thirty who had FIGO stage I MOGCT, three patients experienced disease recur-
nine patients had at least one tumor marker test before surgery; 16 pa- rence. One patient had FIGO stage IA disease and did not receive adju-
tients had an elevated serum cancer antigen 125 level, 20 patients had vant chemotherapy, while the other two patients had FIGO stage IB
an elevated serum alpha fetoprotein level, and five patients had an ele-
vated serum beta-human chorionic gonadotropin level.
All patients underwent surgical management. No one received neo- Table 2
adjuvant chemotherapy before surgery. Table 2 lists the surgical proce- Surgical management of malignant ovarian germ cell tumors (n = 42).

dures that were performed on 42 patients. Surgery was performed Surgical procedures N %
through laparotomy in 38 patients and through laparoscopy in four Unilateral ovarian cystectomy 1 2.4
patients. All patients underwent fertility-sparing surgery, defined as Unilateral oophorectomy 2 4.8
the preservation of at least one adnexa and the uterus. Comprehensive Unilateral salpingo-oophorectomy 31 73.8
surgical staging, involving peritoneal exploration, cytology, and biopsies Unilateral salpingo-oophorectomy and contralateral ovarian 8 19
cystectomy
and omentectomy, was performed on 25 patients. Pelvic and para-aortic
Pelvic lymphadenectomy 15 35.7
lymph node dissection was performed on 15 and 11 patients, respec- Para-aortic lymphadenectomy 11 26.2
tively. Bowel resection and reanastomosis was performed on three pa- Omentectomy 25 59.5
tients as a part of debulking surgery. Complete cytoreduction was Appendectomy 9 21.4
performed on all patients. Intraoperative or preoperative spillage of Small bowel resection and reanastomosis 2 4.8
Large bowel resection and reanastomosis 1 2.4
tumor was observed in 13 patients. Of the 26 patients who underwent

Please cite this article as: Park J-Y, et al, Outcomes of pediatric and adolescent girls with malignant ovarian germ cell tumors, Gynecol Oncol
(2015), http://dx.doi.org/10.1016/j.ygyno.2015.03.054
 J.-Y. Park et al. / Gynecologic Oncology xxx (2015) xxx–xxx 3

Table 3
Characteristics of patients with progressive or recurrent disease (n = 6).

No Age (years) Histology FIGO Operation Adjuvant Time interval to Site of first Treatment at Follow-up Status at last
stage Name chemotherapy recurrence recurrence recurrence time (months) follow-up
(cycles) (months)

1 9 Mixed IA LSO None 21 Pelvic LN Surgery, BEP 158 NED

(6)
2 11 YST IIC LSO, Large BEP (4) 8 Ovary Surgery, BEP 22 DOD
bowel R&A (10)
3 11 YST IIIC RSO, Small None 3 Peritoneal Chemotherapy, 24 AWD
bowel R&A carcinomatosis, BEP (6)
Lung
4 13 IT (grade 2) IIC RSO, LOC, BEP (6) 6 Pelvic Surgery, BEP 36 NED
PLND, peritoneum (6)
PALND,
PO,Appe
5 15 Mixed IC LSO, Appe BEP (6) 3 Paraaortic LN Surgery, BEP 77 NED
(5)
6 16 Dysgerminoma IB RSO, LOC BEP (4) 12 Pelvic LN Surgery, BEP 172 NED
(4)

FIGO, the International Federation of Obstetrics and Gynecology; LSO, left salpingo-oophorectomy; LN, lymph node; NED, no evidence of disease; YST, yolk sac tumor; R&A, resection and
reanastomosis; BEP, bleomycin + etoposide + cisplatin; DOD, die of disease; RSO, right salpingo-oophorectomy; AWD, alive with disease; IT, immature teratoma; LOC, left ovarian
cystectomy; PLND, pelvic lymph node dissection; PALND, paraaortic lymph node dissection; PO, partial omentectomy, Appe, appendectomy.

and IC disease and received adjuvant chemotherapy (Table 4). Among study were not homogenous because the study was done over a long
the 12 patients who had FIGO stage II–IV MOGCT, three patients had dis- period. Twenty seven patients underwent surgery and seven had
ease recurrence. The 5-year disease-free survival rate was 85%, and the gross residual disease. Twenty four received chemotherapy with 22 pa-
5-year overall survival rate was 97% (Fig. 1). We correlated clinicopath- tients receiving platinum-based chemotherapy and two patients receiv-
ologic factors including age (≤ 10 years versus N 10 years), complete ing radiation therapy. Five patients had disease recurrence and died of
surgical staging, lymph node dissection, the use of laparoscopy, lymph the disease. De Backer et al. reported the oncologic and reproductive
node metastasis, histologic types of tumor, peritoneal cytology, rupture outcomes of 24 children and young adolescents (median age, 9 years;
of tumor, FIGO stage (stage I versus II-IV), and adjuvant chemotherapy range, 3 months–15 years) with MOGCT [16]. However, again, the treat-
with disease-free survival in univariate analysis. However, none of ment regimens were not homogeneous; the type of chemotherapy ad-
these factors was significantly associated with disease-free survival. ministered differed from patient to patient and one patient received
At the time of this analysis, the median age of the 41 patients who radiotherapy. Three patients experienced disease recurrence and one
were still alive was 19 years (range, 10–30 years). Seven patients patient died of the disease. The reproductive outcomes of the patients
were premenarchal, 30 patients had regular menstruations, and three who received fertility-sparing management in the two studies were fa-
patients had irregular menstruations. None of the patients experienced vorable. In our study, all patients received uniform treatment consisting
premature ovarian failure. No one tried pregnancy. of fertility-sparing, complete cytoreductive surgery and BEP chemother-
apy. The survival rate was 97%, and all patients had regular or irregular
menstruation without experiencing premature ovarian failure. These
4. Discussion results demonstrate that this treatment constitutes a safe and realistic
standard management procedure for children and young adolescents
In this study, all of the MOGCT patients were subjected to uniform with MOGCT regardless of their histology or FIGO stage.
treatment comprising fertility-sparing, complete cytoreductive surgery Recently, Solheim et al. used serum Anti-Mullerian Hormone (AMH)
followed by adjuvant BEP chemotherapy, which is the current standard levels to evaluate gonadal function in 22 young women (median age,
management protocol for MOGCT. The follow-up time in the study was 30 years; range, 18–39 years) with MOGCT after fertility-sparing sur-
sufficiently long to allow a comprehensive evaluation of the treatment gery and platinum-based adjuvant chemotherapy [17]. Only two
outcomes. The survival outcomes were excellent and reproductive out- women were revealed to have AMH values below 3 pmol/L, but one
comes were favorable. was pregnant and the other was 39 years old with no menopausal
As far as we know, this study is the largest one to report the treat- symptoms. They found no correlation between AMH levels and the cu-
ment outcomes of pediatric and adolescent girls with MOGCT. Spreafico mulative dose of cisplatin. These results support the safety of fertility-
et al. reported the oncologic and reproductive outcomes of 29 children sparing surgery with subsequent platinum-based adjuvant chemother-
and young adolescents (median age, 12 years; range, 6–17 years) with apy in young women with MOGCT from the viewpoint of gonadal
MOGCT [15]. However, the treatments applied to the patients in their function.
A recent issue in the management of MOGCT in children and young
adolescents with FIGO stage I MOGCT is disease surveillance after initial
Table 4 surgery without chemotherapy. In patients with a stage I malignant tes-
Recurrence according to FIGO stage and adjuvant chemotherapy (n = 42). ticular germ cell tumor, 75% were cured by surgery alone, and salvage
with chemotherapy was successful in those with recurrence [18]. There-
Observation Adjuvant chemotherapy
fore, surveillance without chemotherapy after initial surgery for stage I
No Recurrence, n (%) No Recurrence, n (%)
malignant testicular germ cell tumor is regarded as a standard of care in
IA 10 1 (10) 11 0 (0)
IB 0 0 (0) 1 1 (100) prepubertal boys [19]. Encouraged by these results, this surgery-only,
IC 0 0 (0) 8 0 (0) watch-and-wait strategy was evaluated in 25 children and young ado-
II-IV 1 1 (100) 11 2 (18.2) lescents (median age, 12 years; range, 0–16 years) with FIGO stage I
Total 11 2 (18.2) 31 3 (9.7) MGOCT [20]. After a median follow-up time of 42 months, 12 (50%) pa-
FIGO, the International Federation of Obstetrics and Gynecology. tients experienced recurrence and, among these, 11 were successfully

Please cite this article as: Park J-Y, et al, Outcomes of pediatric and adolescent girls with malignant ovarian germ cell tumors, Gynecol Oncol
(2015), http://dx.doi.org/10.1016/j.ygyno.2015.03.054
4 J.-Y. Park et al. / Gynecologic Oncology xxx (2015) xxx–xxx
Fig. 1. Disease-free survival (left) and overall survival (right) in 42 children and young adolescent girls with malignant ovarian germ cell tumors.
salvaged by chemotherapy. The 4-year overall survival rate was 96%,
and applying a surgery-only, watch-and-wait strategy did not impair
the overall oncologic outcomes and resulted in 50% of the patients
avoiding having to take adjuvant chemotherapy. This is important
because renal impairment, neurotoxicity, and hearing loss have
been reported in pediatric patients with MOGCT after platinum-
based chemotherapy. Additionally, some studies have reported an
increase in the number of secondary malignancies after platinum-
based chemotherapy [21,22]. In our study, out of the ten patients
with stage I MOGCT who did not receive adjuvant chemotherapy,
only one experienced disease recurrence 21 months after surgery.
This patient was successfully salvaged by secondary surgery and
BEP chemotherapy (Table 3). This surveillance strategy should be
evaluated further in future studies.
Systematic pelvic and para-aortic lymph node dissection may be
omitted in young girls and adolescents with early stage MOGCT [23].
The inspection and removal of enlarged lymph node may be sufficient
for the evaluation of the status of regional lymph nodes. However, sys-
tematic pelvic and para-aortic lymph node dissection may be some-
times required in patients with advanced stage MOGCT or multiple
lymph node involvement and in patients with early stage MOGCT who
want observation after surgery without chemotherapy. In our series,
these patients underwent systematic pelvic and paraaortic lymph
node dissection.
Three patients with stage I MOGCT who did not undergo complete
staging including lymphadenectomy at initial surgery had recurrent
disease in pelvic or paraaortic lymph nodes. Of them, two patients
with stage IB and IC MOGCT received adjuvant chemotherapy after
initial surgery, but one patient with stage IA MOGCT did not re-
ceived. If the last patient underwent complete stating operation in-
cluding lymphadenectomy, the lymphatic involvement of MOGCT
might be revealed at initial surgery and she might receive adjuvant
chemotherapy and might not have recurrent disease. Because about
half of patients did not undergo complete staging operation in our
series, some patients with stage I disease in our series might be
upstaged after complete staging operation. Therefore, complete
staging operation including lymphadenectomy is crucial to follow-
up patients without adjuvant chemotherapy in stage I MOGCT.
This study is limited by the small number of study subjects; howev-
er, it is the largest one to have studied the outcomes of children and
young adolescents with MOGCT. A strength of this study was that, un-
like previous studies, all patients received a uniform standard treatment
and the follow-up period was long.
In conclusion, oncologic outcomes were excellent and reproduc-
tive outcomes were favorable in children and young adolescent
with MOGCT after fertility-sparing complete cytoreductive surgery
Please cite this article as: Park J-Y, et al, Outcomes of pediatric and adolescent girls with malignant ovarian germ cell tumors, Gynecol Oncol
(2015), http://dx.doi.org/10.1016/j.ygyno.2015.03.054
followed by BEP chemotherapy, regardless of the histologic type or
FIGO stage.
Conflict of interest statement
The authors declare that there are no conflicts of interest.
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Please cite this article as: Park J-Y, et al, Outcomes of pediatric and adolescent girls with malignant ovarian germ cell tumors, Gynecol Oncol
(2015), http://dx.doi.org/10.1016/j.ygyno.2015.03.054