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Pure nongestational ovarian choriocarcinoma: A scoping review

Alison Garrett

Department of Obstetrics and Gynecology, University of Pittsburgh, Magee Women’s Hospital, USA

Amy Knehans

Harrell Health Sciences Library, Penn State College of Medicine, USA

Rebecca Phaeton

Division of Gynecologic Oncology, Penn State Hershey Medical Center, USA

Joshua P. Kesterson

Division of Gynecologic Oncology, Penn State Hershey Medical Center, USA

DOI: 10.15761/ICST.1000229

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Abstract

Choriocarcinoma of the ovary is a rare and highly malignant germ cell tumor.  There are three ways in which an ovarian choriocarcinoma can arise: as a primary gestational choriocarcinoma that results from an ectopic ovarian pregnancy, as a metastatic choriocarcinoma that arises from a gestational choriocarcinoma, and as a germ cell tumor with differentiation into trophoblastic structures.  Ovarian choriocarcinomas are therefore classified as gestational or nongestational.  Recently, DNA polymorphism analysis has allowed investigators to determine the etiology of choriocarcinoma (gestational versus nongestational).  Herein, in this scoping review, we detail the classification of, and clinical aspects of, pure ovarian choriocarcinoma.

Introduction

Choriocarcinoma is a very rare and highly malignant germ cell tumor that accounts for <1% of all malignant germ cell tumors [1]. There are three ways in which an ovarian choriocarcinoma can arise: as a primary gestational choriocarcinoma that results from an ectopic ovarian pregnancy, as a metastatic choriocarcinoma that arises from a gestational choriocarcinoma from another primary site in the female genital tract, and as a germ cell tumor with differentiation into trophoblastic structures [2].

Choriocarcinoma is classified as gestational or nongestational. Gestational choriocarcinoma is a form of gestational trophoblastic disease, which arises from a partial mole, a complete mole, or a normal pregnancy. Gestational choriocarcinoma is estimated to occur in about 2 to 7 pregnancies per 100,000 in the United States [3]. Nongestational choriocarcinoma does not arise from a pregnancy event and is an extremely rare occurrence. The incidence of primary ovarian nongestational choriocarcinoma is estimated to be 1 in 369,000,000 [4]. Differentiating gestational and nongestational choriocarcinoma can be difficult, as their clinical presentation and pathology can be identical. Traditionally, a definitive diagnosis of nongestational choriocarcinoma has been restricted to prepubescent females in whom the possibility of a pregnancy event can be eliminated with certainty.

Choriocarcinoma of the ovary can be pure choriocarcinoma or, more commonly, mixed with other germ cell components [1]. When examined histologically, if other germ cell components are present mixed with choriocarcinoma, a diagnosis of a nongestational origin can be made. However, if no other germ cell component is present, differentiating a nongestational from gestational origin is impossible using histologic means alone.

Recently, however, DNA polymorphism analysis has allowed investigators to determine the etiology of choriocarcinoma via analysis of the patient’s DNA, her partner’s DNA, and the DNA of the choriocarcinoma. By examining the DNA composition of the tumor and comparing it to the maternal and paternal DNA, the etiology of the choriocarcinoma can be determined. If the DNA of the tumor exactly matches the maternal DNA, the tumor is of non-gestational origin. However, if the tumor contains any alleles matching paternal DNA, the tumor is of gestational origin [5].

In 1982, Jacobs et al. published a comprehensive literature review on pure ovarian choriocarcinoma [6]. The study classified all published cases of pure ovarian choriocarcinoma at the time into three categories: gestational ovarian choriocarcinoma, pure nongestational ovarian choriocarcinoma, and choriocarcinoma of uncertain etiology. The pure nongestational ovarian choriocarcinoma category was assigned to all pure ovarian choriocarcinoma cases occurring in prepubertal females, and the uncertain etiology was assigned to all pure ovarian choriocarcinoma cases in postpubertal women who were said to be sexually abstinent or virginal. Since the publication of this review, several other literature reviews on this topic have been published; however, limitations exist, including lack of definitive categorization strategies. As a result, little is known about the incidence, clinical course, most effective treatment regimen, as well as outcomes for pure ovarian nongestational choriocarcinoma. The purpose of this scoping review is to provide a strict definition of pure ovarian choriocarcinoma that allows appropriate classification of nongestational and gestational origin in order to better understand this disease process.

Methods

The search strategy was developed in collaboration with a librarian at Penn State Hershey College of Medicine. We searched PubMed for articles published in English using the following search string: ((("choriocarcinoma"[MeSH Major Topic] OR choriocarcinoma [Title/Abstract]) AND (nongestational[Title/Abstract] OR non-gestational[Title/Abstract])) AND ((ovary[Title/Abstract] OR ovarian[Title/Abstract]) OR gonad[Title/Abstract])) AND english[Language] which resulted in 66 titles. Additionally, we searched Web of Science using All Databases with the following search string: (ts=(choriocarcinoma AND (nongestational OR non-gestational)) OR ti=(choriocarcinoma AND (nongestational OR non-gestational))) AND LANGUAGE: (English), which yielded 57 titles for a sum total of 123 titles. The final search in PubMed and Web of Science was performed on January 6, 2016. Duplicates (n=43) were excluded.

We included case reports and retrospective chart reviews. Review articles and book chapters were excluded (n=7). Review articles and those articles included in the analysis were cross-referenced to identify additional studies missed in initial database search (n=6). Included articles were limited to those dealing with pure non-gestational choriocarcinoma of the ovary.

Criteria used to define a non-gestational origin of the tumor were cases occurring in prepubertal girls or a cases establishing a diagnosis of non-gestational origin via DNA analysis. All other cases were excluded from the results and discussion. Some literature described young G0 females without mention of their history of sexual activity. In these cases, if the patient was <20 years of age, these cases were included (unless nongestational origin was confirmed upon DNA analysis). Because Jacobs et al published an exhaustive literature review on pure choriocarcinoma of the ovary of cases occurring prior to 1981; we included only studies published after 1980. Those articles not meeting this criteria (n=49) were excluded, see Table 4. Additionally, nine articles were inaccessible to us despite multiple requests for full-text articles, and so these were excluded [6-14]. The total number of articles included in this review is 21.

Table 4. Excluded citations

Reason for Exclusion

Title

Authors

Gestational choriocarcinoma

Primary choriocarcinoma of the ovary. Report of two cases

Gangadharan VP, Mathew BS, Kumar KS, Chitrathara K

Intra-operative cytodiagnosis of primary ovarian choriocarcinoma with ki67 immunoexpression

Kar A, Kar T, Mahapatra S, Dehuri P

Pure ovarian choriocarcinoma: a report of two cases

Mood NI, Samadi N, Rahimi-Moghaddam P, Sarmadi S, Eftekhar Z, Yarandi F

Ovarian choriocarcinoma arising from partial mole as evidenced by deoxyribonucleic acid microsatellite analysis

Namba A, Nakagawa S, Nakamura N, Takazawa Y, Kugu K, Tsutsumi O, Taketani Y

Pure choriocarcinoma of ovary diagnosed by fine needle aspiration cytology

Naniwadekar MR, Desai SR, Kshirsagar NS, Angarkar NN, Dombale VD, Jagtap S

Not ovarian choriocarcinoma

Genotyping Diagnosis of Nongestational Choriocarcinom Involving Fallopian Tube and Ligament: A Case Study

Buza N, Rutherford T, Hui P

Extraovarian nongestational choriocarcinoma in a postmenopausal woman

Dilek S, Pata O, Tok E, Polat A

Endometrial carcinoma in elderly women

Hoffman K, Nekhlyudov L, Deligdisch L

Primary non-gestational choriocarcinoma of the uterine cervix: a case report

Maesta L, Michelin OC, Traiman P, Hokama P, Rudge MVC

Fallopian tube choriocarcinoma presenting as ovarian tumour: a case report

Mundkur A, Rai L, Hebbar S, Guruvare S, Adiga P

Concurrent ovarian-type primary peritoneal adenocarcinoma and peritoneal choriocarcinoma. A case report and review of the literature

Pentheroudakis G, White J, Davis J, Brown I, Vasey P

 

Primary omental gestational choriocarcinoma ascertained by deoxyribonucleic acid polymorphism analysis

Sakumoto K, Nagai Y, Inamine M, Kanazawa K

Testicular choriocarcinoma metastatic to the skin: an additional case and literature review

Tinkle LL, Graham BS, Spillane TJ, Barr RJ

Primary renal artery choriocarcinoma causing secondary renovascular hypertension

Usta TA, Karacan T, Ozyurek E, Naki MM, Omeroglu SN, Demirkiran F

Pure nongestational uterine choriocarcinoma in a postmenopausal Chinese woman confirmed with short tandem repeat analysis

Wang YM, Yang YF, Teng F, Zhang HY, Xue FX

Primary choriocarcinoma of the vulva

Weiss S, Amit A, Schwartz MR, Kaplan AL

Not pure choriocarcinoma

Ovarian nongestational choriocarcinoma mixed with various epithelial malignancies in association with endometriosis

Hirabayashi K, Yasuda M, Osamura RY, Hirasawa T, Murakami M

Serous carcinoma of the endometrium with choriocarcinomatous differentiation: A case report and review of the literature indicate the existence of 2 prognostically relevant tumor types

Horn LC, Hanel C, Bartholdt E, Dietel J

Malignant mixed ovarian germ cell tumor with embryonal component

Moniaga NC, Randall LM

Nongestational choriocarcinoma arising from a primary ovarian tumour

Oladipo A, Mathew J, Oriolowo A, Lindsay I, Fisher R, Secki M, Yiannakis D

Nongestational choriocarcinoma of the ovary—a case report

Pai MR, Naik R

Postmenopausal patient

Choriocarcinoma of the ovary in a postmenopausal woman

Babu MK, Kini U

A case of non-gestational choriocarcinoma arising in the ovary of a postmenopausal woman

Park  SH, Park A, Kim JY, Kwon JH, Koh SB

Patient ≥20 years old

Primary pure ovarian choriocarcinoma mimicking ectopic pregnancy: a report of fulminant progression

Balat O, Kutlar I, Ozkur A, Bakir K, Aksoy F, Ugur MG

Primary ovarian choriocarcinoma mimicking ectopic pregnancy managed with laparoscopy--a case report

Chen YX, Xu J, Lv WG, Xie X

Pure nongestational choriocarcinoma of the ovary: a case report

Choi YJ, Chun KY, Kim YW, Ro Dy

Pure nongestational choriocarcinoma of ovary

Corakci A, Ozeren S, Ozkan S, Gurbus Y, Ustun H, Yucesoy I

Pure primary non-gestational ovarian choriocarcinoma: a diagnostic dilemma

Gon S, Majumdar B, Barui G, Karmakar R, Bhattacharya A

Management of non-gestational ovarian choriocarcinoma: laparoscopy can be essential. Report of two cases

Gremeau AS, Bourdel N, Kondo W, Jardon K, Canis M

Primary pure choriocarcinoma of the ovary

Grover V, Grover RK, Usha R, Logani KB

Leydig cell tumor, mature teratoma, and nongestational choriocarcinoma in a single ovary

Jain T, VanKessel K, Reed S, Paley P

Pure choriocarcinoma of the ovary: a case report

Lv L, Yang K, Wu H, Lou J, Peng Z

Ovarian choriocarcinoma: a difficult diagnosis of an unusual tumor and a review of the hook effect

Wheeler CA, Davis S, Degefu S, Thorneycroft IH, O’Quinn AG

Developing retroperitoneal anaplastic carcinoma with choriocarcinoma focus after ovarian nongestational choriocarcinoma: a case report

Nikolic B, Ljubic A, Terzic M, Arandjelovic A, Babic S, Vucic M

Primary pure choriocarcinoma of the ovary in reproductive ages: a case report

Simsek T, Trak B, Tunc M, Karaveli S, Uner M, Sonmez C

Primary ovarian nongestational choriocarcinoma. Report of a case in a young woman of childbearing age

Vogler C, Schmidt WA, Edwards CL

Case labeled as nongestational choriocarcinoma, but no further information of clinical context provided

Primary chemotherapy and the role of second-look laparotomy in non-dysgerminomatous malignancies of the ovary

 

Pippitt CH Jr, Cain JM, Hakes TB, Pierce VK, Lewis JL Jr

Patient <20 years old but with history of sexual activity

Pure choriocarcinoma of the ovary in Silver-Russell Syndrome

Haruma T, Ogawa C, Nishida T, Kusumoto T, Nakamura K, Seki N, Katayama T, Hiramatsu Y

Animal study

Immunohistological Description of Nongestastional Ovarian Choriocarcinoma in Two Female Mice with Conditional Loss of Trp53 Driven by the Tie2 Promoter

Castiglioni V, Ghahremani MF, Goosens S, Maglie MD, Ardizzone M, Haigh JJ, Radelli E

Non-gestational malignant placental site trophoblastic tumor of the ovary in a 4-year-old rhesus monkey

Marbaix E, Defrere S, Duc KH, Lousse JC, Dehoux JP

Cell line study/bench research/no human case study

Limitation of differential expression of HLA-A,B,C antigens on choriocarcinoma cell lines by messenger RNA for HLA heavy chain but not by beta 2-microglobulin

Kawata M, Sizer K, Sekiya S, Parnes JR, Herzenberg LA

Epidermal growth-factor receptors in human corpora-lutea during the menstrual cycle and pregnancy

Khandawood FS, Ayyagari RR, Dawood MY

Localization of the cellular expression of inhibin in trophoblastic tissue

McCluggage WG, Ashe P, McBride H, Maxwell P, Sloan JM

Establishment and properties of a human choriocarcinoma cell line of ovarian origin

Sekiya S, Kaiho T, Shirotake S, Iwasawa H, Inaba N, Kawata M, Higaki K, Ishige H, Takamizawa H, Minamihisamatsu M, Kuwata T

Usefulness of intraoperative imprint cytology in ovarian germ cell tumors

Abe A, Sugiyama Y, Furuta R, Matoda M, Takeshima N

 

The impact of molecular genetic diagnosis on the management of women with hCG-producing malignancies

Fisher RA, Savage PM, MacDermott C, Hook J, Sebire NJ, Lindsay I, Secki MJ

Published prior to 1980

Nongestational choriocarcinoma of ovary—report of a case

Dehaan QC

Primary non-gestational choriocarcinoma of the ovary. Report of a case

Panayotou PP

Author published two studies that described same case (excluded one of studies from review)

Ovarian neoplasms in children and adolescents in Papua New Guinea

Sengupta SK, Everett VJ

Review articles/book chapters

Diagnostic dilemma: non-gestational or gestational choriocarcinoma of the ovary

Bhatia K, Vaid AK

Hormonally Active Organ Tumors in Children and Adolescents

Hicks ML, Danzey TJ

Gestational Choriocarcinoma

Hui P

Recent advances in the pathology and classification of ovarian germ cell tumors

Roth LM, Talerman A

Clinical syndromes associated with ovarian neoplasms: a comprehensive review

Shanbhogue AK, Shanbhogue DK, Prasad SR, Surabhi VR, Fasih N, Menias CO

 

Germ Cell Tumors of the Ovary

Talerman A, Vang R

 

Pathology of Germ Cell Tumors

Zaloudek CJ

 

Results

Classification

Since 1980, a total of 22 possible cases of pure nongestational ovarian choriocarcinoma have been published in the English language. Of these, nine occurred in premenarchal females [12-18], 11 occurred in postmenarchal females but were confirmed by DNA analysis [18,19-25], and eight were considered possible cases of pure NGOC according to the strict criteria described above in the methods section [18,26-32] (Tables 1-3).

Age

In the premenarchal group, the average age at diagnosis was 13.6 years. One study did not include the age of the patient at presentation [20]. Another case occurred in a 39 year-old female with a history of gonadal dysgenesis and primary amenorrhea [19].

In the DNA confirmed group, the average age at diagnosis was 24.5 years. One study that reported on three of these cases did not include the age at diagnosis [21].

In the possible cases group, the average age at diagnosis was 14.0 years.

FIGO Stage

In the premenarchal group, the FIGO stage of eight of the cases did not state the FIGO stage. For the one case that did, the FIGO stage was reported as IC [16].

For the DNA confirmed group, the FIGO stage of five cases was not reported. The remaining cases had FIGO stages of IA [26], IIIC [23], and IV [25].

For the possible cases group, the FIGO stage of five cases was not reported. The remaining cases had FIGO stages of IA [31], I [32], and III [35].

Surgery performed

In the premenarchal group (n=9), surgical therapy was reported for five of the cases but not stated for four cases. Of the five cases which reported surgical therapy, two had a unilateral oophorectomy performed [15], one had a unilateral salpingo-oopherectomy performed [17], one had a unilateral salpingo-oopherectomy and partial omentectomy performed [16], and one had a bilateral salpingo-oopherectomy, hysterectomy, omentectomy, and thoracoscopy and wedge resection for pleural lesions [19].

For the DNA confirmed group (n=11), surgical therapy was reported for all but five of the cases. Of the 11 cases which reported surgical therapy, one had a total abdominal hysterectomy, bilateral salpingo-oopherecotmy, and omentectomy performed two months after completion of chemotherapy [22]; one had an initial removal of the ovarian mass and two rounds of chemotherapy which were followed by followed by a total abdominal hysterectomy, bilateral salpingo-oopherecotmy, omental resection, pelvic lymph node dissection, and appendectomy [23]; one had a total abdominal hysterectomy, bilateral salpingo-oopherecotmy, omentectomy, and pelvic lymph node dissection performed [24]; two had a left salpingo-oopherectomy and partial omentectomy performed [25,26]; and one had a right salpingo-oopherectomy performed [27].

For the possible cases group (n=8), surgicial treatment was not reported for one case. Surgery was not performed in one case [3]. Unilateral salpingo-oopherectomy was performed in two cases [30,34]. The remaining cases were treated surgically with a left salpingo-oopherectomy, total omentectomy, and inversion appendectomy [29]; a left salpingo-oopherectomy and partial omentectomy [31]; a left salpingo-oopherectomy and right ovarian cystectomy [32]; and a right salpingo-oopherectomy, left ovarian cystectomy and omentectomy [35].

Chemotherapy

In the premenarchal group, one case did not state whether chemotherapy was used [21]. Two cases were treated with surgical therapy alone [15]. Two cases were treated with PVB (cisplatin, bleomycin, and vinblastine) therapy [16, 18]. One case was treated with vincristine, methotrexate, leukovorin, bleomycin, Adriamycin, and cyclophosphamide [14]. One cases was treated with multiple rounds of various chemotherapeutic agents, see Table 1 [19]. One case was treated with “radiotherapy and chemotherapy,” but the study did not describe any further details [20]. One case was treated with “three drug chemotherapy,” but the study did not expound upon what these three drugs were [20].

For the DNA group, five cases did not include information of chemotherapy treatment. The BEP chemotherapy regimen was used in two cases for four and five cycles, respectively [22] and [23]. One patient was treated with the MAC regimen for four cycles [16]. One patient was treated with the EMA regimen for four cycles [27]; and one patient was treated with one course of EMA followed by 7 cycles of just etoposide and actinomycin due to methotrexate-toxicity [26].

For the possible cases group, chemotherapy treatment was not reported in two cases. Chemotherapy was not given in one case [33] The BEP regiment was used in two cases for three and six cycles, respectively [30,31]. The BEP regimen was also used on another patient for four cycles, followed by high-dose CTx with carboplatin, etoposide, ifosphamide with subsequent bone marrow transplantation [35]. Finally, two patients were treated methotrexate, actinomycin, and an alkylating agent (MAC) regimen for 4 cycles [32] and 5 cycles [34].

Survival

In the premenarchal group, survival outcomes were not reported for three cases [16,17,21]. One patient was reported to be alive and well at ten-year follow-up [15], one patient had no evidence of disease at six-month follow-up [18], one had no evidence of disease at 17-month follow-up [19], and one had no evidence of disease at one year follow-up [20]. One patient died from immediate postoperative complications [15], and one patient was reported dead of disease [20].

For the DNA-confirmed group, outcome was not reported in six cases. Four patients had no evidence of disease at varying follow-up intervals: one month [22], 12 months [26], 18 months [24], and 30 months [23]. One patient was reported dead of disease at 4 months [27].

For the possible cases group, outcome was not reported in two cases. Five patients had no evidence of disease at varying follow-up intervals: 5 months [32], 9 months [34] 14 months [31], 36 months [35], and 62 months [30]. In one case, the patient arrested during initial imaging and all resuscitation efforts were unsuccessful [33] (Tables 1-3).

Discussion

This study highlights several features of pure nongestational ovarian choriocarcinoma. First, this study emphasizes the rarity of pure nongestational ovarian choriocarcinoma.  Nine cases of premenarchal pure nongestational ovarian choriocarcinoma and eight cases of possible pure nongestational choriocarcinoma have been reported since 1980. Just twelve cases of pure ovarian nongestational ovarian choriocarcinoma have been confirmed by DNA polymorphism analysis. Because of the rarity of this disease process, stricter diagnostic criteria should be used in order to correctly categorize nongestational origin from gestational origin, as unless confirmed by DNA analysis or the disease occurs in a patient who is premenarchal, one cannot with absolute certainty classify an ovarian choriocarcinoma.  Recently, DNA analysis has been used to successfully determine nongestational versus gestational origin of ovarian choriocarcinoma. This technology will allow for appropriate classification of this disease process which will ultimately lead to improved therapeutic strategies as more information is learned about pure nongestational ovarian choriocarcinoma.

Secondary to the rarity of this disease process, no standard therapy has been established. Treatment is often extrapolated from treatment strategies for gestational choriocarcinoma and germ cell tumors, thereby leading to significant heterogeneity in treatment strategies for pure nongestional ovarian choriocarcinoma.  In reviewing the clinical outcomes of those with pure ovarian suspected choriocarcinoma (confirmed and suspected), it is difficult to make definitive treatment recommendations secondary to heterogeneity in, and inconsistent reported of, relevant clinical factors, including disease classification, patient age, stage, surgery, adjuvant therapy and outcomes, combined with the rarity of this particular entity.  For those reported cases in which outcomes were reported (n=16), at a follow-up ranging from one month to ten years, 12 were reported as NED, a majority (n=11) were treated with adjuvant chemotherapy (Tables 1-3).  Commonly used adjuvant combinational treatment regimens include BEP and EMA.   

Table 1. Pure NGOC cases in premenarchal females since 1980

Case

Age (years)

Menarchal Status

hCG

Surgery

FIGO Stage

Chemotherapy

Outcome

 [15]

6

Premenarchal

NS*

RO

NS

None

NED at 10 years

 [15]

11

Premenarchal

NS

RO

NS

None

DOD—“attributed to immediate postoperative complications”

 [16]

10

Premenarchal

7957 mIU/L at 7 days postop

LSO, partial omentectomy

IC

 PVB x 5 cycles

NS

 [17]

11

Premenarchal

Not performed prior to surgery; negative postop

RSO

NS

Vincristin, methotrexate, leukovorin, bleomycin, adriamycin, cyclophosphamide

NS

 [18]

9

Premenarchal

NS

NS

NS

PVB x 3 courses

NED at 6 months

 [19]

39

History of gonadal dysgenesis and primary amenorrhea

 

45XO/46XY karyotype

26392 mIU/ml  at postop referral

Hysterectomy, BSO, omentectomy

 

Thoracoscopy for pleural lesion resection and wedge resection of lung nodules

NS

Cisplatin and etoposide x 4 courses

 

BEP x 1 course

 

Cisplatin, etoposide, ifofsamide x 2 course

 

Oral etoposide x 7 days

 

Carboplatin, vinblastine, Adriamycin x 1 course

 

High-dose CTx + autologous BMT

NED at 17 months

 [20]

NS

Presented with precocious puberty

“precocious puberty 2/2 tumor production of hCG”

NS

NS

“Radiotheray and chemotherapy”

DOD

 [20]

11

Premenarchal

“increased”

NS

NS

“3 drug CTx”

NED at 1 year

 [21]

12

Premenarchal

Elevated

NS

NS

NS

NS

* Abbreviations: NS: Not Stated, AAW: Alive and Well, DOD: Dead of Disease, NED: No Evidence of Disease, TAH: Total Abdominal Hysterectomy, R: Right, L: Left, B: Bilateral, S: Salpingectomy, O: Oophorectomy, MAC: Methotrexate, Actinomycin, Alkylating Agent, BEP: Bleomycin, Etoposide, Cisplatin, PVB: Cisplatin, Bleomycin, Vinblastine, EMA: Etoposide, Methotrexate, Actinomycin, EMA/CO: Etoposide, Methotrexate, Actinomycin, Cyclophosphamide, Oncovin

Figure 1. Flow diagram of included studies.

Table 2. Pure NGOC cases confirmed by DNA analysis

Case

Age (years)

Reproductive Status

hCG

Surgery

FIGO Stage

Chemotherapy

Outcome

DNA analysis

 [22]

24

G1P0A1

675,713 mIU/mL

TAH, BSO, omentectomy 2 months after completion of CTx

NS

BEP x 4 cycles

NED at 1 month

DNA polymorphism analysis at 8 loci

[23]

23

G3P1

26,516 mIU/mL

Initially, removal of mass and omental biopsy

 

TAH, BSO, omental resection, pelvic lymph node dissection, appendectomy following 2 courses of BEP CTx

IIIC

BEP x 5 cycles

NED at 30 months

Histo: ovarian CC and some immature seminiferous tubulues

 

DNA polymorphism analysis with 5 STR loci

 

Karyotype analysis of peripheral blood 46XX

 

FISH confirmed absence of SRY hybridization signal in tumor; all nuclei of ovary and tumor hybridized with two XX signals

 

In testicular tissue both two XX signals (75%) and one X signal (25%)

[24]

33

G0

185,000 mIU/mL

TAH, BSO, omentectomy, pelvic lymph node dissection

NS

MAC x 4 courses

NED at 18 months

DNA polymorphism analysis using eight microsatellite markers

[25]

19

G0, virgin

 

LSO, partial omentectomy, R ovarian biopsy

IV

EMA/CO x “multiple courses”

NS

DNA polymorphism analysis of two loci

[26]

19

G0, virgin

206,949.7 mIU/mL

LSO, partial omentectomy

IA

EMA x 1 course

 

Etoposide, actinomycin x 7 courses

NED at 12 months

DNA polymorphism analysis at 15 loci

[21]

NS

G0, virgin

 

 

 

 

 

DNA polymorphism analysis at 12 loci

[21]

NS

“married”

 

 

 

 

 

DNA polymorphism analysis at 12 loci

[21]

NS

“married”

 

 

 

 

 

DNA polymorphism analysis at 12 loci

[27]

26

G0

64,000 IU/L

RSO

NS

EMA x 4 courses

DOD at 4 months

DNA polymorphism analysis at 9 loci

[28]

25

G0

NS

NS

NS

NS

NS

DNA polymorphism analysis at 11 loci

[28]

27

G0

NS

NS

NS

NS

NS

DNA polymorphism analysis at 11 loci

*See Table 1 for explanations of abbreviations.

Table 3. Possible pure NGOC cases since 1980

Case

Age (years)

Reproductive Status

hCG

Surgery

FIGO Stage

Chemotherapy

Outcome

[29]

15

G0, virgin

Urine positive x 2

 

Blood negative x 3

LSO, total omentectomy, inversion appendectomy

NS

NS

NS

[30]

10

Menarche 6 months prior to presentation

6,600 ng/mL

RSO

NS

BEP x 3 courses

NED at 62 months

[31]

12

G0, virgin

20,257 mIU/mL

LSO, partial omentectomy, multiple peritoneal biopsies

IA

BEP x 6 courses

NED at 14 months

[32]

18

G0, virgin

Urine positive

LSO, R ovarian cystectomy, omental and peritoneal biopsies

I

MAC x 4 courses

NED at 5 months

[33]

16

G0, virgin

NS

Not performed

NS

Not given

Cardiac arrest during imaging, all resuscitating measures unsuccessful

[34]

 

13

G0, virgin

Urine positive

RSO

NS

MAC x 5 courses

NED at 9 months

[21]

16

G0, virgin

NS

NS

NS

NS

NS

[35]

12

G0

1,100,000 IU/L after initial surgery

RSO, L ovarian cystectomy, omentectomy

III

BEP x 4 courses

 

High-dose CTx with carboplatin, etoposide, ifosphamide followed by BMT

NED at 3 years

*See Table 1 for explanation of abbreviations.

Herein, in this scoping review, we have detailed the classification of, and clinical aspects of, pure ovarian choriocarcinoma.  Secondary to its rarity and variability in reporting, conclusive recommendations regarding ideal therapy is lacking.  Going forward, definitive categorization, via DNA polymorphism analysis, and creation of an international tumor registry is warranted for rare disease entities such as pure ovarian choriocarcinoma, in order to facilitate better comprehension of its etiology and standardization of therapy with optimization of outcomes.

Acknowledgements

The authors would like to thank Kathy Shrawder for her expertise in the preparation and formatting of this manuscript.

References

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Editorial Information

Editor-in-Chief

Vicente Notario
Georgetown University Medical Center

Article Type

Review Article

Publication history

Received date: February 02, 2017
Accepted date: February 25, 2017
Published date: February 28, 2017

Copyright

© 2017 Garrett A. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Citation

Garrett A, Knehans A, Phaeton R, Kesterson JP (2017) Pure nongestational ovarian choriocarcinoma: A scoping review. Integr Cancer Sci Therap. 4: DOI: 10.15761/ICST.1000229

Corresponding author

Joshua P. Kesterson

Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Penn State Hershey Medical Center, 500 University Drive, Hershey, PA 17036, USA, Tel: (717) 531-8144, Fax: (717) 531-0007

Figure 1. Flow diagram of included studies.

Table 1. Pure NGOC cases in premenarchal females since 1980

Case

Age (years)

Menarchal Status

hCG

Surgery

FIGO Stage

Chemotherapy

Outcome

 [15]

6

Premenarchal

NS*

RO

NS

None

NED at 10 years

 [15]

11

Premenarchal

NS

RO

NS

None

DOD—“attributed to immediate postoperative complications”

 [16]

10

Premenarchal

7957 mIU/L at 7 days postop

LSO, partial omentectomy

IC

 PVB x 5 cycles

NS

 [17]

11

Premenarchal

Not performed prior to surgery; negative postop

RSO

NS

Vincristin, methotrexate, leukovorin, bleomycin, adriamycin, cyclophosphamide

NS

 [18]

9

Premenarchal

NS

NS

NS

PVB x 3 courses

NED at 6 months

 [19]

39

History of gonadal dysgenesis and primary amenorrhea

 

45XO/46XY karyotype

26392 mIU/ml  at postop referral

Hysterectomy, BSO, omentectomy

 

Thoracoscopy for pleural lesion resection and wedge resection of lung nodules

NS

Cisplatin and etoposide x 4 courses

 

BEP x 1 course

 

Cisplatin, etoposide, ifofsamide x 2 course

 

Oral etoposide x 7 days

 

Carboplatin, vinblastine, Adriamycin x 1 course

 

High-dose CTx + autologous BMT

NED at 17 months

 [20]

NS

Presented with precocious puberty

“precocious puberty 2/2 tumor production of hCG”

NS

NS

“Radiotheray and chemotherapy”

DOD

 [20]

11

Premenarchal

“increased”

NS

NS

“3 drug CTx”

NED at 1 year

 [21]

12

Premenarchal

Elevated

NS

NS

NS

NS

* Abbreviations: NS: Not Stated, AAW: Alive and Well, DOD: Dead of Disease, NED: No Evidence of Disease, TAH: Total Abdominal Hysterectomy, R: Right, L: Left, B: Bilateral, S: Salpingectomy, O: Oophorectomy, MAC: Methotrexate, Actinomycin, Alkylating Agent, BEP: Bleomycin, Etoposide, Cisplatin, PVB: Cisplatin, Bleomycin, Vinblastine, EMA: Etoposide, Methotrexate, Actinomycin, EMA/CO: Etoposide, Methotrexate, Actinomycin, Cyclophosphamide, Oncovin

Table 2. Pure NGOC cases confirmed by DNA analysis

Case

Age (years)

Reproductive Status

hCG

Surgery

FIGO Stage

Chemotherapy

Outcome

DNA analysis

 [22]

24

G1P0A1

675,713 mIU/mL

TAH, BSO, omentectomy 2 months after completion of CTx

NS

BEP x 4 cycles

NED at 1 month

DNA polymorphism analysis at 8 loci

[23]

23

G3P1

26,516 mIU/mL

Initially, removal of mass and omental biopsy

 

TAH, BSO, omental resection, pelvic lymph node dissection, appendectomy following 2 courses of BEP CTx

IIIC

BEP x 5 cycles

NED at 30 months

Histo: ovarian CC and some immature seminiferous tubulues

 

DNA polymorphism analysis with 5 STR loci

 

Karyotype analysis of peripheral blood 46XX

 

FISH confirmed absence of SRY hybridization signal in tumor; all nuclei of ovary and tumor hybridized with two XX signals

 

In testicular tissue both two XX signals (75%) and one X signal (25%)

[24]

33

G0

185,000 mIU/mL

TAH, BSO, omentectomy, pelvic lymph node dissection

NS

MAC x 4 courses

NED at 18 months

DNA polymorphism analysis using eight microsatellite markers

[25]

19

G0, virgin

 

LSO, partial omentectomy, R ovarian biopsy

IV

EMA/CO x “multiple courses”

NS

DNA polymorphism analysis of two loci

[26]

19

G0, virgin

206,949.7 mIU/mL

LSO, partial omentectomy

IA

EMA x 1 course

 

Etoposide, actinomycin x 7 courses

NED at 12 months

DNA polymorphism analysis at 15 loci

[21]

NS

G0, virgin

 

 

 

 

 

DNA polymorphism analysis at 12 loci

[21]

NS

“married”

 

 

 

 

 

DNA polymorphism analysis at 12 loci

[21]

NS

“married”

 

 

 

 

 

DNA polymorphism analysis at 12 loci

[27]

26

G0

64,000 IU/L

RSO

NS

EMA x 4 courses

DOD at 4 months

DNA polymorphism analysis at 9 loci

[28]

25

G0

NS

NS

NS

NS

NS

DNA polymorphism analysis at 11 loci

[28]

27

G0

NS

NS

NS

NS

NS

DNA polymorphism analysis at 11 loci

*See Table 1 for explanations of abbreviations.

Table 3. Possible pure NGOC cases since 1980

Case

Age (years)

Reproductive Status

hCG

Surgery

FIGO Stage

Chemotherapy

Outcome

[29]

15

G0, virgin

Urine positive x 2

 

Blood negative x 3

LSO, total omentectomy, inversion appendectomy

NS

NS

NS

[30]

10

Menarche 6 months prior to presentation

6,600 ng/mL

RSO

NS

BEP x 3 courses

NED at 62 months

[31]

12

G0, virgin

20,257 mIU/mL

LSO, partial omentectomy, multiple peritoneal biopsies

IA

BEP x 6 courses

NED at 14 months

[32]

18

G0, virgin

Urine positive

LSO, R ovarian cystectomy, omental and peritoneal biopsies

I

MAC x 4 courses

NED at 5 months

[33]

16

G0, virgin

NS

Not performed

NS

Not given

Cardiac arrest during imaging, all resuscitating measures unsuccessful

[34]

 

13

G0, virgin

Urine positive

RSO

NS

MAC x 5 courses

NED at 9 months

[21]

16

G0, virgin

NS

NS

NS

NS

NS

[35]

12

G0

1,100,000 IU/L after initial surgery

RSO, L ovarian cystectomy, omentectomy

III

BEP x 4 courses

 

High-dose CTx with carboplatin, etoposide, ifosphamide followed by BMT

NED at 3 years

*See Table 1 for explanation of abbreviations.

Table 4. Excluded citations

Reason for Exclusion

Title

Authors

Gestational choriocarcinoma

Primary choriocarcinoma of the ovary. Report of two cases

Gangadharan VP, Mathew BS, Kumar KS, Chitrathara K

Intra-operative cytodiagnosis of primary ovarian choriocarcinoma with ki67 immunoexpression

Kar A, Kar T, Mahapatra S, Dehuri P

Pure ovarian choriocarcinoma: a report of two cases

Mood NI, Samadi N, Rahimi-Moghaddam P, Sarmadi S, Eftekhar Z, Yarandi F

Ovarian choriocarcinoma arising from partial mole as evidenced by deoxyribonucleic acid microsatellite analysis

Namba A, Nakagawa S, Nakamura N, Takazawa Y, Kugu K, Tsutsumi O, Taketani Y

Pure choriocarcinoma of ovary diagnosed by fine needle aspiration cytology

Naniwadekar MR, Desai SR, Kshirsagar NS, Angarkar NN, Dombale VD, Jagtap S

Not ovarian choriocarcinoma

Genotyping Diagnosis of Nongestational Choriocarcinom Involving Fallopian Tube and Ligament: A Case Study

Buza N, Rutherford T, Hui P

Extraovarian nongestational choriocarcinoma in a postmenopausal woman

Dilek S, Pata O, Tok E, Polat A

Endometrial carcinoma in elderly women

Hoffman K, Nekhlyudov L, Deligdisch L

Primary non-gestational choriocarcinoma of the uterine cervix: a case report

Maesta L, Michelin OC, Traiman P, Hokama P, Rudge MVC

Fallopian tube choriocarcinoma presenting as ovarian tumour: a case report

Mundkur A, Rai L, Hebbar S, Guruvare S, Adiga P

Concurrent ovarian-type primary peritoneal adenocarcinoma and peritoneal choriocarcinoma. A case report and review of the literature

Pentheroudakis G, White J, Davis J, Brown I, Vasey P

 

Primary omental gestational choriocarcinoma ascertained by deoxyribonucleic acid polymorphism analysis

Sakumoto K, Nagai Y, Inamine M, Kanazawa K

Testicular choriocarcinoma metastatic to the skin: an additional case and literature review

Tinkle LL, Graham BS, Spillane TJ, Barr RJ

Primary renal artery choriocarcinoma causing secondary renovascular hypertension

Usta TA, Karacan T, Ozyurek E, Naki MM, Omeroglu SN, Demirkiran F

Pure nongestational uterine choriocarcinoma in a postmenopausal Chinese woman confirmed with short tandem repeat analysis

Wang YM, Yang YF, Teng F, Zhang HY, Xue FX

Primary choriocarcinoma of the vulva

Weiss S, Amit A, Schwartz MR, Kaplan AL

Not pure choriocarcinoma

Ovarian nongestational choriocarcinoma mixed with various epithelial malignancies in association with endometriosis

Hirabayashi K, Yasuda M, Osamura RY, Hirasawa T, Murakami M

Serous carcinoma of the endometrium with choriocarcinomatous differentiation: A case report and review of the literature indicate the existence of 2 prognostically relevant tumor types

Horn LC, Hanel C, Bartholdt E, Dietel J

Malignant mixed ovarian germ cell tumor with embryonal component

Moniaga NC, Randall LM

Nongestational choriocarcinoma arising from a primary ovarian tumour

Oladipo A, Mathew J, Oriolowo A, Lindsay I, Fisher R, Secki M, Yiannakis D

Nongestational choriocarcinoma of the ovary—a case report

Pai MR, Naik R

Postmenopausal patient

Choriocarcinoma of the ovary in a postmenopausal woman

Babu MK, Kini U

A case of non-gestational choriocarcinoma arising in the ovary of a postmenopausal woman

Park  SH, Park A, Kim JY, Kwon JH, Koh SB

Patient ≥20 years old

Primary pure ovarian choriocarcinoma mimicking ectopic pregnancy: a report of fulminant progression

Balat O, Kutlar I, Ozkur A, Bakir K, Aksoy F, Ugur MG

Primary ovarian choriocarcinoma mimicking ectopic pregnancy managed with laparoscopy--a case report

Chen YX, Xu J, Lv WG, Xie X

Pure nongestational choriocarcinoma of the ovary: a case report

Choi YJ, Chun KY, Kim YW, Ro Dy

Pure nongestational choriocarcinoma of ovary

Corakci A, Ozeren S, Ozkan S, Gurbus Y, Ustun H, Yucesoy I

Pure primary non-gestational ovarian choriocarcinoma: a diagnostic dilemma

Gon S, Majumdar B, Barui G, Karmakar R, Bhattacharya A

Management of non-gestational ovarian choriocarcinoma: laparoscopy can be essential. Report of two cases

Gremeau AS, Bourdel N, Kondo W, Jardon K, Canis M

Primary pure choriocarcinoma of the ovary

Grover V, Grover RK, Usha R, Logani KB

Leydig cell tumor, mature teratoma, and nongestational choriocarcinoma in a single ovary

Jain T, VanKessel K, Reed S, Paley P

Pure choriocarcinoma of the ovary: a case report

Lv L, Yang K, Wu H, Lou J, Peng Z

Ovarian choriocarcinoma: a difficult diagnosis of an unusual tumor and a review of the hook effect

Wheeler CA, Davis S, Degefu S, Thorneycroft IH, O’Quinn AG

Developing retroperitoneal anaplastic carcinoma with choriocarcinoma focus after ovarian nongestational choriocarcinoma: a case report

Nikolic B, Ljubic A, Terzic M, Arandjelovic A, Babic S, Vucic M

Primary pure choriocarcinoma of the ovary in reproductive ages: a case report

Simsek T, Trak B, Tunc M, Karaveli S, Uner M, Sonmez C

Primary ovarian nongestational choriocarcinoma. Report of a case in a young woman of childbearing age

Vogler C, Schmidt WA, Edwards CL

Case labeled as nongestational choriocarcinoma, but no further information of clinical context provided

Primary chemotherapy and the role of second-look laparotomy in non-dysgerminomatous malignancies of the ovary

 

Pippitt CH Jr, Cain JM, Hakes TB, Pierce VK, Lewis JL Jr

Patient <20 years old but with history of sexual activity

Pure choriocarcinoma of the ovary in Silver-Russell Syndrome

Haruma T, Ogawa C, Nishida T, Kusumoto T, Nakamura K, Seki N, Katayama T, Hiramatsu Y

Animal study

Immunohistological Description of Nongestastional Ovarian Choriocarcinoma in Two Female Mice with Conditional Loss of Trp53 Driven by the Tie2 Promoter

Castiglioni V, Ghahremani MF, Goosens S, Maglie MD, Ardizzone M, Haigh JJ, Radelli E

Non-gestational malignant placental site trophoblastic tumor of the ovary in a 4-year-old rhesus monkey

Marbaix E, Defrere S, Duc KH, Lousse JC, Dehoux JP

Cell line study/bench research/no human case study

Limitation of differential expression of HLA-A,B,C antigens on choriocarcinoma cell lines by messenger RNA for HLA heavy chain but not by beta 2-microglobulin

Kawata M, Sizer K, Sekiya S, Parnes JR, Herzenberg LA

Epidermal growth-factor receptors in human corpora-lutea during the menstrual cycle and pregnancy

Khandawood FS, Ayyagari RR, Dawood MY

Localization of the cellular expression of inhibin in trophoblastic tissue

McCluggage WG, Ashe P, McBride H, Maxwell P, Sloan JM

Establishment and properties of a human choriocarcinoma cell line of ovarian origin

Sekiya S, Kaiho T, Shirotake S, Iwasawa H, Inaba N, Kawata M, Higaki K, Ishige H, Takamizawa H, Minamihisamatsu M, Kuwata T

Usefulness of intraoperative imprint cytology in ovarian germ cell tumors

Abe A, Sugiyama Y, Furuta R, Matoda M, Takeshima N

 

The impact of molecular genetic diagnosis on the management of women with hCG-producing malignancies

Fisher RA, Savage PM, MacDermott C, Hook J, Sebire NJ, Lindsay I, Secki MJ

Published prior to 1980

Nongestational choriocarcinoma of ovary—report of a case

Dehaan QC

Primary non-gestational choriocarcinoma of the ovary. Report of a case

Panayotou PP

Author published two studies that described same case (excluded one of studies from review)

Ovarian neoplasms in children and adolescents in Papua New Guinea

Sengupta SK, Everett VJ

Review articles/book chapters

Diagnostic dilemma: non-gestational or gestational choriocarcinoma of the ovary

Bhatia K, Vaid AK

Hormonally Active Organ Tumors in Children and Adolescents

Hicks ML, Danzey TJ

Gestational Choriocarcinoma

Hui P

Recent advances in the pathology and classification of ovarian germ cell tumors

Roth LM, Talerman A

Clinical syndromes associated with ovarian neoplasms: a comprehensive review

Shanbhogue AK, Shanbhogue DK, Prasad SR, Surabhi VR, Fasih N, Menias CO

 

Germ Cell Tumors of the Ovary

Talerman A, Vang R

 

Pathology of Germ Cell Tumors

Zaloudek CJ