adult granulosa cell tumor of the ovary: fine-needle-aspiration cytology of 10 cases and review of...

Adult Granulosa Cell Tumorof the Ovary:Fine-Needle-Aspiration Cytologyof 10 Cases and Review of LiteratureSarfraz Ali, M.D.,1 Paolo Gattuso, M.D.,2 Allison Howard, M.D.,2

Marina B. Mosunjac, M.D.,1 and Momin T. Siddiqui, M.D., F.I.A.C1*

Adult granulosa cell tumor (GCT) of the ovary is mostly diag-nosed in postmenopausal women. They typically secrete estro-gen, which stimulates the endometrium to proliferate andcause abnormal bleeding. This study reviews the cytologic fea-tures of adult GCT of the ovary diagnosed by fine-needleaspiration (FNA). We reviewed slides from ten cases diag-nosed by CT guided FNA from 1995 to 2007 at our institu-tions. Smears were stained with Diff-Quik and Papanicolaoustains. Patient’s history and histologic diagnosis were alsoavailable and reviewed for all cases. The patients ranged inage from 39 to 83 yr. All 10 cases were hypercellular withboth large and small overlapping cell clusters and individualcells. The cytologic features identified included: naked nuclei(10/10 cases), Call-Exner bodies (7/10 cases), blood vesselswith prominent perivascular tumor cell growth (4/10 cases),spindle-shaped hyperchromatic stromal cells within cellularclusters (6/10 cases), mixed inflammation (3/10 cases), tumorcell necrosis (1/10 cases), and prominent metachromaticstroma seen in association with blood vessels (1/10 cases).Moderate to scant delicate cytoplasm was also seen (10/10cases). Small, punctuate cytoplasmic vacuoles were also noted(7/10 cases) and were occasionally prominent (3/10 cases). Ingeneral nuclear to cytoplasmic ratios were high althoughlower than those typically seen in a lymphoma or small-cellcarcinoma. Nuclei were generally centrally located althougheccentrically located nuclei were consistently seen in a minor-ity of cells. Nuclei were monotonous in size showing slightlyconvoluted (occasional rentiform and fetiform nuclei) to polyg-onal outlines. Prominent, central nucleoli were also seen (4/10 cases). Nuclear grooves were also seen (9/10 cases). Noatypical mitotic activity was identified in any of the 10 cases(0/10 cases). In summary, the above cytologic features can

also help in the cytologic diagnosis of adult GCTs. Diagn.Cytopathol. 2008;36:297–302. ' 2008 Wiley-Liss, Inc.

Key Words: fine-needle-aspiration; adult granulosa cell tumor;sex-cord stromal tumor

Granulosa cell tumor (GCT) of the ovary is the most

common malignant sex-cord stromal tumor. As the name

implies, GCT is derived from the granulosa cell, a hormo-

nally active part of the ovarian stroma that is responsible

for estradiol production. GCT is therefore referred to as

an ovarian sex cord-stromal tumor, and it accounts for

70% of the tumors in this category. Although they

account for a large proportion of tumors within this cate-

gory, as a group they comprise only 2–3% of all ovarian

tumors and are therefore rare in every day practice.1–4

GCT can occur at any age but most commonly presents

during the perimenopausal or early postmenopausal pe-

riod, with a median age of diagnosis between 50 and

54 yr in most series.2–7 The estimated incidence of GCT

in the United States is 0.99/100,000.2,8,9

A number of recognized risk factors have been associ-

ated with the development of GCT, although most are not

reproducible and have unknown clinical or biologic sig-

nificance. For instance, menopausal status and parity, use

of fertility drugs or oral contraceptives are not consis-

tently associated with a higher risk.6,8,10,11 Unlike epithe-

lial ovarian cancer, there seems to be no known inherited

predisposition. In particular, inherited germ line mutations

of BRCA1 or BRCA2 have not been associated thus far

with a higher risk of developing GCT.

Clinically and morphologically, two types of GCT can

be distinguished, the more frequent Adult type (Adult

Granulosa Cell Tumor, AGCT) and the Juvenile type (Ju-

venile GCT). Juvenile GCT represents only 5% of this tu-

mor type and usually occurs in prepubertal girls and

women younger than 30 years.12 An adnexal mass with or

without endocrine manifestations in a patient usually over

1Department of Pathology, Emory University Hospital, Atlanta, Georgia2Department of Pathology, Rush University Medical Center, Chicago,

Illinois*Correspondence to: Momin T. Siddiqui, M.D., F.I.A.C., Department

of Pathology and Laboratory Medicine, Emory University Hospital, 1364Clifton Road, NE, Atlanta, GA 30322.E-mail: [email protected]

Received 16 August 2007; Accepted 20 November 2007DOI 10.1002/dc.20798Published online in Wiley InterScience (www.interscience.wiley.com).

' 2008 WILEY-LISS, INC. Diagnostic Cytopathology, Vol 36, No 5 297

the age of 50 years is the usual clinical presentation.

AGCTs are hormonally active neoplasms that secrete high

levels of estrogen, which can lead to abnormal uterine

bleeding (Menorrhagia or Metrorrhagia), endometrial

hyperplasia (50–60%) and ultimately adenocarcinoma (5–

10%).5,13 Rarely, AGCTs are androgenic and patients

may present with virilization.14,15

It is clinically very important that a correct and accu-

rate diagnosis of AGCT be established. Fine-needle aspi-

ration (FNA) biopsy is by now an approved and valuable

method in the diagnosis of tumors in many organs. This

method can also be used safely in the diagnosis of ovar-

ian tumors including GCTs. Since individual clinicians

and pathologists encounter such tumors only occasionally,

we felt it worthwhile to document our experience with

the utilization of FNA in the diagnosis of AGCTs. Our

findings are presented in the light of a number of previous

studies on the cytologic features of AGCT.

Materials and Methods

A retrospective review of clinical data of AGCTs was eval-

uated through a search of pathology archives of Emory

University Hospital and Rush University Medical Center.

All cases of AGCTs which were resected, from 1995 to

2007, were reviewed. All cases were primary and proven

histologically. The diagnostic material from CT-guided

FNA on all cases was than retrieved and reviewed for eval-

uating cytological features. The smears from these cases

had been prepared by using both, 95% ethanol-fixed slides

which were stained with Papanicolaou stain, as well as by

air-drying and staining by Diff-Quik techniques.

Results

A total of 10 cases of AGCT were which were diagnosed

by FNA were available and selected for review. All 10

patients had undergone surgical resection and the subse-

quent histological diagnosis was confirmed. The age range

of all the patients was from 39 to 83 years. Two cases

were from the right ovary and eight cases were from the

left ovary.

Salient cytological features were reviewed and are sum-

marized in Table I. All 10 cases were hyper cellular with

both large and small overlapping cell clusters and individ-

ual cells (Fig. 1). Characteristic Call-Exner bodies were

present in most of the cases (Fig. 2). These bodies consist

of small rings of granulosa cells surrounding eosinophilic

fluid and basement membrane material. Blood vessels

with prominent perivascular tumor cell growth and mixed

inflammation were also noted in one third of cases

(Fig. 3). In half of the cases, spindle shaped hyperchro-

matic stromal cells within cellular clusters were present.

Ten percentage of cases showed tumor cell necrosis and

Table I. Cytomorphologic Features of AGCT Which Were Identifiedin the Cases Included in This Study

Cytologic feature of AGCT No. of cases (%)

GeneralHypercellularity 10/10 (100)Call-exner bodies 7/10 (70)Blood vessels 4/10 (40)Spindle-shaped hyperchromatic stromal cells 6/10 (60)Mixed inflammation 3/10 (30)Tumor cell necrosis 1/10 (10)Prominent metachromatic stroma 1/10 (10)Atypical mitotic activity 0/10 (0)High nuclear to cytoplasmic ratio 10/10 (100)

CytoplasmModerate to scant delicate cytoplasm 10/10 (100)Cytoplasmic vacuoles 7/10 (70)

NucleusNaked nuclei 10/10 (100)Nucleoli 4/10 (40)Nuclear grooves 9/10 (90)

Fig. 1. Low power view of fine need aspirate material from an ovarianadult granulosa cell tumor exhibiting hypercellularity with both largeand small overlapping cell clusters and individual dispersed cells (Diff-Quik stain, 3100).

Fig. 2. The tumor cells showed characteristic Call-Exner body formation(Diff-Quik stain, 3400).

ALI ET AL.

298 Diagnostic Cytopathology, Vol 36, No 5

Diagnostic Cytopathology DOI 10.1002/dc

prominent metachromatic stroma seen in association with

blood vessels. No atypical mitotic activity was identified

in any of the 10 cases. In general nuclear to cytoplasmic

ratios were high although lower than typically seen in a

lymphoma or small cell carcinoma. The cells had moder-

ate to scant delicate cytoplasm in all cases. Small, punctu-

ate cytoplasmic vacuoles were also noted and were occa-

sionally prominent in some of the cases (Fig. 4). Nuclei

which were denuded of cytoplasm (naked nuclei) were

also seen (Fig. 5). The nuclei were generally centrally

located although eccentrically located nuclei were consis-

tently seen in a minority of cells. The nuclei were monot-

onous in size and showed slightly convoluted (occasion-

ally rentiform and fetiform nuclei) to polygonal outlines,

sometimes appearing to ‘‘square off’’ especially those

with eccentric locations (Fig. 6). Prominent central nucle-

oli were also occasionally found. Nuclear grooves were

also seen in 90% of cases and ranged in prominence. In

addition subjective scoring was assigned to the presence

of nuclear grooves and is summarized in Table II.

Discussion

Ovarian cancer accounts for about 3% of all cancers

among women and ranks second among gynecologic can-

cers, following cancer of the uterine corpus.16 In recent

Fig. 3. A blood vessel with prominent tumor cell growth is identifiedhere. The background also shows naked nuclei as well as scattered lym-phocytes (Diff-Quik stain, 3200).

Fig. 4. Small, punctuate cytoplasmic vacuoles were also noted and wereoccasionally prominently present in some cells (Diff-Quik stain, 3400).

Fig. 5. A high power view of individual nuclei with denuded of cyto-plasm along with lymphocytes (Diff-Quik stain, 3600).

Fig. 6. The nuclei are monotonous in size and show slightly convolutedto polygonal outlines. Nuclear grooves are also identified in numerouscells (Diff-Quik stain, 3600).

Table II. Distribution and Presence of Nuclear Grooves in the TumorCells of the Cases Studied

Nuclear groove score No. of cases, %

1+ (within occasional cell clusters) 3/9, 332+ (within few cell clusters) 3/9, 333+ (within every cell cluster) 3/9, 33

ADULT GCT OF THE OVARY

Diagnostic Cytopathology, Vol 36, No 5 299


years, incidence of ovarian cancer has declined by 0.7%.

However, *22,000 new cases of ovarian cancer will still

be diagnosed in the United States in 2007.16 These malig-

nancies will also account for more than 14,000 deaths in

the United States this year.16

GCTs are relatively rare functional neoplasms of the

ovary. These tumors are regarded as malignancies,

although of a low-grade type. Most GCTs (70–90%) are

pathologic Stage I disease at diagnosis.5,8,17–19 Although

patients with AGCT present with early-stage disease,

relapses tend to occur in a more indolent fashion, often

many years after the original diagnosis.20,21 Patients with

GCT require long-term clinical follow-up because of the

known, yet unpredictable, recurring or metastasizing

behavior many years after a disease-free interval even in

those with Stage I or Stage II tumor at diagnosis.22,23

It is also important to know that AGCT are usually

diagnosed during child bearing years, however the age

range is broad since they sometimes occur before puberty

or even after menopause.1 A majority of these tumors are

associated with hyperestrinism, which leads to excessive

estrogen production, leading to isosexual precocious pu-

berty in children and to metrorrhagia in adults, including

women in the postmenopausal age group.10 However,

some of the cases are hormonally inactive at the clinical

level, and very rarely androgenic.14,15

The concept of prognosis for AGCT is also of interest.

A number of clinical, pathologic, and molecular prognos-

tic factors have been proposed for AGCT, although the

reproducibility of many factors has been difficult to estab-

lish. More than 75% of GCTs are diagnosed as Interna-

tional Federation of Gynecology and Obstetrics (FIGO)

stage I and only 6% are stage IV.17 Stage of Granulosa

tumor is clearly the most important prognostic factor.6,8,18

The reported 5-year survival rate for patients with stage I

disease ranges from 75 to 95%.5,18 This contrasts with the

55–75% 5-year survival rate for patients with stage II

tumors and the 22–50% survival rate for stage III/IV can-

cers,7,8,19 demonstrating the potential for late relapse and

death in patients with advanced disease. Although AGCT

has been considered to be of low-grade malignancy, 10–

50% of the patients develop recurrences presenting as late

as 20 to 30 years after initial diagnosis.21 A number of

pathologic and molecular factors have also been evaluated

for their prognostic significance. Fujimoto et al., evaluated

several histopathologic variables including stage, p53 sta-

tus, histologic pattern with or without Call-Exner bodies,

mitotic index (MI), and lymphovascular space invasion.19

In this report, only MI and lymphovascular space invasion

were independent prognostic factors. In particular,

patients who experienced a relapse had a significantly

higher MI (median, five mitoses/10 HPF) than those with-

out recurrence (median, 1.5 mitoses/10 HPF; P < 0.001).

Furthermore, the disease-free survival rate at 80 months

for patients with tumors containing fewer than four mito-

ses/10 HPF was 90%, compared with 25% for patients

whose tumors demonstrated four or more mitoses/10 HPF

(P < 0.0005). Other studies however, have not found a

convincing association between MI and prognosis.18,24

Morphologically, different growth patterns can be

observed in AGCT: microfollicular (most frequent), mac-

rofollicular, trabecular, insular, solid-tubular, gyriform,

and diffuse (sarcomatoid). FNA cytology is a well estab-

lished technique for the diagnosis of various neoplastic

and non-neoplastic ovarian masses.25,26 Angstrom et al.,

has reported an accuracy rate of over 90% in benign and

malignant ovarian neoplasms diagnosed by FNA cytol-

ogy.25 In addition, Sevin et al., has reported a sensitivity

of greater than 90% in diagnosing malignant ovarian neo-

plasms by FNA.26 It was the purpose of this study to

review the cytologic features of AGCT which had been

diagnosed by FNA.

The cytological features described in the literature are

quiet distinctive, such as monotonous cells, microfollicu-

lar pattern, and nuclear grooves. We found all of these

characteristic features in AGCT cells demonstrated by

FNA in our study. All of the 10 cases exhibit microfollic-

ular cell pattern. The tumor cells were relatively monoto-

nous, with nuclear grooves in almost all cell nuclei (90%)

in our study. Call-Exner bodies have been demonstrated

in 30–60% of cases of AGCT.4,9,24 We observed Call-

Exner bodies in more than two thirds (70%) of our cases.

The distinct nuclear appearance is one of the hallmark

features of ovarian AGCT. AGCT tumor nuclei are typi-

cally uniform and pale and are often grooved (nuclear

grooves) giving them a ‘‘coffee-bean’’ appearance. We

detected nuclear grooves in 9 of the 10 cases studied,

however the number of cells exhibiting this nuclear fea-

ture was variable (Table II). Conflicting data exist about

the presence of nucleoli in AGCTs. Aboud et al., and

others demonstrated in their studies that nucleoli were

absent in AGCT cells.20,27–29 In contrast to these reports,

nucleoli have been observed in AGCT cells in some other

studies.21,30,31 In our study, we were able to detect promi-

nent nucleoli in only 4 of 10 cases.

Nuclear grooves being one of the classic features of

AGCT need to be discussed further since this feature is

not exclusive to this tumor alone. Proliferating Brenner

Tumor and Sex Cord Tumor with Annular Tubules

(SCTAT) are two other primary ovarian tumors that are

characterized by the presence of prominent nuclear

grooves which are indistinguishable on the basis of cytol-

ogy alone. These three ovarian tumors are all composed

of sheets and trabecular structures lined by a pseudostrati-

fied layer of relatively monotonous cells with the so-

called coffee-bean-shaped nuclei. Proliferating Brenner

Tumor and SCTAT have small nucleoli, which can be

helpful in differentiating from AGCT.32,33 Immunohisto-

ALI ET AL.



chemistry, as demonstrated by some studies, can also be

useful in the differential diagnosis since AGCT is immu-

noreactive for Inhibin and CD99.34,35 The epithelial nests

of Brenner tumor are immunoreactive for cytokeratin and

epithelial membrane antigen, which can help in the diag-

nosis. SCTAT is mainly differentiated on the basis

rosettes, with or without a central acellular core compris-

ing of basement membrane material.33 The rosettes

observed in SCTAT are three dimensional with greater

cellularity than that seen in Call-Exner bodies of AGCT.

In addition, the luminal material in Call-Exner bodies is

less defined than in the rosettes of SCTAT.33

Occasionally, AGCT with a diffuse pattern can be mis-

taken for a poorly differentiated carcinoma. The nuclear

appearance can be very helpful for differentiating the two

entities.36 AGCT nuclei are normally uniform and pale

and are often grooved, whereas the nuclei of undifferenti-

ated carcinomas are often hyperchromatic, without

grooves, and unequal in size and shape.36 Nuclear atypia

and multiple mitotic figures are also less common in

AGCT, as in our study. These two features are frequently

observed in undifferentiated carcinomas.36,37 For difficult

cases, immunohistochemistry staining for epithelial mem-

brane antigen and inhibin may be useful, where AGCT

would be epithelial membrane antigen-negative and

inhibin-positive, whereas carcinoma would exhibit the

reverse pattern.38,39

To conclude, AGCTs may create a diagnostic challenge

in cytologic preparations because of its rarity. We have

studied only a few cases of AGCT by FNA. The most con-

sistent features of AGCTs in cellular aspirates include

cohesion and discohesion, naked nuclei and nuclear

grooves. The findings of admixed hyperchromatic spindle-

shaped stromal cells and blood vessels can also help sup-

port the cytologic diagnosis of adult GCT. We feel that the

cytologic picture of GCTs is fairly characteristic and

includes specifically monotonous cells, nuclear grooves

and Call-Exner bodies. The distinguishing cytologic picture

in FNA preparation should, together with the clinical find-

ings, lead to a correct preoperative diagnosis of adult GCT.

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