Case Reports in Urology
Volume 2019 (2019), Article ID 7156154, 10 pages
https://doi.org/10.1155/2019/7156154

Case Report

Adult Granulosa Cell Tumor of the Testis: A Case Report with a Review of the Literature

Klaus-Peter Dieckmann,¹ Julia Bertolini,² and Christian Wülfing¹

¹Asklepios Klinik Altona, Abteilung Urologie/Hodentumorzentrum, Hamburg, Germany
²MVZ Hanse Histologikum, Hamburg, Germany

Correspondence should be addressed to Klaus-Peter Dieckmann; dieckmannkp@t-online.de

Received 9 February 2019; Accepted 7 May 2019; Published 19 May 2019

Academic Editor: Nicola Zampieri

Copyright © 2019 Klaus-Peter Dieckmann et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Adult granulosa cell tumor (AGCT) of the testis represents a very rare testicular neoplasm that is poorly understood clinically. Here we report the case of a 22-year-old male who presented with unspecific scrotal symptoms. Scrotal sonography disclosed a 6 mm hypoechoic intratesticular lesion. Histological examination after orchiectomy revealed a homogeneous and well demarcated neoplasm with monomorphic cells with nuclear grooving and microfollicular formation of the so-called Call-Exner bodies. Immunohistology showed positive stainings of vimentin, calretinin, and inhibin with negative stainings of the typical germ cell tumor markers. Thus, the diagnosis of a benign AGCT was made. The patient is well one year after surgery. A total of 91 previous AGCT cases were identified in the literature. Median age of the cases reported to date is 44 years, median tumor size 3.2 cm. 54.3% of the AGCT cases were located on the left side. 12 cases (13.2%) were of malignant nature. Testis-sparing surgery would be the treatment of choice, but only two of all cases had received that procedure. The present report aims to increase the clinical knowledge of AGCT and specifically to increase the clinician’s vigilance with respect to testis-sparing surgery in probably benign testicular masses.

1. Introduction

Histologically, about 90% of all testicular neoplasms comprise germ cell tumors (GCTs) while the remainder involves sex cord gonadal stromal tumors, malignant lymphomas, secondary tumors, and other very rare new growths [1, 2]. Among the gonadal stromal tumors, Leydig cell tumors and Sertoli cell tumors are the most common subtypes encompassing 1-2% and 0.5%, respectively, of all testis tumors [3]. The third subtype is the granulosa cell tumor which represents a truly rare neoplasm. Granulosa cell tumors arising in the testis are histologically identical with their ovarian counterparts. With respect to the pathogenesis of these unusual testicular neoplasms, Teilum postulated that cells of the male gonadal stroma retain their embryological ability to differentiate into both male or female specialized stromal cells, i.e., Leydig or Sertoli cells and granulosa or theca cells, respectively [4]. Thus, in the case of neoplastic growth of gonadal stromal cells the tumor cell types of both genders may evolve. Regarding granulosa cell tumors, two subtypes must be considered, the juvenile type occurring only in the first year of life and the adult type occurring later in life [5]. The clinical behavior of gonadal stromal tumors and particularly that of the adult granulosa cell tumor (AGCT) is poorly understood so far. The overall experience rests on a few small case series [6] and predominantly on single case reports [7]. The aim of the present report is to document another case of AGCT and to summarize the knowledge regarding this rare tumor.

2. Case Presentation

This 22-year-old man of European descent presented with unspecific scrotal discomfort lasting for two weeks. Clinical history is uneventful. The patient is unmarried and has no children so far. He is an untrained workingman by profession. Both testicles were of normal size and nonsuspicious upon palpation with only some tenderness on the left scrotal side. Scrotal sonography revealed a 1 cm sized lobulated hypoechoic lesion at the cranial pole of the left testis (Figure 1(a)) showing intense color duplex signals within the lesion (Figure 1(b)). Laboratory workup disclosed no abnormal results. Specifically, the germ cell tumor markers alpha fetoprotein, beta-human chorionic gonadotropin, and lactate dehydrogenase were within normal limits, as were the serum testosterone level (6.57 ng/ml; reference limits 2.4–8.7) and the gonadotropins LH (1.69 U/l) and FSH (2.78 U/l). Upon surgical exploration, a well circumscribed greyish-tan lesion of about 1 cm in size was identified at the cranial pole. Inguinal radical orchiectomy with placement of a silicone testicular implant and contralateral testicular biopsy were performed accordingly. The postoperative course was uneventful. Computed tomography of chest and abdomen did not reveal any metastases. No further treatment was applied. The patient is well and without recurrence of the disease one year after surgery.

(a)

(b)

Figure 1: (a) Sonographic appearance of the adult granulosa cell tumor in the 22-year-old patient. Note the lobulated but well circumscribed shape and homogeneous hypoechoic appearance. (b) The same patient, color-coded duplex sonography showing duplex signals within the hypoechoic lesion.

Pathohistological analysis showed a well demarcated solid neoplasm of 8 mm in size (Figure 2(a)). Histologically, the lesion consisted of monomorphic cells resembling typical ovarian granulosa cells. Many of the cells had large nuclei with many of them having a grooved shape mirroring the appearance of coffee beans (Figure 2(b)). The growth pattern was solid in most parts of the neoplasm but in some areas microfollicular structures prevailed resembling Call-Exner bodies (Figure 3). Mitotic figures were very rare. No necrotic areas were detected. The tumor-surrounding testicular tissue showed normal spermatogenesis. Germ cell neoplasia in situ was detected neither in the ipsilateral parenchyma nor in the contralateral testicular tissue. Immunohistochemical workup revealed positive staining of inhibin, vimentin, and calretinin (Figure 4) and negative staining for Oct 4 and chromogranin A. Staining of progesterone receptor was negative, too. The MIB-1 labeling index revealed a growth fraction of 1%. The histopathological findings were thus consistent with the diagnosis of a benign adult type granulosa cell tumor of the testis.

(a)

(b)

Figure 2: (a) Histological section of the neoplasm, hematoxylin-eosin stain. Well demarcated rim of the testicular neoplasm, no clear encapsulation. Normal testicular parenchyma, upper part of image. 10x magnification. (b) Histological section of the neoplasm. The tumor cells have scant cytoplasm and elongated nuclei with numerous grooves (arrow). Hematoxylin-eosin stain, magnification x20.

Figure 3: Histological section of the tumor. Adult granulosa cell tumor with microfollicular pattern. Call-Exner body: coffee bean-like tumor cells with groove core notches surrounding glandular cavities containing eosinophilic material and tumor cells detached from the dressing (arrows). Hematoxylin-eosin stain, 10x magnification.

Figure 4: Immunohistological stain of calretinin. All neoplastic cells stain positive for calretinin, 10x magnification.

3. Literature Survey

A total of 91 cases could be identified from the literature by using the PUBMED database and by hand-searching the reference lists of previous reports (Table 1). Not all of the case reports specified details regarding all of the clinical characteristics. Therefore, the various clinical features had to be analyzed with different sample sizes. With regard to age, 86 cases are eligible and the median age is 44 years (interquartile range (IQR) 26–55 years; range 12–87 years). With regard to tumor size, 80 cases are evaluable, with the median size amounting to 3.2 cm (IQR 1.5–5.0 cm; range 0.5–18.0 cm). Laterality is specified in 81 reports showing a slight preponderance of the left side with 44 cases (54.3 %; 95% confidence intervals (CIs) 42.9–65.4%) as opposed to 37 cases located on the right side (45.7%, 95% CI 34.6–57.1%). Malignancy was documented in 12 cases (13.2%) with 4 of these cases surviving more than 2 years. Endocrine symptoms were not systematically documented, but gynecomastia was reported in 8 cases. With regard to primary treatment, orchiectomy was the standard therapy. Only two cases had testis-sparing surgery.

Table 1: Synopsis of cases with adult granulosa cell tumor of the testis reported in 1953–2018.

Author (first)
year
reference ()
age (years)
tumor size (cm)
right side
malignant
presenting symptom
endocrine symptoms
F/U

Laskowski
1952
[8]
35
9,00
R

gynecomastia
8,5 yrs

Cohen
1953
[9]
21
<1 cm
L

incidental
gynecomastia
ns

Massachusetts case
1955
[7]
53
10 cm
R

gynecomastia
ns

Melicow
1955
[10]
52
13,00
R

ns

Mostofi
1959
[11]
41
10,10
L
malignant

gynecomastia
DOD 5 m

Marshall
1977
[12]
53
10,00
ns

mass, no pain
gynecomastia
17 yrs

Talerman
1985
[13]
44
3,50
R

mass, no pain

3 yrs

Gaylis
1989
[14]
41
1.8 cm
R

ns

Düe
1990
[15]
83
18 cm
L

mass, no pain

DOC 1 m

Nistal
1992
[16]
61
5,00
R

ns

Matoska
1992
[17]
26
10,00
L
malignant
painful mass
gynecomastia
14 yrs NED

Sasano
1992
[18]
ns
ns
ns

ns

Monobe
1992
[19]
42
ns
L
malignant

AWD

Jiminez-Quintero
1993
[20]
57
2,50
R

3y DOC

Jiminez-Quintero
1993

55
1,30
L

ns

Jiminez-Quintero
1993

60
7,00
L
malignant

DOD 11 yrs

Jiminez-Quintero
1993

39
4,00
L

3 yrs NED

Jiminez-Quintero
1993

29
7,50
R
malignant

Jiminez-Quintero
1993

76
0,70
L

NED 1 m

Renshaw
1997
[21]
ns
ns
ns

ns

Renshaw
1997

ns
ns
ns

ns

Renshaw
1997

ns
ns
ns

ns

Morgan
1999
[22]
49
2,60
L

2 yrs NED

Al-Bozom
2000
[23]
48
5,00
R

7 m NED

Wang
2002
[24]
54
ns
L

hydrocele, asymptomatic

ns

Guzzo
2004
[25]
33
1,00
L

ns

Suppiah
2005
[26]
51
ns
L
malignant

6 yrs AWD

Hisano
2006
[27]
59
15,00
L

4 yrs NED

Arzola
2006
[28]
32
2,10
L

painless mass

Lopez
2007
[29]
77
4,00
L

ns

Ditonno
2007
[30]
45
6,50
R

painless mass

2 yrs NED

Gupta
2008
[31]
12
8,00
L

1 yr NED

Hammerich
2008
[32]
55
ns
ns
malignant

3 yrs NED

Song
2011
[33]
28
2,60
L

ns

Hanson
2011
[34]
21
1,00
L

2 yrs NED

Lima
2012
[35]
77
2,50
R

ns

Lima
2012

22
1,00
L

ns

Lima
2012

40
2,10
L

Schubert
2014
[7]
78
1,3
L

painless mass

23 m NED

Cornejo
2014
[6]
49
3,00
R

137 m, DOOD

Cornejo
2014

22
3,30
L

48 m

Cornejo
2014

50
0,90
L

59 m

Cornejo
2014

ns
3,00
L

lost

Cornejo
2014

27
1,80
R

60 m

Cornejo
2014

87
ns
ns

169 m

Cornejo
2014

47
4,50
R

lost

Cornejo
2014

51
2,10
R

58 m

Cornejo
2014

47
0,50
L

lost

Cornejo
2014

55
2,10
L

80 m

Cornejo
2014

25
2,00
R

lost

Cornejo
2014

45
1,40
R

lost

Cornejo
2014

74
3,50
L

104 m

Cornejo
2014

27
1,40
R

36 m

Cornejo
2014

32
4,20
R

lost

Cornejo
2014

18
3,20
L

lost

Cornejo
2014

60
6,00
R

lost

Cornejo
2014

23
1,40
R

65 m

Cornejo
2014

20
4,50
L

1 m

Cornejo
2014

52
4,30
R
malignant

24 m AWD

Cornejo
2014

14
0,80
R

lost

Cornejo
2014

21
3,00
R

37 m

Cornejo
2014

17
1,50
R

lost

Cornejo
2014

64
2,40
R

28 m

Cornejo
2014

14
3,50
R

35 m

Cornejo
2014

28
2,60
L

lost

Cornejo
2014

51
3,00
L

lost

Cornejo
2014

63
1,00
L

25 m

Cornejo
2014

25
5,50
R

1 m

Cornejo
2014

44
1,20
L

1 m

Cornejo
2014

50
4,70
R

1 m

Köksal
2003
[36]
40
3,50
R

8-month mass
no
20 m

Mitra
2008
[37]
25
0,50
L

scrotal pain 2 weeks

ns

Kucukodaci
2008
[38]
21
1,50
L

incidental
no
1 yr

Harrison
2009
[39]
65
5,00
L
malignant

DOD

Miliaris
2013
[40]
37
4,20
L

painless mass
no
2 yrs

Norman
2013
[41]
68
ns
R

18 m

Rane
2014
[42]
34
5,00
R

6 m

Rane
2014

46
65,00
L

2,5 yrs

Rane
2014

46
11,00
R
malignant

3 m

Tanner
2014
[43]
22
0,60
L

ns

Tsitouridis
2014
[44]
29
2,50
R

1 yr

Giulianelli
2015
[45]
80
6,00
R

mass, no pain
gynecomastia
1 yr

Vallonthaiel
2015
[46]
43
6,00
L

painless mass

1 yr

Gomez-Valcarcel
2016
[47]
23
ns
ns

ns

Mohapatra
2016
[48]
57
4,7
L
malignant
incidental
gynecomastia
32 m NED

Al-Alao
2016
[49]
48
1,20
L

ns

Bani
2016
[50]
20
2,00
R

4 m NED

Elbachiri
2017
[51]
40
5,50
L
malignant
painless growing mass

2 yrs NED

Mezentsev
2017
[52]
74
5,00
R

painless mass

ns

Meilan
2017
[53]
59
3,30
ns

ns

Nunes-Carneiro
2017
[54]
31
4,50
ns

10 yrs

As cited by Schubert et al. 2014.

Ns: not stated.

NED: no evidence of disease; DOD: dead of disease; DOC: dead of complication; AWD: alive with disease; DOOD: dead of other disease.

yrs: years; m: months.

R: right side; L: left side; F/U: follow-up.

4. Discussion

The first documentation of an AGCT is credited to Laskowski in 1952 [8]. By the year 2000, another 28 cases had been reported. In 2014, Schubert et al. summarized 43 cases of the literature [7]. In the same year, Cornejo et al. published the largest consecutive series of 32 patients [6]. Isolated cases not quoted by Schubert [36–39] and several cases documented since 2014 bring the total number to 91 cases reported to date (Table 1). Some more cases are briefly mentioned without providing details in several case series on gonadal stromal tumors [3, 55–57]. Thus, the total number of cases referred to in the medical literature is probably more than one hundred. And as a matter of fact, a large number of cases remained unreported. The number of documented cases has apparently increased since the year 2000. However, this statistical trend does probably not indicate a true increase of the incidence of AGCT but rather reflects a lower rate of misclassification of this rare entity because of increasing knowledge regarding testicular tumors [58]. One additional factor could be publication bias because the possibilities of publishing minor reports have much improved since the beginning of this century because of the ever increasing number of Internet-based scientific journals.

The age of the present patient is 22 years which is clearly lower than the median age of 44 years and even lower than the inter quartile range (26 -55 years) as observed in the literature survey. The lowest age ever observed in AGCT is 12 years [31] while the oldest subject is aged 87 years [6].

The tumor size of 8 mm found in our case is clearly smaller than the median size of 3.2 cm observed in the literature survey and it lies in the lowest quartile of reported findings. Obviously, granulosa cell tumors of the adult type may occur with a wide variety of sizes since seven cases with tumor sizes of less than 1 cm were reported (Table 1) and on the other side there were at least eight patients with giant tumors sized >10 cm. The median size of AGCT is very similar to the sizes of 3.2–3.5 cm and 2.8–3.5 cm found in nonseminomatous and seminomatous germ cell tumors, respectively [59, 60]. Probably, the presenting size of different histological types of testicular tumors does not relate to biological reasons but rather to sensual-cognitive structures of patients. Putatively, a diameter of around 3 cm represents the threshold where the majority of men will recognize a mass in the testicle. Most of the patients with AGCT presented with slowly growing painless testicular masses with several of whom reporting a duration of symptoms for many years [7, 22, 30]. On the other hand, eight cases were sized <1cm that were found incidentally upon autopsy [9] or with ultrasonography [25, 43]. Overall, a palpable mass is probably the typical presenting symptom of AGCT as it is with testicular germ cell tumors [6, 38, 45]. Endocrine-related symptoms were infrequently reported in previous cases, but eight patients of the survey were reported to present with gynecomastia. This symptom is not specific for AGCT because it is frequently observed in Leydig cell tumors and sometimes also in beta-human chorionic gonadotropin secreting germ cell tumors [61]. Our patient presented with unspecific scrotal symptoms that were not related to the tiny testicular tumor that was only detected with ultrasonography. Sonographic features were frequently reported and typically involve hypoechoic well circumscribed masses with positive color-coded sonographic signals [37, 49]. But anechoic areas corresponding to cystic parts of the tumor have also been observed [7, 52].

Regarding laterality of AGCT, our patient presented with a left sided tumor which corresponds to the findings in the majority of cases of the survey where 54.3% (95% CI 42.9–65.4%) had left sided tumors as opposed to 45.7% (95% CI 34.6–57.1%) right sided tumors. However, in view of the overall small database and overlapping confidence intervals of the proportions there is probably no clear evidence for a predisposition of one side. The same is true with germ cell tumors where no clear preponderance of one particular side has been found [59].

The neoplasm detected in our patient was a clearly benign lesion. Among the 91 cases listed in the survey, 12 were malignant (13.2%). A 15% proportion of malignancy was likewise reported by Rove et al. [57] and two additional malignant cases were briefly mentioned by Featherstone et al. [56]. Reportedly, clinical features of malignancy involve tumor size > 5 cm and age > 50 years [34, 57]. Histologically, >3 mitoses per high-power field, invasion of rete testis, vascular invasion, and cellular atypia are considered as characteristics of malignancy [51, 58].

Histologically, AGCT consist of monomorphic cells identical with ovarian granulosa cells with a scanty cytoplasm. Many of the cells may show coffee bean-like nuclei with small grooves [6, 45]. The cells are mostly arranged in trabeculae and sheets and some may form microfollicular structures, the so-called Call-Exner bodies [62]. The histological diagnosis mainly rests on immunohistochemical findings with positive stainings of inhibin, vimentin, and calretinin and negative stainings for pancytokeratin and the typical germ cell tumor specific markers like placental alkaline phosphatase, D2-40, and Oct 3/4 [7, 18, 20, 21, 62].

With regard to treatment, testis-sparing surgery would be the treatment of choice, as only few cases are malignant. As age >50 years and tumor size are the most important characteristics of malignancy the cases qualifying for conservative surgery could in principle be easily identified, preoperatively.

Hence, only two of the cases of the survey received that appropriate therapy and also the present case was submitted to orchiectomy. Clearly, in everyday clinical practice it is difficult to sort out benign tumors from malignant ones by means of clinical assessment only. As malignant tumors of the testis are far more common than benign growths most of the urologic surgeons will proceed to radical orchiectomy. However, as shown in the present case and in many cases of the survey, benign tumors of the testis do actually occur, and small size is one of the leading characteristics of benign nature though not specific. The present case report is thought to increase the overall knowledge of testicular granulosa cell tumors, and it particularly aims to increase the vigilance of urologic surgeons to consider conservative surgery in cases with small testicular neoplasms. Practically, a conservative approach with intraoperative frozen section examination could help to save more testicles and avoid unnecessary orchiectomies.

Consent

Written consent was obtained from the patient for publication of this report and accompanying images.

Conflicts of Interest

They authors declare that none has any potential conflicts of interest with publishing this report.

References

H. M. Rosevear, A. Mishail, Y. Sheynkin, and M. Wald, “Unusual scrotal pathology: an overview,” Nature Reviews Urology, vol. 6, no. 9, pp. 491–500, 2009.

S. R. Williamson, B. Delahunt, C. Magi-Galluzzi et al., “The World Health Organization 2016 classification of testicular germ cell tumours: a review and update from the International Society of Urological Pathology Testis Consultation Panel,” Histopathology, vol. 70, no. 3, pp. 335–346, 2017.

D. S. Conkey, G. C. W. Howard, K. M. Grigor, D. B. McLaren, and G. R. Kerr, “Testicular sex cord-stromal tumours: the Edinburgh experience 1988-2002, and a review of the literature,” Clinical Oncology, vol. 17, no. 5, pp. 322–327, 2005.

G. Teilum, Special tumors of ovary and testis and related extragonadal lesions, Munksgaard, Copenhagen, Denmark, 2nd edition, 1976.

L. M. Roth, B. Lyu, and L. Cheng, “Perspectives on testicular sex cord-stromal tumors and those composed of both germ cells and sex cord-stromal derivatives with a comparison to corresponding ovarian neoplasms,” Human Pathology, vol. 65, pp. 1–14, 2017.

K. M. Cornejo and R. H. Young, “Adult granulosa cell tumors of the testis: A report of 32 cases,” The American Journal of Surgical Pathology, vol. 38, no. 9, pp. 1242–1250, 2014.

T. E. O. Schubert, R. Stoehr, A. Hartmann, S. Schöne, M. Löbelenz, and G. Mikuz, “Adult type granulosa cell tumor of the testis with a heterologous sarcomatous component: case report and review of the literature,” Diagnostic Pathology, vol. 9, article 107, 2014.

J. Laskowski, “Feminizing tumours of testis; general review with case report of granulosa cell tumour of testis,” Endokrynologia Polska, vol. 3, pp. 337–343, 1952.

J. Cohen and J. Diamond, “Leontiasis ossea, slipped epiphyses and granulosa cell tumor of the testis with renal disease,” Archives of Pathology & Laboratory Medicine, vol. 56, pp. 488–500, 1953.

M. M. Melicow, “Classification of tumors of testis: a clinical and pathological study based on 105 primary and 13 secondary cases in adults, and 3 primary and 4 secondary cases in children,” The Journal of Urology, vol. 73, no. 3, pp. 547–574, 1955.

F. K. Mostofi, E. A. Theiss, and D. J. B. Ashley, “Tumors of specialized gonadal stroma in human male patients. Androblastoma, sertoli cell tumor, granulosa‐theca cell tumor of the testis, and gonadal stromal tumor,” Cancer, vol. 12, no. 5, pp. 944–957, 1959.

F. F. Marshall, W. S. Kerr Jr., B. Kliman, and R. E. Scully, “Sex cord stromal (gonadal stromal) tumors of the testis: a report of 5 cases,” The Journal of Urology, vol. 117, no. 2, pp. 180–184, 1977.

A. Talerman, “Pure granulosa cell tumour of the testis. report of a case and review of the literature,” Applied Pathology, vol. 3, no. 3, pp. 117–122, 1985.

F. D. Gaylis, C. August, A. Yeldandi, A. Nemcek, and J. Garnett, “Granulosa cell tumor of the adult testis: Ultrastructural and ultrasonographic characteristics,” The Journal of Urology, vol. 141, no. 1, pp. 126-127, 1989.

W. Düe, K.-P. Dieckmann, G. Niedobitek, G. Bornhoft, V. Loy, and H. Stein, “Testicular sex cord stromal tumour with granulosa cell differentiation: detection of steroid hormone receptors as a possible basis for tumour development and therapeutic management,” Journal of Clinical Pathology, vol. 43, no. 9, pp. 732–737, 1990.

M. Nistal, R. Lázaro, J. García, and R. Paniagua, “Testicular granulosa cell tumor of the adult type,” Archives of Pathology & Laboratory Medicine, vol. 116, pp. 284–287, 1992.

J. Matoška, D. Ondruš, and A. Talerman, “Malignant granulosa cell tumor of the testis associated with gynecomastia and long survival,” Cancer, vol. 69, no. 7, pp. 1769–1772, 1992.

H. Sasano, N. Nakashima, O. Matsuzaki et al., “Testicular sex cord-stromal lesions: Immunohistochemical analysis of cytokeratin, vimentin and steroidogenic enzymes,” Virchows Archiv A Pathological Anatomy and Histopathology, vol. 421, no. 2, pp. 163–169, 1992.

Y. Monobe and T. Manabe, “Malignant sex-cord stromal tumor of the testis: report of a case with special reference to its unusual intracytoplasmic substructures,” Japanese Journal of Clinical Oncology, vol. 22, no. 6, pp. 414–420, 1992.

L. P. Jimenez-Quintero, J. Y. Ro, A. Zavala-Pompa et al., “Granulosa cell tumor of the adult testis: a clinicopathologic study of seven cases and a review of the literature,” Human Pathology, vol. 24, no. 10, pp. 1120–1126, 1993.

A. A. Renshaw, M. Gordon, and C. L. Corless, “Immunohistochemistry of unclassified sex cord-stromal tumors of the testis with a predominance of spindle cells,” Modern Pathology, vol. 10, no. 7, pp. 693–700, 1997.

D. R. Morgan and K. G. Brame, “Granulosa cell tumour of the testis displaying immunoreactivity for inhibin,” BJU International, vol. 83, no. 6, pp. 731-732, 1999.

I. A. Al-Bozom, S. R. El-Faqih, S. H. Hassan, and A. E. El-Tiraifi, “Granulosa cell tumor of the adult type: a case report and review of the literature of a very rare testicular tumor,” Archives of Pathology & Laboratory Medicine, vol. 124, pp. 1525–1528, 2000.

B. Y. Wang, D. S. Rabinowitz, R. C. S. Granato, and P. D. Unger, “Gonadal tumor with granulosa cell tumor features in an adult testis,” Annals of Diagnostic Pathology, vol. 6, no. 1, pp. 56–60, 2002.

T. Guzzo, M. Gerstein, and J. H. Mydlo, “Granulosa cell tumor of the contralateral testis in a man with a history of cryptorchism,” Urologia Internationalis, vol. 72, no. 1, pp. 85–87, 2004.

A. Suppiah, M. M. Musa, D. R. Morgan, and A. D. North, “Adult granulosa cell tumour of the testis and bony metastasis: a report of the first case of granulosa cell tumour of the testicle metastasising to bone,” Urologia Internationalis, vol. 75, no. 1, pp. 91–93, 2005.

M. Hisano, F. M. Mascarenhas Souza, D. M. A. Costa Malheiros, A. C. Lima Pompeo, and A. M. Lucon, “Granulosa cell tumor of the adult testis. Report of a case and review of the literature,” Clinics, vol. 61, no. 1, pp. 77-78, 2006.

J. Arzola, R. L. Hutton, S. M. Baughman, and R. V. Mora, “Adult-type testicular granulosa cell tumor: Case report and review of the literature,” Urology, vol. 68, no. 5, pp. 1121.e13–1121.e16, 2006.

J. I. López, “Adult-type granulosa cell tumor of the testis. report of a case,” Tumori, vol. 93, no. 2, pp. 223-224, 2007.

P. Ditonno, G. Lucarelli, M. Battaglia et al., “Testicular granulosa cell tumor of adult type: a new case and a review of the literature,” Urologic Oncology: Seminars and Original Investigations, vol. 25, no. 4, pp. 322–325, 2007.

A. Gupta, S. Mathur, C. Reddy, and B. Arora, “Testicular granulosa cell tumor, adult type,” Indian Journal of Pathology and Microbiology, vol. 51, no. 3, pp. 405-406, 2008.

K. H. Hammerich, S. Hille, G. E. Ayala et al., “Malignant advanced granulosa cell tumor of the adult testis: case report and review of the literature,” Human Pathology, vol. 39, no. 5, pp. 701–709, 2008.

Z. Song, D. J. Vaughn, and Z. Bing, “Adult type granulosa cell tumor in adult testis: report of a case and review of the literature,” Rare Tumors, vol. 3, no. 4, article e37, pp. 117–119, 2011.

J. A. Hanson and A. B. Ambaye, “Adult testicular granulosa cell tumor: a review of the literature for clinicopathologic predictors of malignancy,” Archives of Pathology & Laboratory Medicine, vol. 135, pp. 143–146, 2011.

J. F. Lima, L. Jin, A. R. de Araujo et al., “Medeiros FOXL2 mutations in granulosa cell tumors occurring in males,” Archives of Pathology & Laboratory Medicine, vol. 136, no. 7, pp. 825–828, 2012.

I. T. Köksal, M. Usta, A. Ciftcioglu, T. Erdogru, E. Kukul, and M. Baykara, “Sex cord tumour of the adult testis,” International Urology and Nephrology, vol. 35, no. 3, pp. 365–367, 2003.

A. Mitra, V. Palit, R. Paes, and M. Ferro, “Sonographic features of an adult granulosa cell tumor of the testis,” Radiology Case Reports, vol. 3, article 188, 2008.

Z. Kucukodaci, M. Keles, T. Yapanoglu, B. F. Alp, Y. Aksoy, and I. Ozbey, “Adult type granulosa cell tumor of the testis: case report and review of the literature,” The Eurasian Journal of Medicine, vol. 40, pp. 39–41, 2008.

M. R. Harrison, W. Huang, G. Liu, and J. Gee, “Response to antiangiogenesis therapy in a patient with advanced adult-type testicular granulosa cell tumor,” Oncology (Williston Park), vol. 23, pp. 792–795, 2009.

D. Miliaras, E. Anagnostou, and I. Moysides, “Adult type granulosa cell tumor: a very rare case of sex-cord tumor of the testis with review of the literature,” Case Reports in Pathology, vol. 2013, Article ID 932086, 4 pages, 2013.

R. W. Norman, A. Sheridan-Jonah, J. Merrimen, and R. Gupta, “Adult granulosa cell tumor of the testicle,” Canadian Journal of Urology, vol. 20, no. 1, pp. 6640–6642, 2013.

S. U. Rane, S. Menon, S. Desai, G. Bakshi, and A. Joshi, “Granulosa cell tumor of testis: clinicopathological correlation of a rare tumor,” Indian Journal of Pathology and Microbiology, vol. 57, no. 4, pp. 564–573, 2014.

S. B. Tanner, D. B. Morilla, and J. D. Schaber, “A case of adult granulosa cell tumor of the testis,” The American Journal of Case Reports, vol. 15, article 471, 2014.

I. Tsitouridis, C. Maskalidis, A. Sdrolia, S. Pervana, E. Pazarli, and E. P. Kariki, “Adult type granulosa cell tumor of the testis: radiological evaluation and review of the literature,” Turkish Journal of Urology, vol. 40, no. 2, pp. 115–119, 2014.

R. Giulianelli, G. Mirabile, G. Vincenti, F. Pellegrino, and G. Soda, “A very rare case of adult-type granulosa cell tumor,” Archivio Italiano di Urologia, Andrologia, vol. 87, no. 1, pp. 98-99, 2015.

A. G. Vallonthaiel, A. Kakkar, A. Singh, P. N. Dogra, and R. Ray, “Adult granulosa cell tumor of the testis masquerading as hydrocele,” International Brazilian Journal of Urology, vol. 41, no. 6, pp. 1226–1231, 2015.

J. Gómez-Valcárcel, J. d. Barranco-García, and I. García-Muñoz, “Tumor de células de la granulosa de tipo adulto. Un caso raro de tumor testicular,” Presentación Y Discusión De Tres Casos Clínicos, vol. 49, no. 1, pp. 62–65, 2016.

A. Mohapatra, A. M. Potretzke, B. A. Knight, M. Han, and R. S. Figenshau, “Metastatic granulosa cell tumor of the testis: clinical presentation and management,” Case Reports in Urology, vol. 2016, Article ID 9016728, 4 pages, 2016.

O. Al-Alao, T. Gul, A. Al-Ani, I. A. Bozom, and K. Al-Jalham, “Adult-type granulosa cell tumour of the testis: report of a case and review of the literature,” Arab Journal of Urology, vol. 14, no. 1, pp. 44–49, 2016.

M. A. Bani, A. Zehani, I. Chelly, A. Fethi, S. Haouet, and N. Kchir, “Adult granulosa cell tumor of the testis: a case report,” La Tunisie Médicale, vol. 94, no. 12, pp. 897-898, 2016.

M. Elbachiri, A. Taleb, N. Derrabi et al., “Adult-type granulosa cell tumor of the testis: Report of a case and review of literature,” Pan African Medical Journal, vol. 26, article 198, 2017.

V. Mezentsev, H. Ali, J. McKenzie, and J. Virdi, “Adult type granulosa cell tumour of the testis: a case report,” Onkourologiya, vol. 13, no. 1, pp. 134–138, 2017.

E. Meilán, C. Esquinas, I. Romero, J. Duarte, and A. García-Tello, “Adult type granulosa cell testicular tumor. case report and bibliographic review,” Archivos Espanoles De Urologia, vol. 70, pp. 617–620, 2017 (Spanish).

D. Nunes-Carneiro, A. Marques-Pinto, V. Cavadas, and A. Fraga, “Adult testicular granulosa cell tumour: an extremely rare entity,” BMJ Case Reports, 2018.

A. A. Mosharafa, R. S. Foster, R. Bihrle et al., “Does retroperitoneal lymph node dissection have a curative role for patients with sex cord-stromal testicular tumors?” Cancer, vol. 98, no. 4, pp. 753–757, 2003.

J. M. Featherstone, H. S. Fernando, J. M. Theaker, P. D. Simmonds, M. C. Hayes, and G. M. Mead, “Sex cord stromal testicular tumors: a clinical series-uniformly stage i disease,” The Journal of Urology, vol. 181, no. 5, pp. 2090–2096, 2009.

K. O. Rove, P. D. Maroni, C. R. Cost et al., “Pathologic risk factors for metastatic disease in postpubertal patients with clinical stage i testicular stromal tumors,” Urology, vol. 97, pp. 138–144, 2016.

F. Bremmer, C. L. Behnes, H.-J. Radzun, M. Bettstetter, and S. Schweyer, “Sex cord gonadal stromal tumors,” Pathologe, vol. 35, pp. 245–251, 2014.

K.-P. Dieckmann, H. Richter-Simonsen, M. Kulejewski et al., “Testicular germ-cell tumours: a descriptive analysis of clinical characteristics at first presentation,” Urologia Internationalis, vol. 100, no. 4, pp. 409–419, 2018.

C. Rothermund, C. Thurneysen, R. Cathomas et al., “Baseline characteristics and patterns of care in testicular cancer patients: First data from the Swiss Austrian German Testicular Cancer Cohort Study (SAG TCCS),” Swiss Medical Weekly, vol. 148, no. 29-30, article w14640, 2018.

P. Zeuschner, C. Veith, J. Linxweiler, M. Stöckle, and J. Heinzelbecker, “Two years of gynecomastia caused by leydig cell tumor,” Case Reports in Urology, vol. 2018, Article ID 7202560, 4 pages, 2018.

F. Bremmer and S. Schweyer, “Leydig cell, Sertoli cell and adult granulosa cell tumors,” Pathologe, vol. 37, no. 1, pp. 71–77, 2016.