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  Table of Contents    
ORIGINAL ARTICLE  
Year : 2014  |  Volume : 57  |  Issue : 4  |  Page : 564-573
Granulosa cell tumor of testis: Clinicopathological correlation of a rare tumor


1 Department of Pathology, Tata Memorial Centre, Mumbai, Maharashtra, India
2 Department of Pathology & Urology Disease Management Group, Tata Memorial Centre, Mumbai, Maharashtra, India
3 Department of Surgical Oncology & Urology Disease Management Group, Tata Memorial Centre, Mumbai, Maharashtra, India
4 Department of Medical Oncology & Urology Disease Management Group, Tata Memorial Centre, Mumbai, Maharashtra, India

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Date of Web Publication11-Oct-2014
 

   Abstract 

Background: Granulosa cell tumor of testis is a rare tumor accounting for less than 4% of adult testicular tumors though they account for nearly 30% of childhood testicular tumors. Due to the rarity of these tumors, exact etiology, pathogenesis, prognostic factors and best treatment approach are not well known. The molecular events in pathogenesis of these stromal tumors have begun to unravel and these developments put forth a reasonable and scientific explanation for the association of these tumors with developmental anomalies like undescended testis. However, many questions remain unanswered. Materials and Methods: We performed a retrospective analysis of clinicopathological features of all Granulosa Cell Tumors of testis from our archives in addition to an extensive literature search using PUBMED with the key words "Granulosa Cell Tumor, testis". Results: We found six cases in our archives, two of which were of juvenile type and four of adult type. One out of these six cases presented with metastases. All cases underwent radical orchidectomy. Morphology and immunohistochemistry were classical in all cases and there was no diagnostic dilemma. Literature search revealed 63 cases of testicular Granulosa Cell Tumor in addition to highlighting the similarities in the biology and the dissimilarities in the clinical behavior as compared to ovarian Granulosa Cell Tumor. Conclusion: Testicular Granulosa Cell Tumor is a rare tumor, which although histologically similar to its ovarian counterpart, differs in clinical behavior. Further detailed investigations are needed to reveal the mystery behind the differing clinical behavior despite histological and immunohistochemical similarity between the testicular and ovarian Granulosa Cell Tumors.

Keywords: Testicular granulosa cell tumor, testicular sex cord stromal tumor, juvenile granulosa cell tumor, adult granulosa cell tumor

How to cite this article:
Rane SU, Menon S, Desai S, Bakshi G, Joshi A. Granulosa cell tumor of testis: Clinicopathological correlation of a rare tumor . Indian J Pathol Microbiol 2014;57:564-73

How to cite this URL:
Rane SU, Menon S, Desai S, Bakshi G, Joshi A. Granulosa cell tumor of testis: Clinicopathological correlation of a rare tumor . Indian J Pathol Microbiol [serial online] 2014 [cited 2019 Dec 7];57:564-73. Available from: http://www.ijpmonline.org/text.asp?2014/57/4/564/142665



   Introduction Top


Testicular tumors are common in all age groups, with germ cell tumors being the most common group. Sex cord stromal tumors are relatively rare accounting for approximately 3-4% of all testicular tumors occurring in adults, though they account for nearly 30% of testicular tumors in children and infants. Due to their rarity and similarity to the ovarian sex cord stromal tumors, the terminology of adult sex cord stromal tumors is the same as that used in ovarian counterparts. However, testicular Granulosa Cell Tumors are rare tumors and hence management issues and prognostic factors are not completely understood with current nomenclature, understanding and management strategies being extrapolations from their ovarian counterparts.


   Aims Top


The aim of our study was to attempt a clinicopathologic correlation of all published cases of testicular Granulosa Cell Tumor in addition to our own archived cases.


   Materials and Methods Top


We searched our archives for testicular Granulosa Cell Tumors, in addition to performing a literature search in PUBMED using the keywords, "Granulosa Cell Tumor, Testis". Archived histology and immunohistochemistry slides were reviewed, clinicopathologic features were reviewed, tabulated and compared. Continuous variables like age of patient, tumor size etc were reported as mean ( ±SD). All published cases of testicular Granulosa Cell Tumor in English literature were also reviewed for clinicopathologic features. In addition studies comparing testicular and ovarian Granulosa Cell Tumors were analyzed.


   Results Top


To the best of our knowledge, only 63 cases of granulosa cell tumor of testis are reported in the English literature (including the present series), 40 of adult type and 23 of juvenile type. In this report, we present one of the largest case series from a single institute comprising six cases of testicular granulosa cell tumors from our pathology archives collected over a period of 10 years accounting for 0.29 % of all testicular tumors at our institute (a tertiary cancer-care institute), along with a review of literature regarding their clinicopathological prognostic factors.

Detailed clinicopathological characteristics of our six cases are presented in [Table 1]. Briefly, there were two cases of juvenile granulosa cell tumors and four cases of adult granulosa cell tumors. All the four adult granulosa cell tumors and one of the juvenile granulosa cell tumor were present in adults (4 th and 5 th decade, mean ± SD age 39.5 ±7.55). One case of juvenile granulosa cell tumor was present in a 2-year-old child. All cases presented with mass in scrotum of 3 months to 2 years duration. None of the cases had elevated serum levels of α-fetoprotein levels. One patient (CC6) had elevated β-HCG and LDH. This was ascribed to a co-existent widely metastatic embryonal carcinoma, which did not have any demonstrable origin in either of the two testes. Left and right testes were equally affected. All cases underwent high inguinal orchidectomy. One patient (CC2) received adjuvant chemotherapy for metastatic disease at presentation. Specimens were received in three of these six patients, who were operated at our institution. Remaining three patients were operated outside and paraffin blocks were referred to our institute. Preoperative radiology was available in 3/4 adult granulosa cell tumor cases and revealed the tumors to be multicystic with intervening solid areas in two cases and completely solid in one case. Mean ( ± SD) tumor size of the non-metastatic cases was 4.33 ± 2.57 cm, while the sole metastatic case had a tumor of 11 cm maximum dimension.
Table 1: Summary of clinicopathological parameters of present 6 cases

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   Discussion Top


Detailed review of clinicopathological features of all the reported cases is shown in [Table 2].
Table 2: Review of all testicular granulosa cell tumors reported till date

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Clinical presentations

Though both the types of granulosa cell tumors can occur at any age, the adult type tends to occur in adults with a mean age of 44 yrs at presentation, while the juvenile type occurs in children, accounting for nearly 6% of prepubertal testicular tumors and is the most common testicular tumor present at birth. There is a reported slight predilection for the juvenile type to occur in the left testis. [1] However, in our experience and review, the predilection is minimal (20 rt. testis vs. 24 lt. testis among the cases with reported laterality). The clinical presentation depends on the type of granulosa cell tumor in question.

Juvenile granulosa cell tumor presents as either painless scrotal or abdominal mass and is associated with ambiguous genitalia in 20% cases and contralateral undescended testis in 30% cases. All such cases tend to have chromosomal anomalies with 45/46XY mosaicism or anomalies of chromosome Y. They do not produce any demonstrable hormonal effects in most cases.

Adult granulosa cell tumors on the other hand present as a slowly increasing painless scrotal mass with gynecomastia being present in approximately 25% of cases. Most of them are not associated with any chromosomal anomalies.

Pathologic features

Grossly, tumors are yellowish and can be either solid or multicystic with the adult type of tumors being commonly solid with only small cystic areas if present, while juvenile granulosa cell tumors are grossly multicystic. AGCT at presentation, range in size from 0.5 to 13 cm with an average of 5 cm, while the JGCT are relatively smaller at presentation (0.5 to 5 cm). However, this apparent difference in size at presentation could be due to the early detection within the pediatric population in which JGCTs are common, as compared to the AGCT, which would be clinically symptomatic only after it reaches a considerable size to replace the adult testis.

Histologically, a variety of patterns is seen in both the histological types, with microfollicular and diffuse patterns being the most common. Other patterns seen are trabecular [Figure 1]a, macrofollicular, gyriform and pseudosarcomatous. A microfollicular pattern is relatively common in the adult type while the JGCTs harbor macrofollicular patterns more frequently. Nuclear features are characteristically different in both types of tumor. AGCT have monomorphic, oval, grooved, coffee-bean shaped nuclei with bland chromatin without any mitoses [Figure 1]b, while the JGCT tend to have round nuclei without significant grooving. Mitoses are common in JGCT with many cases having abundant mitoses. Most tumors are well circumscribed and at times can be enucleated; the presence of invasive margins predicts an aggressive course.
Figure 1: Panel of representative photomicrographs showing (a) trabecular histological pattern (Hand E stain, 100× original magnification). (b) Nuclear grooves giving a coffee-bean appearance is a characteristic feature of adult granulosa cell tumors (H and E stain, 400× original magnification). (c) Presence of necrosis (*) is a feature strongly associated with malignant behavior. (H and E stain, 200× original magnification). (d) Inhibin and (e) MIC2 positivity are common markers of sex cord stromal tumors in general

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Immunohistochemistry

Most of the tumors stain for the pan-sex cord stromal markers [Table 3], namely Inhibin [Figure 1]d, vimentin and calretinin. Among all the cases reported in literature, inhibin (25/26), vimentin (10/10), calretinin (10/11), MIC2 (7/10) [Figure 1]e and smooth muscle actin (6/9) are most common positive markers reported. Other positive markers include S100 (3/9), CK (6/14), EMA (2/13) and WT1 (1/1). Markers which are absent and thus helpful in the differential diagnosis include desmin (0/8), D2-40 (0/1), α-fetoprotein (0/13), β-HCG (0/3), PLAP (0/3), CD117 (0/4), CD30 (0/3), synaptophysin (0/1) and chromogranin (0/1).
Table 3: Immunohistochemical profile of all testicular granulosa cell tumors reported in the literature

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Correlation of pathology features with clinical behavior and predictors of malignancy

Metastasis has been reported in adult granulosa cell tumors in ~20% of cases. [2],[3] The tumors metastasize commonly to retroperitoneal lymph nodes with isolated cases of bone [2] and lung [4] metastases been reported. Irrespective of the reported frequencies, certain features predict metastases. Pathological factors favoring poor prognosis include large tumor size (>5cm), presence of necrosis [Figure 1]c, hemorrhage, vascular invasion and invasion into adjacent testis, rete testis or tunica albuginea. The only consistent feature that predicts malignancy is tumor size more than 5 cm. The size of the malignant tumors reported in the literature averages 69.6 ±15.6 mm as compared to the benign tumors which average 35.2 ± 4.6 mm. This is noted even in our series, where the only malignant adult granulosa cell tumor measured 11 cm in greatest dimension. The cases that do not satisfy these criteria for malignancy have not recurred or metastasized.

Unlike adult granulosa cell tumors, the presence of invasive borders infiltrating into adjacent testis does not appear to predict malignancy for the JGCTs, and no reported cases have had any recurrences or metastases. [5] None of the reported juvenile granulosa cell tumors in testis has been shown to be malignant.

Etiology, histogenesis and molecular pathology

The exact etiology of both the varieties of granulosa cell tumors of testis is unknown. The association with undescended testis and concentration of JGCT in the perinatal age group suggests the occurrence of an occult genetic event during intra-uterine development. Chromosomal anomalies involving the sex chromosomes, commonly the Y chromosome, have been reported frequently in juvenile granulosa cell tumors. [6],[7] No such chromosomal anomaly has been documented in the adult variety. Recently, nearly all AGCTs in women have been demonstrated to harbor a unique and specific mutation within the FOXL2 gene. [8],[9],[10],[11],[12],[13],[14],[15],[16],[17] This mutation, namely 402C ; G (C134W), is proven to result in increased induction of the target aromatase, reduce apoptosis [11],[12],[18] and cause alterations in cell cycle. [19],[20]

Since its demonstration in ovarian AGCTs, this particular mutation (402C ; G) has been demonstrated in testicular AGCTs as well, albeit in a smaller proportion of cases (2/5, 40%). [21] The role of the FOXL2 gene in the pathogenesis of granulosa cell tumor was suggested by Kalfa et al., [22] who were the first to show nuclear expression of FOXL2 in testicular juvenile granulosa cell tumors much like the normal ovarian granulosa cells and juvenile granulosa cell tumors of ovary. They also showed cytoplasmic sequestration of the SOX9 protein, which otherwise shows nuclear expression in normal developing testis. The role of both SOX9 and FOXL2 genes in the gonadal development has been extensively studied in mouse models. SOX9 is one of the foremost genes activated in mammalian male gonad, where it is essential and at the same time sufficient to induce testicular development. [23] In the undifferentiated gonad, the SOX9 protein is sequestered in the cytoplasm and nuclear localization is noted only after commitment toward testicular differentiation, [24] while the SOX9 gene is down regulated in the event of ovarian differentiation. [25] Kalfa et al. [22] thus hypothesized that the aberrant cytoplasmic expression of SOX9 and nuclear expression of FOXL2 suggest transdifferentiation of Sertoli cells toward granulosa cells. However, we believe that this could also be explained by a much simpler explanation that granulosa cell tumor arose within the remnants of the undifferentiated gonads within the testis. In another experiment using mouse models, all Smad1 Smad5 double knock out and Smad1 Smad5 Smad8 (part of the TGF-β pathway) triple knockout female mice developed granulosa cell tumors while male knockout mice developed Sertoli-Leydig cell tumors. [26]

Overall, the evidence outlining the etiology and molecular pathogenesis of testicular granulosa cell tumors is still in its early stages; however, the hypothesis of SOX9 and FOXL2 dysregulation in the pathogenesis of granulosa cell tumors seems promising.

Treatment options

Traditionally, high inguinal orchidectomy has been performed for all granulosa cell tumors, since there are no clinical or radiological criteria to predict the histology or to differentiate between benign and malignant tumors in tumors confined to the testis. However, in a retrospective analysis, one patient having undergone testis sparing enucleation for JGCT has shown no recurrence or progression at the end of 5 years with the authors recommending the procedure for small tumors. [27] Similarly, enucleation was a definite treatment option for small sex cord stromal tumors including granulosa cell tumors within the Italian TREP project. [28] Apart from size, Valla et al., as well as Bullota et al., [29] proposed that absence of raised AFP and/or β-HCG be used as an additional criterion to select patients for testicular sparing surgery amongst the patients with small tumors as it effectively rules out yolk sack tumors and teratomas which are by far the most common tumors in the testis.


   Conclusion Top


Testicular granulosa cell tumors are rare tumors usually presenting as a mass in the testis. Dysregulation of SOX9 and FOXL2 genes as a cause of granulosa cell tumors seems to be a promising target for further study. Metastasis is an uncommon event in these tumors and virtually absent from the set of juvenile granulosa cell tumors. Though most cases have undergone radical orchidectomy, there is compelling evidence to suggest that testicular sparing surgery is a viable option in cases without any evidence of metastases at presentation, normal levels of serum tumor markers (AFP, B-HCG, LDH) and small tumors especially for the juvenile type.[46]

 
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Correspondence Address:
Santosh Menon
Department of Pathology, 8th Floor, Annexe Building, Tata Memorial Hospital, Dr. Ernest Borges Road, Parel, Mumbai - 400 012, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0377-4929.142665

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