Prerpints.org logo
Preprint
Case Report

This version is not peer-reviewed.

Adult-Type Granulosa Cell Tumor of the Testis: A Report of a Case and a Discussion of the Literature

A peer-reviewed article of this preprint also exists.

Submitted:

15 May 2023

Posted:

16 May 2023

You are already at the latest version

Abstract
Testicular granulosa cell tumors (TGCTs) are rare tumors of sex cord stromal origin. TGCTs can be classified into the adult type and the juvenile type. The adult type is extremely rare with only 93 known cases reported in the literature. We, herein, present a report of a case of a 30 year old male patient who presented with a testicular mass, underwent radical inguinal orchiectomy and the pathology examination revealed an adult type granulosa tumor. We additionally review the literature to summarize the scientific knowledge of an entity barely described worldwide.
Keywords: 
Testis
;  
granulosa-cell tumor
;  
adult–type
;  
sex cord-stromal tumor of testis
;  
testicular cancer
Subject: 
Medicine and Pharmacology  -   Urology and Nephrology

Introduction

Testicular granulosa cell tumors (TGCTs) are rare tumors of sex cord-stromal tissue. They originate from epithelial elements of the sex cords. The mechanism underpinning the development of TGCTs remains poorly understood due to the rarity of these cases. They comprise granulosa cells and stromal components are generally low-grade malignancies, manifested by indolent growth and a low risk of metastasis [1]. GCTs are more frequently discovered in the ovaries, where the adult type is more prevalent. On the other hand, the juvenile type, despite being uncommon, predominates in the testis [2]. Men with juvenile tGCT never had documented metastatic disease [2]. On the other hand, men with adult GCT can have metastatic disease (10% to 13% of all documented cases) [2, 3]. These tumors appear to be slow-growing neoplasm with the potential to metastasize to distant sites years after initial diagnosis. There have been cases described that during the follow up were diagnosed with distant sited metastases even 10 years after the first radical surgical treatment, though appearing with no progression in this whole period. As a result, men who have undergone orchiectomy require extended follow-up because of the delayed metastatic potential of these tumors [4]. Due to the rarity of tGCT, there are several unanswered questions regarding the optimal management of patients with localized or metastatic tGCT. The aim of the present case report is to document a case of an adult type GCT and to commit an updated summary of the international literature concerning the reported cases of adult type of granulosa cell tumor of the testis, so a very infrequent oddity to be reminded and a tumor that both urologists and oncologists should have in mind.

Case Presentation

A male patient, age 30 years old, was admitted to our outpatient private office from an internal medicine department with a swelling in the left testis that was at first noticed two years ago and was growing slowly. The patient did not show any disturbance or anxiety due to the slow growth of the testis and he only decided to visit a doctor when the testis changed texture in self-examination. By the time of the examination left testis was enlarged, hard to palpation. The medical history revealed no trauma or signs of inflammation or any other known disease. We performed blood tests and radiological control. Blood tests revealed no indication of inflammation (urine culture was negative and C - reactive protein was within normal values). A-fp (A – fetoprotein), β- hg (β-choric gonadotropin) and LDH (lactate dehydrogenase) values found to be within normal range. Initially, we performed a scrotum ultrasound, which revealed a hypoechoic - solid mass of 3,8 cm diameter suspicious of malignancy. A scrotum magnetic resonance imaging confirmed the suspicion of malignancy, showing a mass with septum which was enhancing the intravenous paramagnetic contrast agent. The rest of the imaging control with CT scan of chest, abdomen and brain revealed no sites of metastatic disease or any other pathology.
According to the European Association Guidelines 2022 edition update, radical inguinal orchiectomy was proposed to the patient and he agreed.
We performed a radical inguinal orchiectomy and the left testis with its components was removed lege artis and was sent for pathology examination. The patient had a normal postoperative course with no complications according to the Clavien – Dindo score noticed. The pathology report revealed a tumor with septa consisting of large elongated cells with large grooved nuclei, inhibin positive, proposing an adult type testis granulosa tumor with a diameter of 3.8 cm, inhibin positive. Moreover, the presence of Call-Exner bodies helped to underline the diagnosis of adult type granullosa cell tumor of testis. There was a proliferation rate of mitosis lower than 3/10 hpf. The other components of the testis, rete testis, the tunica albuginea, the epididymis or the vans deferens were free of the disease. Serum inhibin type B measured in the patient right after the operation and one month later showed a decrease from 32 pg/dL to 4 pg/dL. Nevertheless, Inhibin type A did not show the same downward trend. One month after the surgery was at 10pg/dL and 6 months after the surgery was at 16pg/dL. At this timepoint we conducted a new screening with CT scan of the chest, abdomen and brain, which did not reveal any metastatic sites. 9 months after the surgery, we performed a new laboratory control and was revealed an Inhibin type A at 90 pg/dL. We conducted a FDG-PET/CT. It revealed no site of recurrence or any distant metastases or lymph nodes. Next follow up is planned to take place in 3 months’ time with new serum markers and any imaging tests needed.

Discussion

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.
Testicular granulosa cell tumors are rare neoplasms. They are sex cord stromal tumors of the testicles (SCSTs). SCSTs show differentiation towards Leydig cells, Sertoli cells, and/or other types of sex cord-stromal cells (eg, granulosa cells) [5]. Compared to germ cell tumors (GCTs), SCSTs are substantially less frequent, making up fewer than 5% of all testicular neoplasms in adults. 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. However, prepubertal men have SCSTs at a somewhat higher rate [6].
Granulosa cell tumors resemble ovarian granulosa cell tumors morphologically and are classified into adult and juvenile types, just as granulosa cell cancers in the ovary. The first documentation of an AGCT is credited to Laskowski in 1952.
The adult form is more prevalent in the ovaries, where GCTs are more frequently detected. On the other hand, the adult form is less common and the juvenile type, despite being rare, predominates in the testis [2].
Some studies have suggested that the formation of granulosa cell tumors is associated with sex chromosome abnormalities and aberrant gonadal development. It has been shown that infants with mixed gonadal dysgenesis or intersexual disorder develop juvenile-type GCTs (59). Regarding to the adult type, the expression of FOXL2 gene is supposed to play a leading role in the growth. FOXL2, a granulosa cell-expressed gene, regulates granulosa cell fate and ovarian function. A missense mutation of FOXL2 is vital in the pathogenesis of adult-type ovarian GCTs (60). With regard to its contribution to GCT development, studies have shown that this mutation impairs the capability of growth differentiation factor 9, an oncocyte-produced protein, in promoting follistatin transcription in the presence of SMAD3. This may lead to increased cell proliferation due to unopposed activin signaling. In addition, FOXL2 mutation also reduces apoptosis and increases the induction of aromatase (CYP19), which promotes estrogen synthesis (61).
Using the PUBMED database and manually scanning the reference lists of earlier studies, only 93 examples of adult type GCTs in testis could be found in the literature (Table 1). Not every case report had specific information about every clinical trait. As a result, numerous clinical aspects have to be examined using varied sample sizes.
The juvenile variety of granulosa cell tumor is the most prevalent (though uncommon) testicular tumor in infancy and is only infrequently encountered in adults. Granulosa cell tumors of the juvenile type don't exhibit the usual Call-Exner body development, have a tendency to have a little bit more cytoplasm, or have the pronounced grooving of the adult variety. The cells are instead grouped in solid sheets, nests, or nodules and frequently form ectatic areas filled with eosinophilic or basophilic material that resemble enormous follicles [7]. Infants under six months old are the age group when these tumors are most frequently found [8].
Although malignant behavior has rarely been described, adult-type granulosa cell tumors of the testicles tend to grow slowly and have a good prognosis [2, 9].
The adult type of granulosa cell tumor shares the same histologic characteristics as ovarian granulosa cell tumors. Known as typical Call-Exner body formation, the cells are organized to form solid sheets and microfollicular structures and feature elongated, grooved nuclei and little cytoplasm [9].
In our patient the pathology review revealed neoplasm tumor with septa consisting of large cells with large elongated grooved nuclei, inhibin positive, proposing an adult type testis granulosa tumor with a diameter of 3.8 cm, inhibin positive. Also the presence of Call-Exner bodies helped to underline the diagnosis of adult type granullosa cell tumor of testis.
The age of the present patient is 30 years which is clearly lower than the median age of 43.2 years and even lower than the inter quartile range (26 -55 years) as observed in the literature survey.
From our review the median tumor size at the diagnosis was 3,2 cm. Our patient at the time of diagnosis presented with a tumor of 3,8 cm in the largest dimension. 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 46 (50% of cases) had left sided tumors as opposed to 37 (40% of cases) right sided tumors. For 10 (10% of cases) patients there are no side location information.
Our analysis of the literature revealed that the painless scrotal lump or enlargement is the most typical presenting symptom in patients with adult tGCTs. Overall, like with testicular germ cell tumors, a palpable mass is likely the typical presenting sign of AGCT [3,10]. Gynecomastia and other endocrine-related symptoms are uncommon in these patients, however occurrences of the aforementioned symptoms in patients with adult-type GCTs have been documented. More specifically, gynecomastia or other endocrine symptoms were observed in 9 of the 93 reported instances (9% of reported cases). 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 [11].
Metastatic disease was never observed in men with juvenile tGCT but in men with adult tGCT [2,3]. Primary site of metastasis is represented by the retroperitoneal lymph nodes, but other sites including lungs, liver, bone and inguinal lymph nodes can also be affected [2]. In our review the average of metastatic patients was 12 of the 93 reported cases (13% of all reported cases were metastatic). Crogg et al in a recent analysis of the literature defined some predictive factors for metastases, Predictive variables for metastatic disease included tumor size, angiolymphatic invasion and presence of gynecomastia (62). Our patient was not metastatic at the initial staging, despite the increased level of Inhibin type A. We proceed a thorough follow up with control of Inhibin type A, which revealed a remarkable upward trend (from 10 pg/dL to 90 pg/dL within 3 months). We performed a FDG-PET/CT, which revealed no site of distant metastases. Till the time this report is being written, the patient remains 9 months after the initial radical surgical treatment with no recurrence and under strict follow up.

Conclusions

In conclusion, in this case presentation we report a case of adult type of germ cell tumor of testis and we committed a summary of all reported cases in the international medical literature. This is a very rare entity in adult men with specific histopathological characteristics, specific clinical characteristics and in most cases a benign clinical behavior. Nevertheless, there are some cases with metastatic disease even many years after the initial diagnosis, a fact that underlines the need of a proper oncological follow up and a detailed staging even in tumors that predominantly have a benign clinical behavior.
  • TGCTs: Testicular granulosa cell tumors
  • AGCT: Adult granulosa cell tumor
  • CT: computed tomography
  • LDH: lactate dehydrogenase

Funding

This research received no external funding.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Acknowledgements

None

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Scully, R.E. Ovarian tumors. A review. Am J Pathol. 1977, 87, 686–720. [Google Scholar] [PubMed]
  2. Grogg, J.B.; Schneider, K.; Bode, P.K.; et al. Risk factors and treatment outcomes of 239 patients with testicular granulosa cell tumors: a systematic review of published case series data. J Cancer Res Clin Oncol 2020, 146, 2829–2841. [Google Scholar] [CrossRef] [PubMed]
  3. Dieckmann, K.; Bertolini, J.; Wülfing, K. Adult Granulosa Cell Tumor of the Testis: A Case Report with a Review of the Literature. Case Reports in Urology Volume 2019. [CrossRef] [PubMed]
  4. Elbachiri, M.; Taleb, A.; Derrabi, N.; Bouchbika, Z.; Benchakroun, N.; Jouhadi, H.; Tawfiq, N.; Sahraoui, S.; Benider, A. Adult-type granulosa cell tumor of the testis: report of a case and review of literature. Pan Afr Med J. 2017, 26, 198. [Google Scholar] [CrossRef] [PubMed]
  5. WHO Classification of Tumours of the Urinary System and Male Genital Organs, 4th ed, Moch H, Humphrey PA, Ulbright TM, Reuter VE (Eds), International Agency for Research on Cancer, Lyon 2016. Vol 7, p.335.
  6. Ulbright, T.M.; Amin, M.B.; Young, R.H. Tumors of the testis, adenexa, spermatic cord, and scrotum. In: Atlas of Tumor Pathology, 3rd ed, Rosai J, Sobin LH (Eds), Armed Forces Institute of Pathology, Washington, DC 1999.
  7. Garrett, J.E.; Cartwright, P.C.; Snow, B.W.; Coffin, C.M. Cystic testicular lesions in the pediatric population. J Urol. 2000, 163, 928. [Google Scholar] [CrossRef]
  8. Acar, C.; Gurocak, S.; Sozen, S. Current treatment of testicular sex cord-stromal tumors: critical review. Urology. 2009, 73, 1165. [Google Scholar] [CrossRef]
  9. Jimenez-Quintero, L.P.; Ro, J.Y.; Zavala-Pompa, A.; Amin, M.B.; Tetu, B.; Ordoñez, N.G.; Ayala, A.G. Granulosa cell tumor of the adult testis: a clinicopathologic study of seven cases and a review of the literature. Hum Pathol. 1993, 24, 1120. [Google Scholar] [CrossRef]
  10. Cornejo, K.M.; Young, R.H. Adult granulosa cell tumors of the testis: A report of 32 cases. The American Journal of Surgical Pathology 2014, 38, 1242–1250. [Google Scholar] [CrossRef]
  11. Zeuschner, P.; Veith, C.; Linxweiler, J.; Stöckle, M.; Heinzelbecker, J. Two years of gynecomastia caused by leydig cell tumor. Case Reports in Urology 2018, 2018, 7202560. [Google Scholar] [CrossRef]
  12. Laskowski, J. Feminizing tumours of testis; general review with case report of granulosa cell tumour of testis. Endokrynologia Polska 1952, 3, 337–343. [Google Scholar]
  13. Cohen, J.; Diamond, J. Leontiasis ossea, slipped epiphyses and granulosa cell tumor of the testis with renal disease. Archives of Pathology & Laboratory Medicine 1953, 56, 488–500. [Google Scholar]
  14. Schubert, T.E.O.; Stoehr, R.; Hartmann, A.; Schöne, S.; Löbelenz, M.; Mikuz, G. Adult type granulosa cell tumor of the testis with a heterologous sarcomatous component: case report and review of the literature. Diagnostic Pathology 2014, 9, 107. [Google Scholar] [CrossRef] [PubMed]
  15. Melicow, M.M. 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 1955, 73, 547–574. [Google Scholar] [CrossRef] [PubMed]
  16. Mostofi, F.K.; Theiss, E.A.; Ashley, D.J.B. 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 1959, 12, 944–957. [Google Scholar] [CrossRef] [PubMed]
  17. Marshall, F.F.; Kerr Jr, W.S.; Kliman, B.; Scully, R.E. Sex cord stromal (gonadal stromal) tumors of the testis: a report of 5 cases. The Journal of Urology 1977, 117, 180–184. [Google Scholar] [CrossRef] [PubMed]
  18. Talerman, A. Pure granulosa cell tumour of the testis. report of a case and review of the literature. Applied Pathology 1985, 3, 117–122. [Google Scholar] [PubMed]
  19. Gaylis, F.D.; August, C.; Yeldandi, A.; Nemcek, A.; Garnett, J. Granulosa cell tumor of the adult testis: Ultrastructural and ultrasonographic characteristics. The Journal of Urology 1989, 141, 126–127. [Google Scholar] [CrossRef]
  20. Düe, W.; Dieckmann, K.-P.; Niedobitek, G.; Bornhoft, G.; Loy, V.; Stein, H. 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 1990, 43, 732–737. [Google Scholar] [CrossRef]
  21. Nistal, M.; Lázaro, R.; García, J.; Paniagua, R. Testicular granulosa cell tumor of the adult type. Archives of Pathology & Laboratory Medicine 1992, 116, 284–287. [Google Scholar]
  22. Matoška, J.; Ondruš, D.; Talerman, A. Malignant granulosa cell tumor of the testis associated with gynecomastia and long survival. Cancer 1992, 69, 1769–1772. [Google Scholar] [CrossRef]
  23. Sasano, H.; Nakashima, N.; Matsuzaki, O.; et al. Testicular sex cord-stromal lesions: Immunohistochemical analysis of cytokeratin, vimentin and steroidogenic enzymes. Virchows Archiv A Pathological Anatomy and Histopathology 1992, 421, 163–169. [Google Scholar] [CrossRef]
  24. Monobe, Y.; Manabe, T. 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 1992, 22, 414–420. [Google Scholar]
  25. Renshaw, A.A.; Gordon, M.; Corless, C.L. Immunohistochemistry of unclassified sex cord-stromal tumors of the testis with a predominance of spindle cells. Modern Pathology 1997, 10, 693–700. [Google Scholar]
  26. Morgan, D.R.; Brame, K.G. Granulosa cell tumour of the testis displaying immunoreactivity for inhibin. BJU International 1999, 83, 731–732. [Google Scholar] [CrossRef]
  27. Al-Bozom, I.A.; El-Faqih, S.R.; Hassan, S.H.; El-Tiraifi, A.E. 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 2000, 124, 1525–1528. [Google Scholar]
  28. Wang, B.Y.; Rabinowitz, D.S.; Granato RC, S.; Unger, P.D. Gonadal tumor with granulosa cell tumor features in an adult testis. Annals of Diagnostic Pathology 2002, 6, 56–60. [Google Scholar] [CrossRef]
  29. Guzzo, T.; Gerstein, M.; Mydlo, J.H. Granulosa cell tumor of the contralateral testis in a man with a history of cryptorchism. Urologia Internationalis 2004, 72, 85–87. [Google Scholar] [CrossRef]
  30. Suppiah, A.; Musa, M.M.; Morgan, D.R.; North, A.D. 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 2005, 75, 91–93. [Google Scholar] [CrossRef]
  31. Hisano, M.; Mascarenhas Souza, F.M.; Costa Malheiros DM, A.; Lima Pompeo, A.C.; Lucon, A.M. Granulosa cell tumor of the adult testis. Report of a case and review of the literature. Clinics 2006, 61, 77–78. [Google Scholar] [CrossRef]
  32. Arzola, J.; Hutton, R.L.; Baughman, S.M.; Mora, R.V. Adult-type testicular granulosa cell tumor: Case report and review of the literature. Urology 2006, 68, 1121–e13. [Google Scholar] [CrossRef]
  33. López, J.I. Adult-type granulosa cell tumor of the testis. report of a case. Tumori 2007, 93, 223–224. [Google Scholar] [CrossRef]
  34. Ditonno, P.; Lucarelli, G.; Battaglia, M.; et al. Testicular granulosa cell tumor of adult type: a new case and a review of the literature. Urologic Oncology: Seminars and Original Investigations 2007, 25, 322–325. [Google Scholar] [CrossRef]
  35. Gupta, A.; Mathur, S.; Reddy, C.; Arora, B. Testicular granulosa cell tumor, adult type. Indian Journal of Pathology and Microbiology 2008, 51, 405–406. [Google Scholar] [CrossRef]
  36. Hammerich, K.H.; Hille, S.; Ayala, G.E.; et al. Malignant advanced granulosa cell tumor of the adult testis: case report and review of the literature. Human Pathology 2008, 39, 701–709. [Google Scholar] [CrossRef]
  37. Song, Z.; Vaughn, D.J.; Bing, Z. Adult type granulosa cell tumor in adult testis: report of a case and review of the literature. Rare Tumors 2011, 3, 117–119. [Google Scholar] [CrossRef]
  38. Hanson, J.A.; Ambaye, A.B. Adult testicular granulosa cell tumor: a review of the literature for clinicopathologic predictors of malignancy. Archives of Pathology & Laboratory Medicine 2011, 135, 143–146. [Google Scholar]
  39. Lima, J.F.; Jin, L.; de Araujo, A.R.; et al. Medeiros FOXL2 mutations in granulosa cell tumors occurring in males. Archives of Pathology & Laboratory Medicine 2012, 136, 825–828. [Google Scholar]
  40. Köksal, I.T.; Usta, M.; Ciftcioglu, A.; Erdogru, T.; Kukul, E.; Baykara, M. Sex cord tumour of the adult testis. International Urology and Nephrology 2003, 35, 365–367. [Google Scholar] [CrossRef]
  41. Mitra, A.; Palit, V.; Paes, R.; Ferro, M. Sonographic features of an adult granulosa cell tumor of the testis. Radiology Case Reports 2008, 3, 188. [Google Scholar] [CrossRef]
  42. Kucukodaci, Z.; Keles, M.; Yapanoglu, T.; Alp, B.F.; Aksoy, Y.; Ozbey, I. Adult type granulosa cell tumor of the testis: case report and review of the literature. The Eurasian Journal of Medicine 2008, 40, 39–41. [Google Scholar]
  43. Harrison, M.R.; Huang, W.; Liu, G.; Gee, J. Response to antiangiogenesis therapy in a patient with advanced adult-type testicular granulosa cell tumor. Oncology (Williston Park) 2009, 23, 792–795. [Google Scholar]
  44. Miliaras, D.; Anagnostou, E.; Moysides, I. 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 2013, 2013, 932086. [Google Scholar] [CrossRef]
  45. Norman, R.W.; Sheridan-Jonah, A.; Merrimen, J.; Gupta, R. Adult granulosa cell tumor of the testicle. Canadian Journal of Urology 2013, 20, 6640–6642. [Google Scholar]
  46. Rane, S.U.; Menon, S.; Desai, S.; Bakshi, G.; Joshi, A. Granulosa cell tumor of testis: clinicopathological correlation of a rare tumor. Indian Journal of Pathology and Microbiology 2014, 57, 564–573. [Google Scholar]
  47. Tanner, S.B.; Morilla, D.B.; Schaber, J.D. A case of adult granulosa cell tumor of the testis. The American Journal of Case Reports 2014, 15, 471. [Google Scholar]
  48. Tsitouridis, I.; Maskalidis, C.; Sdrolia, A.; Pervana, S.; Pazarli, E.; Kariki, E.P. Adult type granulosa cell tumor of the testis: radiological evaluation and review of the literature. Turkish Journal of Urology 2014, 40, 115–119. [Google Scholar] [CrossRef]
  49. Giulianelli, R.; Mirabile, G.; Vincenti, G.; Pellegrino, F.; Soda, G. A very rare case of adult-type granulosa cell tumor. Archivio Italiano di Urologia, Andrologia 2015, 87, 98–99. [Google Scholar] [CrossRef]
  50. Vallonthaiel, A.G.; Kakkar, A.; Singh, A.; Dogra, P.N.; Ray, R. Adult granulosa cell tumor of the testis masquerading as hydrocele. International Brazilian Journal of Urology 2015, 41, 1226–1231. [Google Scholar] [CrossRef]
  51. Gómez-Valcárcel, J.; d Barranco-García, J.; García-Muñoz, I. Tumor de células de la granulosa de tipo adulto. Un caso raro de tumor testicular. Presentación Y Discusión De Tres Casos Clínicos 2016, 49, 62–65. [Google Scholar]
  52. Mohapatra, A.; Potretzke, A.M.; Knight, B.A.; Han, M.; Figenshau, R.S. Metastatic granulosa cell tumor of the testis: clinical presentation and management. Case Reports in Urology 2016, 2016, 9016728. [Google Scholar] [CrossRef]
  53. Al-Alao, O.; Gul, T.; Al-Ani, A.; Bozom, I.A.; Al-Jalham, K. Adult-type granulosa cell tumour of the testis: report of a case and review of the literature. Arab Journal of Urology 2016, 14, 44–49. [Google Scholar] [CrossRef]
  54. Bani, M.A.; Zehani, A.; Chelly, I.; Fethi, A.; Haouet, S.; Kchir, N. Adult granulosa cell tumor of the testis: a case report. La Tunisie Médicale 2016, 94, 897–898. [Google Scholar]
  55. Mezentsev, V.; Ali, H.; McKenzie, J.; Virdi, J. Adult type granulosa cell tumour of the testis: a case report. Onkourologiya 2017, 13, 134–138. [Google Scholar] [CrossRef]
  56. Meilán, E.; Esquinas, C.; Romero, I.; Duarte, J.; García-Tello, A. Adult type granulosa cell testicular tumor. case report and bibliographic review. Archivos Espanoles De Urologia 2017, 70, 617–620. [Google Scholar]
  57. Nunes-Carneiro, D.; Marques-Pinto, A.; Cavadas, V.; Fraga, A. Adult testicular granulosa cell tumour: an extremely rare entity. BMJ Case Reports 2018. [Google Scholar] [CrossRef]
  58. Kabore, M.; Ido, F.; Yameogo, C.A.M.K.D.; Ouedraogo, A.A.; Kirakoya, B.; Kabore, F.A. Adult Granulosa Cell Tumor of the Testis: A case report and review of the literature. Urol Case Rep. 2021, 38, 101718. [Google Scholar] [CrossRef]
  59. Young, R.H.; Lawrence, W.D.; Scully, R.E. Juvenile granulosa cell tumor-another neoplasm associated with abnormal chromosomes and ambiguous genitalia. A report of three cases. Am J Surg Pathol. 1985, 9, 737–743. [Google Scholar]
  60. Shah, S.P.; Kobel, M.; Senz, J.; Morin, R.D.; Clarke, B.A.; Wiegand, K.C.; Leung, G.; Zayed, A.; Mehl, E.; Kalloger, S.E.; et al. : Mutation of FOXL2 in granulosa-cell tumors of the ovary. N Engl J Med. 2009, 360, 2719–2729. [Google Scholar] [CrossRef]
  61. Leung, D.T.H.; Fuller, P.J.; Chu, S. Impact of FOXL2 mutations on signaling in ovarian granulosa cell tumors. Int J Biochem Cell Biol. 2016, 72, 51–54. [Google Scholar] [CrossRef]
  62. Grogg, J.B.; Schneider, K.; Bode, P.K.; et al. Risk factors and treatment outcomes of 239 patients with testicular granulosa cell tumors: a systematic review of published case series data. J Cancer Res Clin Oncol 2020, 146, 2829–2841. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.
Copyright: This open access article is published under a Creative Commons CC BY 4.0 license, which permit the free download, distribution, and reuse, provided that the author and preprint are cited in any reuse.
Prerpints.org logo

Preprints.org is a free preprint server supported by MDPI in Basel, Switzerland.

facebook logotwitter logolinkedin logo
bsky
MDPI Initiatives
Important Links
Subscribe

Disclaimer

Terms of Use

Privacy Policy

Privacy Settings

© 2025 MDPI (Basel, Switzerland) unless otherwise stated