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Gonadal tumor with granulosa cell tumor features in an adult testis
Gonadal Tumor With Granulosa Cell Tumor Features in an Adult Testis Beverly Y. Wang, MD, David S. Rabinowitz, MD, Roberto C. Granato, Sr, MD, and Pamela D. Unger, MD Granulosa cell tumor is almost exclusively an ovarian tumor. Rare cases of granulosa cell tumor have been reported involving the testes. We report a testicular gonadal stromal tumor with granulosa cell differentiation in a 54-year-old white man. The tumor was discovered by an ultrasound evaluation for left hydrocele. The patient was clinically asymptomatic. On frozen section, the initial impression was a malignant lymphoma. Final histology on the orchiectomy specimen showed a gonadal stromal tumor with granulosa cell features. Immunohistochemical studies excluded malignant lymphoma and germ cell tumors, consistent with a stromal tumor. This case report illustrates the challenges for the pathologist in making an accurate diagnosis in unusual testicular tumors. Ann Diagn Pathol 6: 56-60, 2002. Copyright © 2002 by W.B. Saunders Company Index Words: Testis, sex cord stromal tumor, granulosa cell tumor
S
INCE THE first testicular granulosa cell tumor (GCT) was reported in 1952, isolated case reports and small serial studies have been described.1-4 These rare neoplasms are comparable to the GCT found in the ovary, although far less common than their ovarian counterparts.5 Since that time, two separate types of testicular GCT have been identified: the adult type (rare) and the juvenile type (more frequent).2-4,6 Pure classic GCTs are exceedingly rare in the testis.2,6 Most of these tumors occurred in asymptomatic men; only a few cases had signs and symptoms associated with hormonal disturbances such as estrogen over-secretion7 or congenital anomalies.8 The biologic behavior of the testicular GCT appears to be somewhat less aggressive than that of its homologous ovarian counterpart5,9; however, it may be an indolent entity with unpredictable outcome.2,3,8,10
From the Lilian and Henry M. Stratton-Hans Popper Department of Pathology, The Mount Sinai School of Medicine, The Mount Sinai Medical Center, New York; and the Department of Genitourology, The Mount Sinai Hospital of Queens, New York, NY. Address reprint requests to Pamela D. Unger, MD, Department of Pathology, The Mount Sinai School of Medicine, The Mount Sinai Medical Center. New York, NY 10029. Copyright © 2002 by W.B. Saunders Company 1092-9134/02/0601-0004$35.00/0 doi:10.1053/adpa.2002.30607
56
The morphology of adult GCT of testis is similar to those identified in the ovaries; however, it may cause diagnostic difficulties for pathologists. Unlike other nongerm cell tumors in the testis or sex cord stromal tumors, testicular GCT may be confused with other tumors such as malignant lymphoma. We report a case of gonadal tumor of testis with GCT differentiation, which was misdiagnosed as malignant lymphoma on frozen section. The histologic features of testicular GCT and relevant differential diagnoses are discussed. Case History A 54-year-old healthy white man presented in the genitourology clinic at The Mount Sinai Hospital of Queens, New York, NY for routine examination. Physical examination showed a well-developed male with no apparent abnormalities except for mild left testicular hydrocele. An ultrasound evaluation disclosed a dime-sized painless mobile soft nodule within the left testis. The duration of the nodule was not known. His past medical history was only remarkable for hypertension. Preoperative laboratory tests were unremarkable. Clinically, the lesion was felt to be a neoplasm and the patient was scheduled for an orchiectomy. During the procedure, the nodule appeared to be encapsulated and was easily enucleated. The entire lesion was 1.6⫻1.5⫻1.5 cm and was submitted for frozen section. Touch imprints and frozen sections showed uniform small lymphocyte-like cells, most of which contain cleaved nuclei (Fig1). The frozen section diagnosis was reported as malignant lym-
Annals of Diagnostic Pathology, Vol 6, No 1 (February), 2002: pp 56-60
Gonadal Tumor in an Adult Testis
57
Figure 1. Microphotograph of touch imprints showing the tumor composed of uniform small cells with “coffee bean” shaped nuclear grooves (arrows). The cytopasmic outlines are indistinct. (DiffQick Giemsa stain.)
phoma. Subsequently, a left radical orchiectomy specimen was received which did not show any additional lesions. The patient recovered uneventfully.
Pathology Results Gross Examination On cut surface, the testis was 3.5⫻⫻3.0⫻2.6 cm and contained a well-circumscribed homogeneous tan soft nodule. The nodule measured 1.6⫻1.5⫻1.5 cm in size and was confined within the testicular parenchyma. The remainder of the testis showed unremarkable testicular texture. The tunica albuginea and the attached spermatic cord and epididymis appeared unremarkable.
Histologic Examination Morphologic evaluation was based on paraffin embedded tissue and hematoxylin-eosin stained sections. The tumor was composed of uniform small cells, most of which exhibited nuclear grooves. This feature was better appreciated on touch imprints with DiffQick (RichardAllan Scientific, Kalamazoo, MI) Giemsa stain (Fig 1). On tissue sections, the tumor cells were arranged in cords, small nests, and microfollicles with occasional entrapped seminiferous tubules (Fig 2). In addition, other areas of the tumor showed Call-Exner body-like formation (Fig 3). The tumor was confined to the testis. The remainder of the testis, epididymis, and spermatic cord showed no significant pathology.
Immunohistochemical Studies The tumor cells were positive for low molecular weight cytokeratin (Cam 5.2: Becton Dickinson; Mountain View,
CA), strongly positive for vimentin, and negative for placental alkaline phosphatase (Dako; Carpinteria, CA), alpha fetoprotein (Dako), leukocyte common antigen (Dako), estrogen receptor (Dako), and progesterone receptor (Zymed, South San Francisco, CA). Inhibin stain was not available. The results of tumor immunoreactivity excluded the differential diagnoses of malignant lymphoma and germ cell tumors. The findings support the diagnoses of testicular gonadal stromal tumor with granulosa cell features.
Discussion Granulosa cell tumor in the testis is rare and its morphology is similar to the conventional GCT of the ovary.2-4 The majority of affected adult male patients were white and asymptomatic.4,11 These tumors were often discovered incidentally, were of unknown duration, and exhibited no endocrinerelated symptoms.11 Only a few cases of testicular GCT were reported with associated gynecomastia or chromosomal anomalies7, 8,12,13; however, it has not been described that there is an obvious relation between tumor morphology and endocrine function in the literature. Ovarian GCT accounts for 5% of all ovarian tumors, 5% of which occur before puberty as juvenile GCT and 40% in the postmenopausal group as the adult type. Less than 5% are bilateral.2,4,11 Unlike most ovarian GCTs of the adult type, testicular GCTs are mainly of the juvenile type. Juvenile GCT is a relatively common sex cord stromal neoplasm that has been estimated to comprise about
58
Wang et al
Figure 2. Low magnification of the tumor showing the tumor cells arranged in cords and nests with an entrapped seminiferous tubule (arrow).
15% of gonadal stromal tumors of the infantile testis, with a peak incidence during the first months of life.4,6,10,14,15 Although the adult type of GCT in the ovary involves predominantly postmenopausal women, it can be found in the testes of both young
Figure 3. High magnification of the tumor showing some areas with CallExner body-like structures (arrows).
and older males, with as average age around 42.5 years.6,11 It usually produces estrogens in both sexes.6,7,9 Testicular GCT shares similar histology with ovarian GCT. Most testicular GCTs described are well
Gonadal Tumor in an Adult Testis
circumscribed, yellow to gray, with a solid to partially cystic appearance. Microscopically, they have a variety of morphologies including the typical patterns of ovarian GCT such as solid, cystic, microfollicular, gyriform, insular, and trabecular patterns. Call-Exner bodies are present in some cases. Tumor cells may exhibit the usual pale nuclei with occasional or frequent nuclear grooves. Rare cases show surrounding testicular parenchyma with Leydig cell hyperplasia and a Sertoli cell nodule.2,4,11 Our current case showed tumor growth in cords and nests with microfollicles and Call-Exner body formation (Figs 2, 3). These architectural patterns are characteristics of GCT of the adult type. Histologic features do not always predict the clinical course of the tumor. However, in rare cases, a potentially malignant tumor should be suspected if the tumor is more than 7cm, necrotic, hemorrhagic, or shows vascular/lymphatic invasion.6,7,9,11 A panel of immunohistochemical markers may aid in the diagnosis. The immunologic features of GCT usually include strong immunoreactivity for vimentin, variable results for cytokeratin, and negative for epithelial membrane antigen.4,11 Our case was positive for vimentin and cytokeratin Cam 5.2, negative for leukocyte common antigens, placental alkaline phosphatase, and alpha fetoprotein. Estrogen receptor/progesterone receptor are expressed by testicular sex cord stromal tumor with GCT differentiation of adult type,4,16 both antibodies were nonimmunoreactive in our case. In this particular case, one should emphasize that tumor cytology on frozen section mimicked malignant lymphoma (Fig1). In such a situation, leukocyte common antigen plays an important role. The immunohistochemical profile can easily exclude malignant lymphoma and germ cell tumors. Because of the relative rarity and heterogeneity of testicular stromal tumors, these tumors frequently pose diagnostic problems for pathologists. One should pay attention to the histologic features and try to eliminate differential diagnoses. Certain patterns of GCT, such as microfollicular, are so distinctive that diagnostic problems do not arise when this pattern is accompanied by the typical cytologic features of neoplastic granulosa cells.6 The diagnosis is more likely to be problematic when a diffuse pattern is present; in such cases appreciation of the characteristic cytological features is extremely helpful.6 Clinically, the behavior of testicular GCT is
59
thought to be benign, with occasional cases being indolent with unpredictable behavior. However, rare cases were reported to be malignant with metastasis.2,6,7,9,11 Mostofi et al18 reported a malignant testicular GCT as high as 10%. It is said that the prognosis of the adult type of GCT is worse in the ovary than in the testis in general.5,17,18 Ovarian GCT is sometimes associated with metastatic disease occurring 5 to 20 years after excision of the primary tumor.5 However, in the case reported by Matoska et al,9 metastatic spread had occurred only 7 months after the tumor was noticed. Therefore, it is mandatory to rule out the presence of metastatic spread and staging of the disease after orchiectomy through careful investigation. In summary, our findings and a review of the literature indicate that GCT of the adult testis is a rare and slow-growing neoplasm. Morphologically, it may mimic other types of testicular neoplasms. The rarity of this entity should not preclude an accurate diagnosis, which will provide correct information for clinicians to take appropriate clinical management. Clinically, it may have uncertain potential to form distant metastases. Because recurrence or distant metastasis may occur late in the clinical course, long-term follow-up is warranted. Acknowledgement The authors greatly appreciate Norman Katz and Micha Zeffren for their excellent photographic assistance, and Dr Lorraine Miller for providing immunomarker studies.
References 1. Laskowski J: Feminizing tumors of the testis: General review with case report of granulosa cell tumor of testis. Endokrynol Pol 1995;3:337-343 2. Talerman A: Pure granulosa cell tumor of the testis. Report of a case and review of the literature. Appl Pathol 1985;3:117122 3. Gaylis FD, August C, Yeldandi A, et al: Granulosa cell tumor of the adult testis: Ultrastructural and ultrasonographic characteristics. J Urol 1989;141:126-127 4. Nistal M, Lazaro R, Garcia J, et al: Testicular granulosa cell tumor of the adult type. Arch Pathol Lab Med 1992;116:284-287 5. Scully RE: Tumors of the ovary and maldeveloped gonalds, fallopian tube and round ligment. in Rosai J, Sobin LH (eds). Atlas of Tumor Pathology, Fascicle 23. Washington, DC, Armed Forces Institute of Pathology, 1998, pp 169-186 6. Young RH, Talerman A: Testicular tumors other than germ cell tumors. Semin Diagn Pathol 1987;4:342-360 7. Dilworth JP, Farrow GM, Pesterling JE: Non-germ cell tumors of testis. Urology 1991;37:399-417 8. Cohen J, Diamond J: Leontiasis Ossea, slipped epiphyses.
60
Wang et al
Granulosa cell tumor of the testis with renal disease: Report of case with autopsy findings. Arch Pathol 1953;56:488-500 9. Matoska J, Ondrus O, Talerman A: Malignant granulosa cell tumor of the testis associated gynecomastia and long survival. Cancer 1991;69:1769-1772 10. Lawrence WD, Young RH, Scully RE: Juvenile granulosa cell tumor of the infantile testis: A report of 14 cases. Am J Surg Pathol 1985;9:87-94 11. Jimenez-Quintero LP, Ro JY, Zavala-Pompa A, et al: Granulosa cell tumor of the adult testis: A clinicopathologic study of seven cases and a review of the literature. Hum Pathol 1993;24: 1120-1126 12. Raju U: Congenital testicular juvenile granulosa cell tumor in a neonate with X/XY mosaicism. Am J Surg Pathol 1986;10:577-581 13. Crump WD: Juvenile granulosa cell (sex cord-stromal) tumor of fetal testis. J Urol 1983;129:1057-1058 14. Kaplan GW, Cromie WJ, Kelalis PP: Gonadal stromal
tumors: A report of the prepuberted testicular tumors registry. J Urol 1986;136:300-301 15. Uehling DT, Smith JE, Logan R, et al: Newborn granulosa cell tumor of the testis. J Urol 1987;138:385-386 16. Due W, Dieckmann KP, Niedobitek G, et al: Testicular sex cord stromal tumor with granulosa cell differentiation: Detection of steroid hormone receptors as a possible basis for tumor development and therapeutic management. J Clin Pathol 1990; 43:732-737 17. Ulbright TM, Amin MB, Young RH: Granulosa-stromal cell tumors, in tumors of the testis, adnexa, spermatic cord, and scrotum, in Ulbright TM, Amin MB, Young RH (eds): Atlas of Tumor Pathology, third series, fascle 25. Washington, DC, Armed Forces Institute of Pathology, 1999, pp 219-233 18. Mostofi FK, Theiss EA, Ashley DJB: Tumors of specialized gonadal stroma in human male subjects. Cancer 1959;12:944957
S
INCE THE first testicular granulosa cell tumor (GCT) was reported in 1952, isolated case reports and small serial studies have been described.1-4 These rare neoplasms are comparable to the GCT found in the ovary, although far less common than their ovarian counterparts.5 Since that time, two separate types of testicular GCT have been identified: the adult type (rare) and the juvenile type (more frequent).2-4,6 Pure classic GCTs are exceedingly rare in the testis.2,6 Most of these tumors occurred in asymptomatic men; only a few cases had signs and symptoms associated with hormonal disturbances such as estrogen over-secretion7 or congenital anomalies.8 The biologic behavior of the testicular GCT appears to be somewhat less aggressive than that of its homologous ovarian counterpart5,9; however, it may be an indolent entity with unpredictable outcome.2,3,8,10
From the Lilian and Henry M. Stratton-Hans Popper Department of Pathology, The Mount Sinai School of Medicine, The Mount Sinai Medical Center, New York; and the Department of Genitourology, The Mount Sinai Hospital of Queens, New York, NY. Address reprint requests to Pamela D. Unger, MD, Department of Pathology, The Mount Sinai School of Medicine, The Mount Sinai Medical Center. New York, NY 10029. Copyright © 2002 by W.B. Saunders Company 1092-9134/02/0601-0004$35.00/0 doi:10.1053/adpa.2002.30607
56
The morphology of adult GCT of testis is similar to those identified in the ovaries; however, it may cause diagnostic difficulties for pathologists. Unlike other nongerm cell tumors in the testis or sex cord stromal tumors, testicular GCT may be confused with other tumors such as malignant lymphoma. We report a case of gonadal tumor of testis with GCT differentiation, which was misdiagnosed as malignant lymphoma on frozen section. The histologic features of testicular GCT and relevant differential diagnoses are discussed. Case History A 54-year-old healthy white man presented in the genitourology clinic at The Mount Sinai Hospital of Queens, New York, NY for routine examination. Physical examination showed a well-developed male with no apparent abnormalities except for mild left testicular hydrocele. An ultrasound evaluation disclosed a dime-sized painless mobile soft nodule within the left testis. The duration of the nodule was not known. His past medical history was only remarkable for hypertension. Preoperative laboratory tests were unremarkable. Clinically, the lesion was felt to be a neoplasm and the patient was scheduled for an orchiectomy. During the procedure, the nodule appeared to be encapsulated and was easily enucleated. The entire lesion was 1.6⫻1.5⫻1.5 cm and was submitted for frozen section. Touch imprints and frozen sections showed uniform small lymphocyte-like cells, most of which contain cleaved nuclei (Fig1). The frozen section diagnosis was reported as malignant lym-
Annals of Diagnostic Pathology, Vol 6, No 1 (February), 2002: pp 56-60
Gonadal Tumor in an Adult Testis
57
Figure 1. Microphotograph of touch imprints showing the tumor composed of uniform small cells with “coffee bean” shaped nuclear grooves (arrows). The cytopasmic outlines are indistinct. (DiffQick Giemsa stain.)
phoma. Subsequently, a left radical orchiectomy specimen was received which did not show any additional lesions. The patient recovered uneventfully.
Pathology Results Gross Examination On cut surface, the testis was 3.5⫻⫻3.0⫻2.6 cm and contained a well-circumscribed homogeneous tan soft nodule. The nodule measured 1.6⫻1.5⫻1.5 cm in size and was confined within the testicular parenchyma. The remainder of the testis showed unremarkable testicular texture. The tunica albuginea and the attached spermatic cord and epididymis appeared unremarkable.
Histologic Examination Morphologic evaluation was based on paraffin embedded tissue and hematoxylin-eosin stained sections. The tumor was composed of uniform small cells, most of which exhibited nuclear grooves. This feature was better appreciated on touch imprints with DiffQick (RichardAllan Scientific, Kalamazoo, MI) Giemsa stain (Fig 1). On tissue sections, the tumor cells were arranged in cords, small nests, and microfollicles with occasional entrapped seminiferous tubules (Fig 2). In addition, other areas of the tumor showed Call-Exner body-like formation (Fig 3). The tumor was confined to the testis. The remainder of the testis, epididymis, and spermatic cord showed no significant pathology.
Immunohistochemical Studies The tumor cells were positive for low molecular weight cytokeratin (Cam 5.2: Becton Dickinson; Mountain View,
CA), strongly positive for vimentin, and negative for placental alkaline phosphatase (Dako; Carpinteria, CA), alpha fetoprotein (Dako), leukocyte common antigen (Dako), estrogen receptor (Dako), and progesterone receptor (Zymed, South San Francisco, CA). Inhibin stain was not available. The results of tumor immunoreactivity excluded the differential diagnoses of malignant lymphoma and germ cell tumors. The findings support the diagnoses of testicular gonadal stromal tumor with granulosa cell features.
Discussion Granulosa cell tumor in the testis is rare and its morphology is similar to the conventional GCT of the ovary.2-4 The majority of affected adult male patients were white and asymptomatic.4,11 These tumors were often discovered incidentally, were of unknown duration, and exhibited no endocrinerelated symptoms.11 Only a few cases of testicular GCT were reported with associated gynecomastia or chromosomal anomalies7, 8,12,13; however, it has not been described that there is an obvious relation between tumor morphology and endocrine function in the literature. Ovarian GCT accounts for 5% of all ovarian tumors, 5% of which occur before puberty as juvenile GCT and 40% in the postmenopausal group as the adult type. Less than 5% are bilateral.2,4,11 Unlike most ovarian GCTs of the adult type, testicular GCTs are mainly of the juvenile type. Juvenile GCT is a relatively common sex cord stromal neoplasm that has been estimated to comprise about
58
Wang et al
Figure 2. Low magnification of the tumor showing the tumor cells arranged in cords and nests with an entrapped seminiferous tubule (arrow).
15% of gonadal stromal tumors of the infantile testis, with a peak incidence during the first months of life.4,6,10,14,15 Although the adult type of GCT in the ovary involves predominantly postmenopausal women, it can be found in the testes of both young
Figure 3. High magnification of the tumor showing some areas with CallExner body-like structures (arrows).
and older males, with as average age around 42.5 years.6,11 It usually produces estrogens in both sexes.6,7,9 Testicular GCT shares similar histology with ovarian GCT. Most testicular GCTs described are well
Gonadal Tumor in an Adult Testis
circumscribed, yellow to gray, with a solid to partially cystic appearance. Microscopically, they have a variety of morphologies including the typical patterns of ovarian GCT such as solid, cystic, microfollicular, gyriform, insular, and trabecular patterns. Call-Exner bodies are present in some cases. Tumor cells may exhibit the usual pale nuclei with occasional or frequent nuclear grooves. Rare cases show surrounding testicular parenchyma with Leydig cell hyperplasia and a Sertoli cell nodule.2,4,11 Our current case showed tumor growth in cords and nests with microfollicles and Call-Exner body formation (Figs 2, 3). These architectural patterns are characteristics of GCT of the adult type. Histologic features do not always predict the clinical course of the tumor. However, in rare cases, a potentially malignant tumor should be suspected if the tumor is more than 7cm, necrotic, hemorrhagic, or shows vascular/lymphatic invasion.6,7,9,11 A panel of immunohistochemical markers may aid in the diagnosis. The immunologic features of GCT usually include strong immunoreactivity for vimentin, variable results for cytokeratin, and negative for epithelial membrane antigen.4,11 Our case was positive for vimentin and cytokeratin Cam 5.2, negative for leukocyte common antigens, placental alkaline phosphatase, and alpha fetoprotein. Estrogen receptor/progesterone receptor are expressed by testicular sex cord stromal tumor with GCT differentiation of adult type,4,16 both antibodies were nonimmunoreactive in our case. In this particular case, one should emphasize that tumor cytology on frozen section mimicked malignant lymphoma (Fig1). In such a situation, leukocyte common antigen plays an important role. The immunohistochemical profile can easily exclude malignant lymphoma and germ cell tumors. Because of the relative rarity and heterogeneity of testicular stromal tumors, these tumors frequently pose diagnostic problems for pathologists. One should pay attention to the histologic features and try to eliminate differential diagnoses. Certain patterns of GCT, such as microfollicular, are so distinctive that diagnostic problems do not arise when this pattern is accompanied by the typical cytologic features of neoplastic granulosa cells.6 The diagnosis is more likely to be problematic when a diffuse pattern is present; in such cases appreciation of the characteristic cytological features is extremely helpful.6 Clinically, the behavior of testicular GCT is
59
thought to be benign, with occasional cases being indolent with unpredictable behavior. However, rare cases were reported to be malignant with metastasis.2,6,7,9,11 Mostofi et al18 reported a malignant testicular GCT as high as 10%. It is said that the prognosis of the adult type of GCT is worse in the ovary than in the testis in general.5,17,18 Ovarian GCT is sometimes associated with metastatic disease occurring 5 to 20 years after excision of the primary tumor.5 However, in the case reported by Matoska et al,9 metastatic spread had occurred only 7 months after the tumor was noticed. Therefore, it is mandatory to rule out the presence of metastatic spread and staging of the disease after orchiectomy through careful investigation. In summary, our findings and a review of the literature indicate that GCT of the adult testis is a rare and slow-growing neoplasm. Morphologically, it may mimic other types of testicular neoplasms. The rarity of this entity should not preclude an accurate diagnosis, which will provide correct information for clinicians to take appropriate clinical management. Clinically, it may have uncertain potential to form distant metastases. Because recurrence or distant metastasis may occur late in the clinical course, long-term follow-up is warranted. Acknowledgement The authors greatly appreciate Norman Katz and Micha Zeffren for their excellent photographic assistance, and Dr Lorraine Miller for providing immunomarker studies.
References 1. Laskowski J: Feminizing tumors of the testis: General review with case report of granulosa cell tumor of testis. Endokrynol Pol 1995;3:337-343 2. Talerman A: Pure granulosa cell tumor of the testis. Report of a case and review of the literature. Appl Pathol 1985;3:117122 3. Gaylis FD, August C, Yeldandi A, et al: Granulosa cell tumor of the adult testis: Ultrastructural and ultrasonographic characteristics. J Urol 1989;141:126-127 4. Nistal M, Lazaro R, Garcia J, et al: Testicular granulosa cell tumor of the adult type. Arch Pathol Lab Med 1992;116:284-287 5. Scully RE: Tumors of the ovary and maldeveloped gonalds, fallopian tube and round ligment. in Rosai J, Sobin LH (eds). Atlas of Tumor Pathology, Fascicle 23. Washington, DC, Armed Forces Institute of Pathology, 1998, pp 169-186 6. Young RH, Talerman A: Testicular tumors other than germ cell tumors. Semin Diagn Pathol 1987;4:342-360 7. Dilworth JP, Farrow GM, Pesterling JE: Non-germ cell tumors of testis. Urology 1991;37:399-417 8. Cohen J, Diamond J: Leontiasis Ossea, slipped epiphyses.
60
Wang et al
Granulosa cell tumor of the testis with renal disease: Report of case with autopsy findings. Arch Pathol 1953;56:488-500 9. Matoska J, Ondrus O, Talerman A: Malignant granulosa cell tumor of the testis associated gynecomastia and long survival. Cancer 1991;69:1769-1772 10. Lawrence WD, Young RH, Scully RE: Juvenile granulosa cell tumor of the infantile testis: A report of 14 cases. Am J Surg Pathol 1985;9:87-94 11. Jimenez-Quintero LP, Ro JY, Zavala-Pompa A, et al: Granulosa cell tumor of the adult testis: A clinicopathologic study of seven cases and a review of the literature. Hum Pathol 1993;24: 1120-1126 12. Raju U: Congenital testicular juvenile granulosa cell tumor in a neonate with X/XY mosaicism. Am J Surg Pathol 1986;10:577-581 13. Crump WD: Juvenile granulosa cell (sex cord-stromal) tumor of fetal testis. J Urol 1983;129:1057-1058 14. Kaplan GW, Cromie WJ, Kelalis PP: Gonadal stromal
tumors: A report of the prepuberted testicular tumors registry. J Urol 1986;136:300-301 15. Uehling DT, Smith JE, Logan R, et al: Newborn granulosa cell tumor of the testis. J Urol 1987;138:385-386 16. Due W, Dieckmann KP, Niedobitek G, et al: Testicular sex cord stromal tumor with granulosa cell differentiation: Detection of steroid hormone receptors as a possible basis for tumor development and therapeutic management. J Clin Pathol 1990; 43:732-737 17. Ulbright TM, Amin MB, Young RH: Granulosa-stromal cell tumors, in tumors of the testis, adnexa, spermatic cord, and scrotum, in Ulbright TM, Amin MB, Young RH (eds): Atlas of Tumor Pathology, third series, fascle 25. Washington, DC, Armed Forces Institute of Pathology, 1999, pp 219-233 18. Mostofi FK, Theiss EA, Ashley DJB: Tumors of specialized gonadal stroma in human male subjects. Cancer 1959;12:944957