Sex Cord-Stromal Tumors of the Ovary: An Update and Review. Part II - Pure Sex Cord and Sex Cord-Stromal Tumors.
Journal
Advances in anatomic pathology
ISSN: 1533-4031
Titre abrégé: Adv Anat Pathol
Pays: United States
ID NLM: 9435676
Informations de publication
Date de publication:
29 Feb 2024
29 Feb 2024
Historique:
medline:
29
2
2024
pubmed:
29
2
2024
entrez:
29
2
2024
Statut:
aheadofprint
Résumé
We review the time honored but still frequently challenging features of ovarian sex cord-stromal tumors and also emphasize new developments, including unusual morphologic appearances that, despite the relative rarity of many of the tumors, result in a disproportionate number of differential diagnostic problems, variant immunohistochemical profiles, and specific molecular and syndromic associations. These neoplasms are also of historical interest as current knowledge is still based in significant part to the contributions of 2 giants of gynecologic pathology, Dr Robert Meyer and Dr. Robert E. Scully. In part I, we reviewed the pure ovarian stromal tumors. Now, in part II, we present the major clinical, pathologic, and genomic features of pure sex cord and sex cord-stromal tumors.
Identifiants
pubmed: 38420747
doi: 10.1097/PAP.0000000000000436
pii: 00125480-990000000-00092
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
Copyright © 2024 Wolters Kluwer Health, Inc. All rights reserved.
Déclaration de conflit d'intérêts
The authors have no funding or conflicts of interest to disclose.
Références
Lee IH, Choi CH, Hong DG, et al. Clinicopathologic characteristics of granulosa cell tumors of the ovary: a multicenter retrospective study. J Gynecol Oncol. 2011;22:188–195.
Ottolina J, Ferrandina G, Gadducci A, et al. Is the endometrial evaluation routinely required in patients with adult granulosa cell tumors of the ovary? Gynecol Oncol. 2015;136:230–234.
Nakashima N, Young RH, Scully RE. Androgenic granulosa cell tumors of the ovary. A clinicopathologic analysis of 17 cases and review of the literature. Arch Pathol Lab Med. 1984;108:786–791.
Young RH, Dudley AG, Scully RE. Granulosa cell, Sertoli-Leydig cell, and unclassified sex cord-stromal tumors associated with pregnancy: a clinicopathological analysis of thirty-six cases. Gynecol Oncol. 1984;18:181–205.
Oge T, Ozalp SS, Yalcin OT, et al. Ruptured granulosa cell tumor of the ovary as a cause of acute abdomen in postmenopausal woman. Case Rep Oncol Med. 2012;2012:451631.
Mom CH, Engelen MJA, Willemse PHB, et al. Granulosa cell tumors of the ovary: the clinical value of serum inhibin A and B levels in a large single center cohort. Gynecol Oncol. 2007;105:365–372.
Sun HD, Lin H, Jao MS, et al. A long-term follow-up study of 176 cases with adult-type ovarian granulosa cell tumors. Gynecol Oncol. 2012;124:244–249.
Bryk S, Farkkila A, Butzow R, et al. Clinical characteristics and survival of patients with an adult-type ovarian granulosa cell tumor: a 56-year single-center experience. Int J Gynecol Cancer. 2015;25:33–41.
Bryk S, Farkkila A, Butzow R, et al. Characteristics and outcome of recurrence in molecularly defined adult-type ovarian granulosa cell tumors. Gynecol Oncol. 2016;143:571–577.
Wilson MK, Fong P, Mesnage S, et al. Stage I granulosa cell tumours: a management conundrum? Results of long-term follow up. Gynecol Oncol. 2015;138:285–291.
Hines JF, Khalifa MA, Moore JL, et al. Recurrent granulosa cell tumor of the ovary 37 years after initial diagnosis: a case report and review of the literature. Gynecol Oncol. 1996;60:484–488.
Portuesi R, Loppini A, Mancari R, et al. Role of inhibin B in detecting recurrence of granulosa cell tumors of the ovary in postmenopausal patients. Int J Gynecol Cancer. 2021;31:893–898.
Groeneweg JW, Roze JF, Peters EDJ, et al. FOXL2 and TERT promoter mutation detection in circulating tumor DNA of adult granulosa cell tumors as biomarker for disease monitoring. Gynecol Oncol. 2021;162:413–420.
Farkkila A, McConechy MK, Yang W, et al. FOXL2 402C>G mutation can be identified in the circulating tumor DNA of patients with adult-type granulosa cell tumor. J Mol Diagn. 2017;19:126–136.
Boyraz B, Watkins JC, Soubeyran I, et al. Cystic granulosa cell tumors of the ovary: an analysis of 80 cases of an often diagnostically challenging entity. Arch Pathol Lab Med. 2022;146:1450–1459.
Irving JA, Young RH. Granulosa cell tumors of the ovary with a pseudopapillary pattern: a study of 14 cases of an unusual morphologic variant emphasizing their distinction from transitional cell neoplasms and other papillary ovarian tumors. Am J Surg Pathol. 2008;32:581–586.
Stall JN, Young RH. Granulosa cell tumors of the ovary with prominent thecoma-like foci: a report of 16 cases emphasizing the ongoing utility of the reticulin stain in the modern era. Int J Gynecol Pathol. 2019;38:143–150.
Buza N, Wong S, Hui P. FOXL2 mutation analysis of ovarian sex cord-stromal tumors: genotype-phenotype correlation with diagnostic considerations. Int J Gynecol Pathol. 2018;37:305–315.
Devins KM, Young RH. Sclerosis in sex cord-stromal tumors other than the sclerosing stromal tumor: a report of 70 cases. Am J Surg Pathol. 2023;47:774–784.
The WHO classification of tumors editorial board. WHO Classification of Tumours Editorial Board Female Genital Tumours, 5th ed. International Agency for Research on Cancer; 2020.
Young RH, Oliva E, Scully RE. Luteinized adult granulosa cell tumors of the ovary: a report of four cases. Int J Gynecol Pathol. 1994;13:302–310.
Ganesan R, Hirschowitz L, Baltrusaityte I, et al. Luteinized adult granulosa cell tumor--a series of 9 cases: revisiting a rare variant of adult granulosa cell tumor. Int J Gynecol Pathol. 2011;30:452–459.
Young RH, Scully RE. Ovarian sex cord-stromal tumors with bizarre nuclei: a clinicopathologic analysis of 17 cases. Int J Gynecol Pathol. 1983;1:325–335.
Gaffey MJ, Frierson HF Jr, Iezzoni JC, et al. Ovarian granulosa cell tumors with bizarre nuclei: an immunohistochemical analysis with fluorescence in situ hybridization documenting trisomy 12 in the bizarre component. Mod Pathol. 1996;9:308–315.
Ahmed E, Young RH, Scully RE. Adult granulosa cell tumor of the ovary with foci of hepatic cell differentiation: a report of four cases and comparison with two cases of granulosa cell tumor with Leydig cells. Am J Surg Pathol. 1999;23:1089–1093.
Nogales FF, Concha A, Plata C, et al. Granulosa cell tumor of the ovary with diffuse true hepatic differentiation simulating stromal luteinization. Am J Surg Pathol. 1993;17:85–90.
Dickersin GR, Young RH, Scully RE. Signet-ring stromal and related tumors of the ovary. Ultrastruct Pathol. 1995;19:401–419.
Taylor J, McCluggage WG. Ovarian sex cord-stromal tumors with melanin pigment: report of a previously undescribed phenomenon. Int J Gynecol Pathol. 2019;38:92–96.
Andrade LALA, Alame M, Truffaux N, et al. Adult granulosa cell tumour with heterologous adipocytic differentiation: report of a unique case. Int J Gynecol Pathol. 2023;42:508–513.
Fashedemi Y, Coutts M, Wise O, et al. Adult granulosa cell tumor with high-grade transformation: report of a series with FOXL2 mutation analysis. Am J Surg Pathol. 2019;43:1229–1238.
Stewart CJR, Amanuel B, De Kock L, et al. Evaluation of molecular analysis in challenging ovarian sex cord-stromal tumours: a review of 50 cases. Pathology. 2020;52:686–693.
Zhao C, Vinh TN, McManus K, et al. Identification of the most sensitive and robust immunohistochemical markers in different categories of ovarian sex cord-stromal tumors. Am J Surg Pathol. 2009;33:354–366.
Al-Agha OM, Huwait HF, Chow C, et al. FOXL2 is a sensitive and specific marker for sex cord-stromal tumors of the ovary. Am J Surg Pathol. 2011;35:484–494.
Alexiadis M, Eriksson N, Jamieson S, et al. Nuclear receptor profiling of ovarian granulosa cell tumors. Horm Cancer. 2011;2:157–169.
Shaker N, Chen W, Sinclair W, et al. Identifying SOX17 as a sensitive and specific marker for ovarian and endometrial carcinomas. Mod Pathol. 2023;36:100038.
Oliva E, Garcia-Miralles N, Vu Q, et al. CD10 expression in pure stromal and sex cord-stromal tumors of the ovary: an immunohistochemical analysis of 101 cases. Int J Gynecol Pathol. 2007;26:359–367.
Costa MJ, Morris R, Sasano H. Sex steroid biosynthesis enzymes in ovarian sex-cord stromal tumors. Int J Gynecol Pathol. 1994;13:109–119.
McCluggage WG, McKenna M, McBride HA. CD56 is a sensitive and diagnostically useful immunohistochemical marker of ovarian sex cord-stromal tumors. Int J Gynecol Pathol. 2007;26:322–327.
Shah SP, Kobel M, Senz J, et al. Mutation of FOXL2 in granulosa cell tumors of the ovary. NEJM. 2009;260:2719–2729.
Zannoni GF, Improta G, Petrillo M, et al. FOXL2 molecular status in adult granulosa cell tumors of the ovary: a study of primary and metastatic cases. Oncol Lett. 2016;12:1159–1163.
Nolan A, Joseph NM, Sangoi AR, et al. FOXL2 mutation status in granulosa theca cell tumors of the ovary. Int J Gynecol Pathol. 2017;36:568–574.
Roze J, Monroe G, Kutzera J, et al. Whole genome analysis of ovarian granulosa cell tumors reveals tumor heterogeneity and a high-grade TP53-specific subgroup. Cancers (Basel). 2020;12:1308.
Goulvent T, Ray-Coquard I, Borel S, et al. DICER1 and FOXL2 mutations in ovarian sex cord-stromal tumours: a GINECO Group study. Histopathology. 2016;68:279–285.
Karnezis AN, Wang Y, Keul J, et al. DICER1 and FOXL2 mutation status correlates with clinicopathologic features in ovarian sertoli-leydig cell tumors. Am J Surg Pathol. 2019;43:628–638.
Hillman RT, Celestino J, Terranova C, et al. KMT2D/MLL2 inactivation is associated with recurrence in adult-type granulosa cell tumors of the ovary. Nat Commun. 2018;9:2496.
Pilsworth JA, Cochrane DR, Xia Z, et al. TERT promoter mutation in adult granulosa cell tumor of the ovary. Mod Pathol. 2018;31:1107–1115.
Da Cruz Paula A, da Silva EM, Segura SE, et al. Genomic profiling of primary and recurrent adult granulosa cell tumors of the ovary. Mod Pathol. 2020;33:1606–1617.
Alexiadis M, Rowley SM, Chu S, et al. Mutational landscape of ovarian adult granulosa cell tumors from whole exome and targeted TERT promoter sequencing. Mol Cancer Res. 2019;17:177–185.
Young RH, Dickersin GR, Scully RE. Juvenile granulosa cell tumor of the ovary: a clinicopathologic analysis of 125 cases. Am J Surg Pathol. 1984;8:575–596.
Talerman A, Hughesdon PE, Anderson MC. Diffuse nonlobular ovarian androblastoma usually associated with feminization. Int J Gynecol Pathol. 1982;1:155–171.
Young RH, Prat J, Scully RE. Ovarian endometrioid carcinomas resembling sex cord-stromal tumors: a clinicopathological analysis of 13 cases. Am J Surg Pathol. 1982;6:513–522.
Young RH. Ovarian sex cord-stromal tumours and their mimics. Pathology. 2018;50:5–15.
McCluggage WG, Oliva E, Connolly LE, et al. An immunohistochemical analysis of ovarian small cell carcinoma of hypercalcemic type. Int J Gyncol Pathol. 2004;23:330–336.
Young RH, Scully RE. Malignant melanoma metastatic to the ovary: a clinicopathologic analysis of 20 cases. Am J Surg Pathol. 1991;15:849–860.
Oliva E, Egger JF, Young RH. Primary endometrioid stromal sarcoma of the ovary: a clinicopathologic study of 27 cases with morphologic and behavioral features similar to those of uterine low-grade endometrial stromal sarcoma. Am J Surg Pathol. 2014;38:305–315.
Young RH, Scully RE. Sarcomas metastatic to the ovary: a report of 21 cases. Int J Gynecol Pathol. 1990;9:231–252.
Clement PB, Young RH, Scully RE. Ovarian granulosa cell proliferations of pregnancy: a report of nine cases. Hum Pathol. 1988;19:657–662.
Scully RE. Tumors of the Ovary and Maldeveloped Gonads. Armed Forces Institute of Pathology; 1979.
Zaloudek C, Norris HJ. Granulosa tumors of the ovary in children: a clinical and pathologic study of 32 cases. Am J Surg Pathol. 1982;6:513–522.
Zaloudek C, Norris HJ. Sertoli-Leydig tumors of the ovary: a clinicopathologic study of 64 intermediate and poorly differentiated neoplasms. Am J Surg Pathol. 1984;8:405–418.
Parikshaa G, Ariba Z, Pranab D, et al. Juvenile granulosa cell tumor of the ovary: a comprehensive clinicopathologic analysis of 15 cases. Ann Diagn Pathol. 2021;52:151721.
Smith R, Moss J, Shore I, et al. Juvenile granulosa cell tumour with hepatocyte-like cells and raised serum alpha-fetoprotein. Histopathology. 2010;57:637–641.
Schultz KAP, Pacheco MC, Yang J, et al. Ovarian sex cord-stromal tumors, pleuropulmonary blastoma, and DICER1 mutations: a report from the International Pleuropulmonary Blastoma Registry. Gynecol Oncol. 2011;122:246–250.
Lim D, Oliva E. Gynecological neoplasms associated with paraneoplastic hypercalcemia. Semin Diagn Pathol. 2019;36:246–259.
Bergamini A, Ferrandina G, Candotti G, et al. Stage I juvenile granulosa cell tumors of the ovary: a multicentre analysis from the MITO-9 study. Eur J Surg Oncol. 2021;47:1705–1709.
Ndhlovu E, Liu L, Dai J, et al. Retrospective analysis of clinicopathological characteristics of 19 ovarian juvenile granulosa cell tumor cases. J Obs Gynaecol Res. 2021;47:2492–2499.
Zhao D, Song Y, Zhang Y, et al. Outcomes of fertility-sparing surgery in ovarian juvenile granulosa cell tumor. Int J Gynecol Cancer. 2019;29:787–791.
Calaminus G, Wessalowski R, Harms D, et al. Juvenile granulosa cell tumors of the ovary in children and adolescents: results from 33 patients registered in a prospective cooperative study. Gynecol Oncol. 1997;65:447–452.
Conlon N, Silva A, Guerra E, et al. Loss of SMARCA4 expression is both sensitive and specific for the diagnosis of small cell carcinoma of ovary, hypercalcemic type. Am J Surg Pathol. 2016;40:395–403.
Bessiere L, Todeschini AL, Auguste A, et al. A hot-spot of in-frame duplications activates the oncoprotein AKT1 in juvenile granulosa cell tumors. EBioMedicine. 2015;2:421–431.
Heravi-Moussavi A, Anglesio M, Cheng SWG, et al. Recurrent somatic DICER1 mutations in nonepithelial ovarian cancers. N Eng J Med. 2012;366:234–242.
Kalfa N, Ecochard A, Patte C, et al. Activating mutations of the stimulatory G protein in juvenile ovarian granulosa cell tumors: a new prognostic factor? J Clin Endrinol Metab. 2006;91:1842–1847.
Baillard P, Genestie C, Croce S, et al. Rare DICER1 and absent FOXL2 mutations characterize ovarian juvenile granulosa cell tumors. Am J Surg Pathol. 2021;45:223–229.
Vougiouklakis T, Zhu K, Vasudevaraja V, et al. Integrated analysis of ovarian juvenile granulosa cell tumors reveals distinct epigenetic signatures and recurrent TERT rearrangements. Clin Cancer Res. 2022;28:1724–1733.
McCluggage WG. Immunoreactivity of ovarian juvenile granulosa cell tumours with epithelial membrane antigen. Histopathology. 2005;46:235–236.
Ramos P, Karnezis AN, Hendricks WP, et al. Loss of the tumor suppressor SMARCA4 in small cell carcinoma of the ovary, hypercalcemic type (SCCOHT). Rare Dis. 2014;2:e967148.
Ramos P, Karnezis AN, Craig DW, et al. Small cell carcinoma of the ovary, hypercalcemic type, displays frequent inactivating germline and somatic mutations in SMARCA4. Nat Genet. 2014;46:427–429.
Simoes MFE, da Costa AABA, Silva TN, et al. Case report of small cell carcinoma of the ovary, hypercalcemic type (ovarian rhabdoid tumor) with SMARCB1 mutation: a literature review of a rare and aggressive condition. Curr Oncol. 2022;29:411–422.
Young RH, Wong A, Stall JN. Yolk sac tumor of the ovary: a report of 150 cases and review of the literature. Am J Surg Pathol. 2022;46:309–325.
Safdar NS, Stall JN, Young RH. Malignant mixed germ cell tumors of the ovary: an analysis of 100 cases emphasizing the frequency and interrelationships of their tumor types. Am J Surg Pathol. 2021;45:727–741.
Jones MW, Harri R, Dabbs DJ, et al. Immunohistochemical profile of steroid cell tumor of the ovary: a study of 14 cases and a review of the literature. Int J Gynecol Pathol. 2010;29:315–320.
Burandt EC, Young RH. Pregnancy luteoma: a study of 20 cases on the occasion of the 50th anniversary of entity’s description by Dr William H. Sternberg, with an emphasis on the common presence of follicle-like spaces and their diagnostic implications. Am J Surg Pathol. 2014;38:239–244.
Ordulu Z, Young RH. Sertoli-Leydig cell tumors of the ovary with follicular differentiation often resembling juvenile granulosa cell tumor: a report of 38 cases including comments on sex cord-stromal tumors of mixed forms (so-called gynandroblastoma). Am J Surg Pathol. 2021;45:59–67.
Wang Y, Karnezis AN, Magrill J, et al. DICER1 hot-spot mutations in ovarian gynandroblastoma. Histopathology. 2018;73:306–313.
Young RH, Scully RE. Ovarian Sertoli cell tumors: a report of 10 cases. Int J Gynecol Pathol. 1984;2:349–363.
Oliva E, Alvarez T, Young RH. Sertoli cell tumors of the ovary: a clinicopathologic and immunohistochemical study of 54 cases. Am J Surg Pathol. 2005;29:143–156.
Tavassoli FA, Norris HJ. Sertoli tumors of the ovary. A clinicopathologic study of 28 cases with ultrastructural observations. Cancer. 1980;46:2281–2297.
Ravishankar S, Mangray S, Kurkchubasche A, et al. Unusual Sertoli cell tumor associated with sex cord tumor with annular tubules in Peutz-Jeghers syndrome: report of a case and review of the literature on ovarian tumors in Peutz-Jeghers syndrome. Int J Surg Pathol. 2016;24:269–273.
Ferry JA, Young RH, Engel G, et al. Oxyphilic Sertoli cell tumor of the ovary: a report of three cases, two in patients with the Peutz-Jeghers syndrome. Int J Gynecol Pathol. 1994;13:259–266.
Christian E. Un cas d’epitheliome a granulations de luteive d’origine probablement ovarienne. Soc Anat Ann. 1910;12:639–641.
Zhao C, Barner R, Vinh TN, et al. SF-1 is a diagnostically useful immunohistochemical marker and comparable to other sex cord-stromal tumor markers for the differential diagnosis of ovarian sertoli cell tumor. Int J Gynecol Pathol. 2008;27:507–514.
Zhao C, Bratthauer GL, Barner R, et al. Diagnostic utility of WT1 immunostaining in ovarian sertoli cell tumor. Am J Surg Pathol. 2007;31:1378–1386.
Zhao C, Bratthauer GL, Barner R, et al. Comparative analysis of alternative and traditional immunohistochemical markers for the distinction of ovarian sertoli cell tumor from endometrioid tumors and carcinoid tumor: a study of 160 cases. Am J Surg Pathol. 2007;31:255–266.
Kato N, Fukase M, Ono I, et al. Sertoli-stromal cell tumor of the ovary: immunohistochemical, ultrastructural, and genetic studies. Hum Pathol. 2001;32:796–802.
Conlon N, Schultheis AM, Piscuoglio S, et al. A survey of DICER1 hotspot mutations in ovarian and testicular sex cord-stromal tumors. Mod Pathol. 2015;28:1603–1612.
Lim D, Oliva E. Ovarian sex cord-stromal tumours: an update in recent molecular advances. Pathology. 2018;50:178–189.
Roth LM, Liban E, Czernobilsky B. Ovarian endometrioid tumors mimicking Sertoli and Sertoli-Leydig cell tumors: Sertoliform variant of endometrioid carcinoma. Cancer. 1982;50:1322–1331.
Ordi J, Schammel DP, Rasekh L, et al. Sertoliform endometrioid carcinomas of the ovary: a clinicopathologic and immunohistochemical study of 13 cases. Mod Pathol. 1999;12:933–940.
McCluggage WG, Stewart CJR, Iacobelli J, et al. Microscopic extraovarian sex cord proliferations: an undescribed phenomenon. Histopathology. 2015;66:555–564.
Young RH, Scully RE. Ovarian Sertoli-Leydig cell tumors: a clinicopathological analysis of 207 cases. Am J Surg Pathol. 1985;9:543–569.
McCluggage WG, Rivera B, Chong AS, et al. Well-differentiated Sertoli-Leydig cell tumors (SLCTs) are not associated with DICER1 pathogenic variants and represent a different tumor type to moderately and poorly differentiated SLCTs. Am J Surg Pathol. 2023;47:490–496.
Young RH, Scully RE. Well-differentiated ovarian Sertoli-Leydig cell tumors: a clinicopathological analysis of 23 cases. Int J Gynecol Pathol. 1984;3:277–290.
Gui T, Cao D, Shen K, et al. A clinicopathological analysis of 40 cases of ovarian Sertoli-Leydig cell tumors. Gynecol Oncol. 2012;127:384–389.
Sigismondi C, Gadducci A, Lorusso D, et al. Ovarian Sertoli-Leydig cell tumors: a retrospective MITO study. Gynecol Oncol. 2012;125:673–676.
Strus M, Rajtar-Ciosek A, Jach R, et al. Ovarian Sertoli-Leydig cell tumour with α-fetoprotein-producing intestinal glandular cells. Clinical case and short review of basic literature. Pol J Pathol. 2019;70:226–231.
Young RH, Perez-Atayde AR, Scully RE. Ovarian Sertoli-Leydig cell tumor with retiform and heterologous components. Report of a case with hepatocytic differentiation and elevated serum alpha-fetoprotein. Am J Surg Pathol. 1984;8:709–718.
Al-Hussaini M, Al-Othman Y, Hijazi E, et al. A report of ovarian Sertoli-Leydig cell tumors with heterologous intestinal-type glands and alpha fetoprotein elevation and review of the literature. Int J Gynecol Pathol. 2018;37:275–283.
Watanabe T, Yamada H, Morimura Y, et al. Ovarian Sertoli-Leydig cell tumor with heterologous gastrointestinal epithelium as a source of alpha-fetoprotein: a case report. J Obs Gynaecol Res. 2008;34:418–421.
Chadha S, Honnebier WJ, Schaberg A. Raised serum alpha-fetoprotein in Sertoli-Leydig cell tumor (androblastoma) of ovary: report of two cases. Int J Gynecol Pathol. 1987;6:82–88.
Chan R, Tucker M, Russell P. Ovarian gynandroblastoma with juvenile granulosa cell component and raised alpha fetoprotein. Pathology. 2005;37:312–315.
Roth LM, Anderson MC, Govan AD, et al. Sertoli-Leydig cell tumors: a clinicopathologic study of 34 cases. Cancer. 1981;48:187–197.
Young RH, Scully RE. Ovarian Sertoli-Leydig cell tumors with a retiform pattern: a problem in histopathologic diagnosis. Am J Surg Pathol. 1983;7:755–771.
Young RH, Prat J, Scully RE. Ovarian Sertoli-Leydig cell tumors with heterologous elements: I. Gastrointestinal epithelium and carcinoid: a clinicopathologic analysis of thirty-six cases. Cancer. 1982;50:2448–2456.
Prat J, Young RH, Scully RE. Ovarian Sertoli-Leydig cell tumors with heterologous elements: II. Cartilage and skeletal muscle: a clinicopathologic analysis of twelve cases. Cancer. 1982;50:2465–2475.
Mooney EE, Nogales FF, Tavassoli FA. Hepatocytic differentiation in retiform Sertoli-Leydig cell tumors: distinguishing a heterologous element from Leydig cells. Hum Pathol. 1999;30:611–617.
Yamamoto S, Sakai Y. Ovarian Sertoli-Leydig cell tumor with heterologous hepatocytes and a hepatocellular carcinomatous element. Int J Gynecol Pathol. 2019;38:247–252.
de Kock L, Terzic T, McCluggage WG, et al. DICER1 mutations are consistently present in moderately and poorly differentiated Sertoli-Leydig cell tumors. Am J Surg Pathol. 2017;41:1178–1187.
Schultz KAP, Harris AK, Finch M, et al. DICER1-related Sertoli-Leydig cell tumor and gynandroblastoma: clinical and genetic findings from the International Ovarian and Testicular Stromal Tumor Registry. Gynecol Oncol. 2017;147:521–527.
Hazard FK, Longacre TA. Ovarian surface epithelial neoplasms in the pediatric population: incidence, histologic subtype, and natural history. Am J Surg Pathol. 2013;37:548–553.
Kiyokawa T, Young RH, Scully RE. Krukenberg tumors of the ovary: a clinicopathologic analysis of 120 cases with emphasis on their variable pathologic manifestations. Am J Surg Pathol. 2006;30:277–299.
Horta M, Cunha TM, Marques RC, et al. Ovarian Sertoli-Leydig cell tumor with heterologous elements of gastrointestinal type associated with elevated serum alpha-fetoprotein level: an unusual case and literature review. J Radiol Case Rep. 2014;8:30–41.
Rutgers JL, Scully RE. Functioning ovarian tumors with peripheral steroid cell proliferation: a report of twenty-four cases. Int J Gynecol Pathol. 1986;5:319–337.
Scully RE. Sex cord tumor with annular tubules a distinctive ovarian tumor of the Peutz-Jeghers syndrome. Cancer. 1970;25:1107–1121.
Young RH, Welch WR, Dickersin GR, et al. Ovarian sex cord tumor with annular tubules: review of 74 cases including 27 with Peutz-Jeghers syndrome and four with adenoma malignum of the cervix. Cancer. 1982;50:1384–1402.
Barker D, Sharma R, McIndoe A, et al. An unusual case of sex cord tumor with annular tubules with malignant transformation in a patient with Peutz-Jeghers syndrome. Int J Gynecol Pathol. 2010;29:27–32.
Lele SM, Sawh RN, Zaharopoulos P, et al. Malignant ovarian sex cord tumor with annular tubules in a patient with Peutz-Jeghers syndrome: a case report. Mod Pathol. 2000;13:466–470.
Onder S, Hurdogan O, Bayram A, et al. The role of FOXL2, SOX9, and β-catenin expression and DICER1 mutation in differentiating sex cord tumor with annular tubules from other sex cord tumors of the ovary. Virchows Arch. 2021;479:317–324.
Tan H, Mei L, Huang Y, et al. Three novel mutations of STK11 gene in Chinese patients with Peutz-Jeghers syndrome. BMC Med Genet. 2016;17:77.
Kato N, Romero M, Catasus L, et al. The STK11/LKB1 Peutz-Jegher gene is not involved in the pathogenesis of sporadic sex cord-stromal tumors, although loss of heterozygosity at 19p13.3 indicates other gene alteration in these tumors. Hum Pathol. 2004;35:1101–1104.
Connolly DC, Katabuchi H, Cliby WA, et al. Somatic mutations in the STK11/LKB1 gene are uncommon in rare gynecological tumor types associated with Peutz-Jegher’s syndrome. Am J Surg Pathol. 2000;156:339–345.
Chang RJ, Reuther J, Gandhi I, et al. Sex cord tumor with annular tubules-like histologic pattern in adult granulosa cell tumor: case report of a hitherto unreported morphologic variant. Int J Surg Pathol. 2021;29:433–437.
Feng YY, Li Z, Zhang MH. Bilateral Peutz-Jeghers-associated sex cord tumor with annular tubules combined with unilateral adult granulosa cell tumor: a case report. Int J Surg Pathol. 2023;31:1352–1358.
Seidman JD. Unclassified ovarian gonadal stromal tumors: a clinicopathologic study of 32 cases. Am J Surg Pathol. 1996;20:699–706.
Oparka R, Cassidy A, Reilly S, et al. The C134W (402 C>G) FOXL2 mutation is absent in ovarian gynandroblastoma: insights into the genesis of an unusual tumour. Histopathology. 2012;60:838–842.
Young RH. A tribute to Robert E. Scully, M.D. Int J Gynecol Pathol. 2014;33:325–329.
Young RH, Oliva E. Selected topics in gynecologic pathology honoring Robert E. Scully, M.D. His life and legacy. Int J Gynecol Pathol. 2014;33:323–324.
Young RH, Clement PB. History of gynecologic pathology: Robert E. Scully, MD. Int J Gynecol Pathol. 2016;36:2–23.
Meyer R. The pathology of some special ovarian tumors and their relation to sex characteristics. Am J Obs Gynecol. 1931;22:697–713.
Novak E. Life and works of Robert Meyer. Am J Obs Gynecol. 1947;53:50–64.
Dallenbach-Hellweg G, Schmidt D. History of gynecological pathology: Dr. Robert Meyer. Int J Gynecol Pathol. 2001;20:289–308.
Young RH. Sertoli-Leydig cell tumors of the ovary: review with emphasis on historical aspects and unusual variants. Int J Gynecol Pathol. 1993;12:141–147.
Young RH, Teilum D, Talerman A. History of gynecological pathology: Dr. Gunnar Teilum. Int J Gynecol Pathol. 2013;32:520–527.
Gruhn JG. A selective historical survey of ovarian pathology emphasizing neoplasms. In: Roth LM, Czernobilsky B, eds. Contemporary Issues in Surgical Pathology: Tumors and Tumorlike Conditions of the Ovary. Churchill Livingstone; 1985.
Young RH. A brief history of the pathology of the gonads. Mod Pathol. 2005(Suppl 2):S3–S17.
Young RH. The rich history of gynaecological pathology: brief notes on some of its personalities and their contributions. Pathology. 2007;39:6–25.
Young RH. The female reproductive system. In: Van Den Tweel J, Taylor CR, eds. From Magic to Molecules: An Illustrated History of Disease. Beijing University Press; 2016.