High-grade serous carcinoma of tubo-ovarian origin: recent developments

Histopathology

Volumn 71, Issue 3, 2017, Pages 339-356

  Singh, Naveena ^a   McCluggage, W Glenn ^b   Gilks, C Blake ^c  

^a BARTS HEALTH NHS TRUST   (United Kingdom)

^b ROYAL GROUP OF HOSPITALS TRUST   (United Kingdom)

^c VANCOUVER GENERAL HOSPITAL   (Canada)

Author keywords

diagnosis; genetic abnormalities; HGSC; high grade serous carcinoma; immunohistochemistry; pathology

Indexed keywords

CANCER CHEMOTHERAPY; CANCER CLASSIFICATION; CANCER DIAGNOSIS; CANCER LOCALIZATION; CANCER MORTALITY; CANCER PROGNOSIS; CLEAR CELL CARCINOMA; DIFFERENTIAL DIAGNOSIS; FALLOPIAN TUBE; HIGH GRADE SEROUS CARCINOMA OF TUBO OVARIAN; HISTOPATHOLOGY; HUMAN; INVASIVE CARCINOMA; MOLECULAR PATHOLOGY; MORBIDITY; OVARY CARCINOMA; PRIORITY JOURNAL; REVIEW; TRANSITIONAL CELL CARCINOMA; UNDIFFERENTIATED CARCINOMA; UTERINE TUBE CARCINOMA; CYSTADENOCARCINOMA; FEMALE; OVARY TUMOR; PATHOLOGY; UTERINE TUBE TUMOR;

CYSTADENOCARCINOMA, SEROUS; FALLOPIAN TUBE NEOPLASMS; FEMALE; HUMANS; OVARIAN NEOPLASMS;

EID: 85024401024     PISSN: 03090167     EISSN: 13652559     Source Type: Journal    
DOI: 10.1111/his.13248     Document Type: Review

References (115)

1. Gilks CB, Prat J. Ovarian carcinoma pathology and genetics: recent advances. Hum. Pathol. 2009; 40; 1213–1223.
2. World Health Organization. World Health Organization classification of tumors of the female reproductive organs. 4th ed. Lyon: International Agency for Research on Cancer (IARC), 2014.
3. Mills AM, Longacre TA. Lynch syndrome: female genital tract cancer diagnosis and screening. Surg. Pathol. Clin. 2016; 9; 201–214.
4. World Health Organization. Pathology and genetics of tumours of the breast and female genital organs. Lyon: International Agency for Research on Cancer (IARC), 2003.
5. Mackenzie R, Talhouk A, Eshragh S et al. Morphologic and molecular characteristics of mixed epithelial ovarian cancers. Am. J. Surg. Pathol. 2015; 39; 1548–1557.
6. Han G, Gilks CB, Leung S et al. Mixed ovarian epithelial carcinomas with clear cell and serous components are variants of high-grade serous carcinoma: an interobserver correlative and immunohistochemical study of 32 cases. Am. J. Surg. Pathol. 2008; 32; 955–964.
7. Kobel M, Kalloger SE, Huntsman DG et al. Differences in tumor type in low-stage versus high-stage ovarian carcinomas. Int. J. Gynecol. Pathol. 2010; 29; 203–211.
8. Bertelsen K, Holund B, Andersen E. Reproducibility and prognostic value of histologic type and grade in early epithelial ovarian cancer. Int. J. Gynecol. Cancer 1993; 3; 72–79.
9. Baak JP, Langley FA, Talerman A, Delemarre JF. Interpathologist and intrapathologist disagreement in ovarian tumor grading and typing. Anal. Quant. Cytol. Histol. 1986; 8; 354–357.
10. Cramer SF, Roth LM, Ulbright TM et al. Evaluation of the reproducibility of the World Health Organization classification of common ovarian cancers. With emphasis on methodology. Arch. Pathol. Lab. Med. 1987; 111; 819–829.
11. Lund B, Thomsen HK, Olsen J. Reproducibility of histopathological evaluation in epithelial ovarian carcinoma. Clinical implications. APMIS 1991; 99; 353–358.
12. Sakamoto A, Sasaki H, Furusato M et al. Observer disagreement in histological classification of ovarian tumors in Japan. Gynecol. Oncol. 1994; 54; 54–58.
13. Gilks CB. Subclassification of ovarian surface epithelial tumors based on correlation of histologic and molecular pathologic data. Int. J. Gynecol. Pathol. 2004; 23; 200–205.
14. Shih IM, Kurman RJ. Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am. J. Pathol. 2004; 164; 1511–1518.
15. McCluggage WG. My approach to and thoughts on the typing of ovarian carcinomas. J. Clin. Pathol. 2008; 61; 152–163.
16. Soslow RA. Histologic subtypes of ovarian carcinoma: an overview. Int. J. Gynecol. Pathol. 2008; 27; 161–174.
17. Singer G, Kurman RJ, Chang HW, Cho SK, Shih IM. Diverse tumorigenic pathways in ovarian serous carcinoma. Am. J. Pathol. 2002; 160; 1223–1228.
18. Singer G, Shih IM, Truskinovsky A, Umudum H, Kurman RJ. Mutational analysis of K-ras segregates ovarian serous carcinomas into two types: invasive MPSC (low-grade tumor) and conventional serous carcinoma (high-grade tumor). Int. J. Gynecol. Pathol. 2003; 22; 37–41.
19. Russell SE, McCluggage WG. A multistep model for ovarian tumorigenesis: the value of mutation analysis in the KRAS and BRAF genes. J. Pathol. 2004; 203; 617–619.
20. Ho CL, Kurman RJ, Dehari R, Wang TL, Shih IM. Mutations of BRAF and KRAS precede the development of ovarian serous borderline tumors. Cancer Res. 2004; 64; 6915–6918.
21. Singer G, Stohr R, Cope L et al. Patterns of p53 mutations separate ovarian serous borderline tumors and low- and high-grade carcinomas and provide support for a new model of ovarian carcinogenesis: a mutational analysis with immunohistochemical correlation. Am. J. Surg. Pathol. 2005; 29; 218–224.
22. Sieben NL, Macropoulos P, Roemen GM et al. In ovarian neoplasms, BRAF, but not KRAS, mutations are restricted to low-grade serous tumours. J. Pathol. 2004; 202; 336–340.
23. Vang R, Shih IM, Kurman RJ. Ovarian low-grade and high-grade serous carcinoma: pathogenesis, clinicopathologic and molecular biologic features, and diagnostic problems. Adv. Anat. Pathol. 2009; 16; 267–282.
24. Ahn G, Folkins AK, McKenney JK, Longacre TA. Low-grade serous carcinoma of the ovary: clinicopathologic analysis of 52 invasive cases and identification of a possible noninvasive intermediate lesion. Am. J. Surg. Pathol. 2016; 40; 1165–1176.
25. Malpica A, Deavers MT, Lu K et al. Grading ovarian serous carcinoma using a two-tier system. Am. J. Surg. Pathol. 2004; 28; 496–504.
26. Malpica A, Deavers MT, Tornos C et al. Interobserver and intraobserver variability of a two-tier system for grading ovarian serous carcinoma. Am. J. Surg. Pathol. 2007; 31; 1168–1174.
27. Soslow RA, Han G, Park KJ et al. Morphologic patterns associated with BRCA1 and BRCA2 genotype in ovarian carcinoma. Mod. Pathol. 2012; 25; 625–636.
28. Milea A, George SH, Matevski D et al. Retinoblastoma pathway deregulatory mechanisms determine clinical outcome in high-grade serous ovarian carcinoma. Mod. Pathol. 2014; 27; 991–1001.
29. Beirne JPMD, James JA, Salto-Tellez M, Maxwell P, McCluggage WG. p16 as a prognostic indicator in ovarian/tubal high grade serous carcinoma. Histopathology 2016; 64; 615–618.
30. Kobel M, Kalloger SE, Baker PM et al. Diagnosis of ovarian carcinoma cell type is highly reproducible: a transcanadian study. Am. J. Surg. Pathol. 2010; 34; 984–993.
31. Kobel M, Bak J, Bertelsen BI et al. Ovarian carcinoma histotype determination is highly reproducible, and is improved through the use of immunohistochemistry. Histopathology 2014; 64; 1004–1013.
32. Kommoss S, Gilks CB, du Bois A, Kommoss F. Ovarian carcinoma diagnosis: the clinical impact of 15 years of change. Br. J. Cancer 2016; 115; 993–999.
33. Al-Hussaini M, Stockman A, Foster H, McCluggage WG. WT-1 assists in distinguishing ovarian from uterine serous carcinoma and in distinguishing between serous and endometrioid ovarian carcinoma. Histopathology 2004; 44; 109–115.
34. McCluggage WG. WT1 is of value in ascertaining the site of origin of serous carcinomas within the female genital tract. Int. J. Gynecol. Pathol. 2004; 23; 97–99.
35. Shimizu M, Toki T, Takagi Y, Konishi I, Fujii S. Immunohistochemical detection of the Wilms’ tumor gene (WT1) in epithelial ovarian tumors. Int. J. Gynecol. Pathol. 2000; 19; 158–163.
36. Goldstein NS, Uzieblo A. WT1 immunoreactivity in uterine papillary serous carcinomas is different from ovarian serous carcinomas. Am. J. Clin. Pathol. 2002; 117; 541–545.
37. Kobel M, Kalloger SE, Carrick J et al. A limited panel of immunomarkers can reliably distinguish between clear cell and high-grade serous carcinoma of the ovary. Am. J. Surg. Pathol. 2009; 33; 14–21.
38. Hoang LN, Zachara S, Soma A et al. Diagnosis of ovarian carcinoma histotype based on limited sampling: a prospective study comparing cytology, frozen section, and core biopsies to full pathologic examination. Int. J. Gynecol. Pathol. 2015; 34; 517–527.
39. Kobel M, Piskorz AM, Lee S et al. Optimized p53 immunohistochemistry is an accurate predictor of TP53 mutation in ovarian carcinoma. J. Pathol. Clin. Res. 2016; 2; 247–258.
40. McCluggage WG, Soslow RA, Gilks CB. Patterns of p53 immunoreactivity in endometrial carcinomas: ‘all or nothing’ staining is of importance. Histopathology 2011; 59; 786–788.
41. Dehari R, Kurman RJ, Logani S, Shih IM. The development of high-grade serous carcinoma from atypical proliferative (borderline) serous tumors and low-grade micropapillary serous carcinoma: a morphologic and molecular genetic analysis. Am. J. Surg. Pathol. 2007; 31; 1007–1012.
42. Boyd C, McCluggage WG. Low-grade ovarian serous neoplasms (low-grade serous carcinoma and serous borderline tumor) associated with high-grade serous carcinoma or undifferentiated carcinoma: report of a series of cases of an unusual phenomenon. Am. J. Surg. Pathol. 2012; 36; 368–375.
43. Garg K, Park KJ, Soslow RA. Low-grade serous neoplasms of the ovary with transformation to high-grade carcinomas: a report of 3 cases. Int. J. Gynecol. Pathol. 2012; 31; 423–428.
44. Stewart CJ, Brennan BA, Chan T, Netreba J. WT1 expression in endometrioid ovarian carcinoma with and without associated endometriosis. Pathology 2008; 40; 592–599.
45. Yamamoto S, Tsuda H, Aida S, Shimazaki H, Tamai S, Matsubara O. Immunohistochemical detection of hepatocyte nuclear factor 1beta in ovarian and endometrial clear-cell adenocarcinomas and nonneoplastic endometrium. Hum. Pathol. 2007; 38; 1074–1080.
46. DeLair D, Oliva E, Kobel M, Macias A, Gilks CB, Soslow RA. Morphologic spectrum of immunohistochemically characterized clear cell carcinoma of the ovary: a study of 155 cases. Am. J. Surg. Pathol. 2011; 35; 36–44.
47. DeLair D, Han G, Irving JA et al. HNF-1beta in ovarian carcinomas with serous and clear cell change. Int. J. Gynecol. Pathol. 2013; 32; 541–546.
48. Iwamoto M, Nakatani Y, Fugo K, Kishimoto T, Kiyokawa T. Napsin A is frequently expressed in clear cell carcinoma of the ovary and endometrium. Hum. Pathol. 2015; 46; 957–962.
49. Fadare O, Zhao C, Khabele D et al. Comparative analysis of Napsin A, alpha-methylacyl-coenzyme A racemase (AMACR, P504S), and hepatocyte nuclear factor 1 beta as diagnostic markers of ovarian clear cell carcinoma: an immunohistochemical study of 279 ovarian tumours. Pathology 2015; 47; 105–111.
50. Fadare O, Gwin K, Desouki MM et al. The clinicopathologic significance of p53 and BAF-250a (ARID1A) expression in clear cell carcinoma of the endometrium. Mod. Pathol. 2013; 26; 1101–1110.
51. Eichhorn JH, Young RH. Transitional cell carcinoma of the ovary: a morphologic study of 100 cases with emphasis on differential diagnosis. Am. J. Surg. Pathol. 2004; 28; 453–463.
52. Ali RH, Seidman JD, Luk M, Kalloger S, Gilks CB. Transitional cell carcinoma of the ovary is related to high-grade serous carcinoma and is distinct from malignant brenner tumor. Int. J. Gynecol. Pathol. 2012; 31; 499–506.
53. Karnezis AN, Aysal A, Zaloudek CJ, Rabban JT. Transitional cell-like morphology in ovarian endometrioid carcinoma: morphologic, immunohistochemical, and behavioral features distinguishing it from high-grade serous carcinoma. Am. J. Surg. Pathol. 2013; 37; 24–37.
54. Logani S, Oliva E, Amin MB, Folpe AL, Cohen C, Young RH. Immunoprofile of ovarian tumors with putative transitional cell (urothelial) differentiation using novel urothelial markers: histogenetic and diagnostic implications. Am. J. Surg. Pathol. 2003; 27; 1434–1441.
55. Silva EG, Deavers MT, Malpica A. Undifferentiated carcinoma of the endometrium: a review. Pathology 2007; 39; 134–138.
56. Coatham M, Li X, Karnezis AN et al. Concurrent ARID1A and ARID1B inactivation in endometrial and ovarian dedifferentiated carcinomas. Mod. Pathol. 2016; 29; 1586–1593.
57. Hoang LN, Lee YS, Karnezis AN et al. Immunophenotypic features of dedifferentiated endometrial carcinoma – insights from BRG1/INI1-deficient tumors. Histopathology 2016; 69; 560–569.
58. Medeiros F, Muto MG, Lee Y et al. The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome. Am. J. Surg. Pathol. 2006; 30; 230–236.
59. Kindelberger DW, Lee Y, Miron A et al. Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship. Am. J. Surg. Pathol. 2007; 31; 161–169.
60. Przybycin CG, Kurman RJ, Ronnett BM, Shih IM, Vang R. Are all pelvic (nonuterine) serous carcinomas of tubal origin? Am. J. Surg. Pathol. 2010; 34; 1407–1416.
61. Herrington CS, McCluggage WG. The emerging role of the distal fallopian tube and p53 in pelvic serous carcinogenesis. J. Pathol. 2010; 220; 5–6.
62. Lee Y, Miron A, Drapkin R et al. A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J. Pathol. 2007; 211; 26–35.
63. Lee Y, Medeiros F, Kindelberger D, Callahan MJ, Muto MG, Crum CP. Advances in the recognition of tubal intraepithelial carcinoma: applications to cancer screening and the pathogenesis of ovarian cancer. Adv. Anat. Pathol. 2006; 13; 1–7.
64. McCluggage WG, Hirschowitz L, Gilks CB, Wilkinson N, Singh N. The fallopian tube origin and primary site assignment in extrauterine high-grade serous carcinoma: findings of a survey of pathologists and clinicians. Int. J. Gynecol. Pathol. 2017; 36; 230–239.
65. Singh N, Gilks CB, Wilkinson N, McCluggage WG. The secondary Mullerian system, field effect, BRCA, and tubal fimbria: our evolving understanding of the origin of tubo-ovarian high-grade serous carcinoma and why assignment of primary site matters. Pathology 2015; 47; 423–431.
66. Piek JM, van Diest PJ, Zweemer RP et al. Dysplastic changes in prophylactically removed fallopian tubes of women predisposed to developing ovarian cancer. J. Pathol. 2001; 195; 451–456.
67. Piek JM, Verheijen RH, Kenemans P, Massuger LF, Bulten H, van Diest PJ. BRCA1/2-related ovarian cancers are of tubal origin: a hypothesis. Gynecol. Oncol. 2003; 90; 491.
68. Singh N, Gilks CB, Wilkinson N, McCluggage WG. Assessment of a new system for primary site assignment in high-grade serous carcinoma of the fallopian tube, ovary, and peritoneum. Histopathology 2015; 67; 331–337.
69. Gilks CB, Irving J, Kobel M et al. Incidental nonuterine high-grade serous carcinomas arise in the fallopian tube in most cases: further evidence for the tubal origin of high-grade serous carcinomas. Am. J. Surg. Pathol. 2015; 39; 357–364.
70. Morrison JC, Blanco LZ Jr, Vang R, Ronnett BM. Incidental serous tubal intraepithelial carcinoma and early invasive serous carcinoma in the nonprophylactic setting: analysis of a case series. Am. J. Surg. Pathol. 2015; 39; 442–453.
71. Semmel DR, Folkins AK, Hirsch MS, Nucci MR, Crum CP. Intercepting early pelvic serous carcinoma by routine pathological examination of the fimbria. Mod. Pathol. 2009; 22; 985–988.
72. Rabban JT, Garg K, Crawford B, Chen LM, Zaloudek CJ. Early detection of high-grade tubal serous carcinoma in women at low risk for hereditary breast and ovarian cancer syndrome by systematic examination of fallopian tubes incidentally removed during benign surgery. Am. J. Surg. Pathol. 2014; 38; 729–742.
73. Ahmed AA, Etemadmoghadam D, Temple J, et al. Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J. Pathol. 2010; 221; 49–56.
74. Cancer Genome Atlas Research N. Integrated genomic analyses of ovarian carcinoma. Nature 2011; 474; 609–615.
75. Bashashati A, Ha G, Tone A et al. Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling. J. Pathol. 2013; 231; 21–34.
76. Kuhn E, Kurman RJ, Vang R et al. TP53 mutations in serous tubal intraepithelial carcinoma and concurrent pelvic high-grade serous carcinoma – evidence supporting the clonal relationship of the two lesions. J. Pathol. 2012; 226; 421–426.
77. McDaniel AS, Stall JN, Hovelson DH et al. Next-generation sequencing of tubal intraepithelial carcinomas. JAMA Oncol. 2015; 1; 1128–1132.
78. Rabban JT, Vohra P, Zaloudek CJ. Nongynecologic metastases to fallopian tube mucosa: a potential mimic of tubal high-grade serous carcinoma and benign tubal mucinous metaplasia or nonmucinous hyperplasia. Am. J. Surg. Pathol. 2015; 39; 35–51.
79. Jarboe EA, Miron A, Carlson JW et al. Coexisting intraepithelial serous carcinomas of the endometrium and fallopian tube: frequency and potential significance. Int. J. Gynecol. Pathol. 2009; 28; 308–315.
80. Kommoss F, Faruqi A, Gilks CB et al. Uterine serous carcinomas frequently metastasize to the fallopian tube and can mimic serous tubal intraepithelial carcinoma. Am. J. Surg. Pathol. 2016; 41; 161–170.
81. Kuhn E, Meeker A, Wang TL, Sehdev AS, Kurman RJ, Shih IM. Shortened telomeres in serous tubal intraepithelial carcinoma: an early event in ovarian high-grade serous carcinogenesis. Am. J. Surg. Pathol. 2010; 34; 829–836.
82. Kuhn E, Wang TL, Doberstein K et al. CCNE1 amplification and centrosome number abnormality in serous tubal intraepithelial carcinoma: further evidence supporting its role as a precursor of ovarian high-grade serous carcinoma. Mod. Pathol. 2016; 29; 1254–1261.
83. Kurman RJ. Origin and molecular pathogenesis of ovarian high-grade serous carcinoma. Ann. Oncol. 2013; 24(Suppl. 10); x16–x21.
84. Song Z. Ovarian enzymatically active stromal cells can be a promoter of ovarian surface epithelial tumor. Med. Hypotheses 2011; 77; 356–358.
85. Carlson JW, Jarboe EA, Kindelberger D, Nucci MR, Hirsch MS, Crum CP. Serous tubal intraepithelial carcinoma: diagnostic reproducibility and its implications. Int. J. Gynecol. Pathol. 2010; 29; 310–314.
86. Visvanathan K, Vang R, Shaw P et al. Diagnosis of serous tubal intraepithelial carcinoma based on morphologic and immunohistochemical features: a reproducibility study. Am. J. Surg. Pathol. 2011; 35; 1766–1775.
87. Vang R, Visvanathan K, Gross A et al. Validation of an algorithm for the diagnosis of serous tubal intraepithelial carcinoma. Int. J. Gynecol. Pathol. 2012; 31; 243–253.
88. Mehra K, Mehrad M, Ning G et al. STICS, SCOUTs and p53 signatures; a new language for pelvic serous carcinogenesis. Front. Biosci. (Elite edn) 2011; 3; 625–634.
89. Vang R, Shih IM, Kurman RJ. Fallopian tube precursors of ovarian low- and high-grade serous neoplasms. Histopathology 2013; 62; 44–58.
90. Mehrad M, Ning G, Chen EY, Mehra KK, Crum CP. A pathologist's road map to benign, precancerous, and malignant intraepithelial proliferations in the fallopian tube. Adv. Anat. Pathol. 2010; 17; 293–302.
91. Folkins AK, Jarboe EA, Saleemuddin A et al. A candidate precursor to pelvic serous cancer (p53 signature) and its prevalence in ovaries and fallopian tubes from women with BRCA mutations. Gynecol. Oncol. 2008; 109; 168–173.
92. Hirschowitz L, Ganesan R, McCluggage WG. WT1, p53 and hormone receptor expression in uterine serous carcinoma. Histopathology 2009; 55; 478–482.
93. Mahe E, Tang S, Deb P, Sur M, Lytwyn A, Daya D. Do deeper sections increase the frequency of detection of serous tubal intraepithelial carcinoma (STIC) in the ‘sectioning and extensively examining the FIMbriated end’ (SEE-FIM) protocol? Int. J. Gynecol. Pathol. 2013; 32; 353–357.
94. Kulkarni S, Singh N, Faruqi AZ. Tubal handling significantly affects site assignment in non-uterine high-grade serous carcinoma. Histopathology 2015; 67; 485–487.
95. Meserve EM, Mirkovic J, Conner J, Yang E, Howitt BE, Crum CE. Detection of serous tubal intraepithelial carcinoma (STIC) in incidentally removed fallopian tubes from low-risk women. Mod. Pathol. 2016; 29(Suppl. 2); 297A.
96. Wethington SL, Park KJ, Soslow RA et al. Clinical outcome of isolated serous tubal intraepithelial carcinomas (STIC). Int. J. Gynecol. Cancer 2013; 23; 1603–1611.
97. Chay WY, McCluggage WG, Lee CH et al. Outcomes of incidental fallopian tube high-grade serous carcinoma and serous tubal intraepithelial carcinoma in women at low risk of hereditary breast and ovarian cancer. Int. J. Gynecol. Cancer 2016; 26; 431–436.
98. Prat J; Foundation for the Children's Oncology Group (Oncology FCoG). Staging classification for cancer of the ovary, fallopian tube, and peritoneum. Int. J. Gynaecol. Obstet. 2014; 124; 1–5.
99. Bloss JD, Liao SY, Buller RE et al. Extraovarian peritoneal serous papillary carcinoma: a case-control retrospective comparison to papillary adenocarcinoma of the ovary. Gynecol. Oncol. 1993; 50; 347–351.
100. McCluggage WG, Judge MJ, Clarke BA et al. Data set for reporting of ovary, fallopian tube and primary peritoneal carcinoma: recommendations from the International Collaboration on Cancer Reporting (ICCR). Mod. Pathol. 2015; 28; 1101–1122.
101. Singh N, Gilks CB, Wilkinson N, McCluggage WG. Assignment of primary site in high-grade serous tubal, ovarian and peritoneal carcinoma: a proposal. Histopathology 2014; 65; 149–154.
102. Singh N, Gilks CB, Hirshowitz L, Wilkinson N, McCluggage WG. Adopting a uniform approach to site assignment in tubo-ovarian high-grade serous carcinoma: the time has come. Int. J. Gynecol. Pathol. 2016; 35; 230–237.
103. Singh N, Gilks CB, Hirschowitz L et al. Primary site assignment in tubo-ovarian high-grade serous carcinoma: consensus statement on unifying practice worldwide. Gynecol. Oncol. 2016; 141; 195–198.
104. Powell CB. Risk reducing salpingo-oophorectomy for BRCA mutation carriers: twenty years later. Gynecol. Oncol. 2014; 132; 261–263.
105. Alsop K, Fereday S, Meldrum C et al. BRCA mutation frequency and patterns of treatment response in BRCA mutation-positive women with ovarian cancer: a report from the Australian Ovarian Cancer Study Group. J. Clin. Oncol. 2012; 30; 2654–2663.
106. Schrader KA, Hurlburt J, Kalloger SE et al. Germline BRCA1 and BRCA2 mutations in ovarian cancer: utility of a histology-based referral strategy. Obstet. Gynecol. 2012; 120; 235–240.
107. Nakayama N, Nakayama K, Shamima Y et al. Gene amplification CCNE1 is related to poor survival and potential therapeutic target in ovarian cancer. Cancer 2010; 116; 2621–2634.
108. Etemadmoghadam D, Weir BA, Au-Yeung G, et al. Synthetic lethality between CCNE1 amplification and loss of BRCA1. Proc. Natl Acad. Sci. USA 2013; 110; 19489–19494.
109. Patch AM, Christie EL, Etemadmoghadam D, et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature 2015; 521; 489–494.
110. Au-Yeung G, Lang F, Azar WJ et al. Selective targeting of cyclin E1 amplified high grade serous ovarian cancer by cyclin-dependent kinase 2 and AKT inhibition. Clin. Cancer Res. 2017;. https://doi.org/10.1158/1078-0432.CCR-16-0620.
111. Wang YK, Bashashati A, Anglesio MS et al. Genomic conseqences of aberrant DNA repair mechanisms stratify ovarian cancer histotypes. Nat. Genet. 2017; 49; 856–865.
112. Bohm S, Faruqi A, Said I et al. Chemotherapy response score: development and validation of a system to quantify histopathologic response to neoadjuvant chemotherapy in tubo-ovarian high-grade serous carcinoma. J. Clin. Oncol. 2015; 33; 2457–2463.
113. Ditzel HM, Stickland K, Meserve E et al. Assessment of the chemotherapy response score (CRS) system in high grade serous carcinoma (HGSC). Mod. Pathol. 2016; 29(Suppl. 2); 281A.
114. Said I, Bohm S, Beasley J et al. The Chemotherapy Response Score (CRS): interobserver reproducibility in a simple and prognostically relevant system for reporting the histologic response to neoadjuvant chemotherapy in tuboovarian high-grade serous carcinoma. Int. J. Gynecol. Pathol. 2017; 36; 172–179.
115. Gilks C, Movahedi-Lankarani S, Baker PM, Otis CN, Soslow RA, Oliva E; for the Members of the Cancer Committee, College of American Pathologists. Protocol for the examination of specimens from patients with primary tumors of the ovary or fallopian tube. Northfield, IL: College of American Pathologists, 2016.