The dualistic model of ovarian carcinogenesis revisited, revised, and expanded

American Journal of Pathology

Volumn 186, Issue 4, 2016, Pages 733-747

  Kurman, Robert J ^a   Shih, Ie Ming ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRENNER TUMOR; CANCER SCREENING; CANCER STAGING; CANCER SURVIVAL; CARCINOSARCOMA; CHROMATIN ASSEMBLY AND DISASSEMBLY; CLEAR CELL CARCINOMA; COLLOID CARCINOMA; DNA DAMAGE; DNA REPAIR; DRUG RESISTANCE; ENDOMETRIOID CARCINOMA; ENDOMETRIOSIS; FEMALE; HISTOPATHOLOGY; HUMAN; MALIGNANT TRANSFORMATION; MISMATCH REPAIR; MIXED MULLERIAN TUMOR; MOLECULAR PATHOLOGY; NEXT GENERATION SEQUENCING; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; SEROMUCINOUS CARCINOMA; UNDIFFERENTIATED CARCINOMA; WNT SIGNALING PATHWAY; WORLD HEALTH ORGANIZATION; ANIMAL; CARCINOGENESIS; CELL TRANSFORMATION; FALLOPIAN TUBE; GENETICS; OVARY; OVARY TUMOR; PATHOLOGY;

ADENOCARCINOMA, MUCINOUS; ANIMALS; CARCINOGENESIS; CELL TRANSFORMATION, NEOPLASTIC; FALLOPIAN TUBES; FEMALE; HUMANS; OVARIAN NEOPLASMS; OVARY;

EID: 84962496502     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.11.011     Document Type: Review

References (104)

1. IeM. Shih, and R.J. Kurman Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis Am J Pathol 164 2004 1511 1518
2. K.M. Schmeler, X. Tao, M. Frumovitz, M.T. Deavers, C.C. Sun, A.K. Sood, J. Brown, D.M. Gershenson, and P.T. Ramirez Prevalence of lymph node metastasis in primary mucinous carcinoma of the ovary Obstet Gynecol 116 2010 269 273
3. R.J. Kurman, M.L. Carcangiu, S. Herrington, and R.H. Young WHO classification of tumours of female reproductive organs ed 4 2014 IARC Lyon, France
4. R.J. Kurman, and IeM. Shih Seromucinous tumors of the ovary. What's in a name? Int J Gynecol Pathol 35 2016 78 81
5. R. Mackenzie, A. Talhouk, S. Eshragh, S. Lau, D. Cheung, C. Chow, N. Le, L.S. Cook, N. Wilkinson, J. McDermott, N. Singh, F. Kommoss, J. Pfisterer, D.G. Huntsman, M. Kobel, S. Kommoss, C.B. Gilks, and M.S. Anglesio Morphologic and molecular characteristics of mixed epithelial ovarian cancers Am J Surg Pathol 39 2015 1548 1557
6. J.D. Seidman, K. Cho, B.M. Ronnett, and R.J. Kurman Surface epithelial tumors of the ovary R.J. Kurman, L.H. Ellenson, B.M. Ronnett, Blaustein's Pathology of the Female Genital Tract ed 6 2011 Springer Verlag New York 679 784
7. L. Ardighieri, F. Zeppernick, C.G. Hannibal, R. Vang, L. Cope, J. Junge, S.K. Kjaer, and R.J. Kurman Shih IeM: Mutational analysis of BRAF and KRAS in ovarian serous borderline (atypical proliferative) tumours and associated peritoneal implants J Pathol 232 2014 16 22
8. T.A. Longacre, J.K. McKenney, H.D. Tazelaar, R.L. Kempson, and M.R. Hendrickson Ovarian serous tumors of low malignant potential (borderline tumors): outcome-based study of 276 patients with long-term (> or =5-year) follow-up Am J Surg Pathol 29 2005 707 723
9. H.S. Shvartsman, C.C. Sun, D.C. Bodurka, V. Mahajan, M. Crispens, K.H. Lu, M.T. Deavers, A. Malpica, E.G. Silva, and D.M. Gershenson Comparison of the clinical behavior of newly diagnosed stages II-IV low-grade serous carcinoma of the ovary with that of serous ovarian tumors of low malignant potential that recur as low-grade serous carcinoma Gynecol Oncol 105 2007 625 662
10. R. Dehari, R.J. Kurman, S. Logani, and IeM. Shih 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 31 2007 1007 1012
11. Y.T. Tsang, M.T. Deavers, C.C. Sun, S.Y. Kwan, E. Kuo, A. Malpica, S.C. Mok, D.M. Gershenson, and K.K. Wong KRAS (but not BRAF) mutations in ovarian serous borderline tumour are associated with recurrent low-grade serous carcinoma J Pathol 231 2013 449 456
12. R.N. Grisham, G. Iyer, K. Garg, D. DeLair, D.M. Hyman, Q. Zhou, A. Iasonos, M.F. Berger, F. Dao, D.R. Spriggs, D.A. Levine, C. Aghajanian, and D.B. Solit BRAF mutation is associated with early stage disease and improved outcome in patients with low-grade serous ovarian cancer Cancer 119 2013 548 554
13. K.K. Wong, Y.T. Tsang, M.T. Deavers, S.C. Mok, Z. Zu, C. Sun, A. Malpica, J.K. Wolf, K.H. Lu, and D.M. Gershenson BRAF mutation is rare in advanced-stage low-grade ovarian serous carcinomas Am J Pathol 177 2010 1611 1617
14. F. Zeppernick, L. Ardighieri, C.G. Hannibal, R. Vang, J. Junge, S.K. Kjaer, R. Zhang, R.J. Kurman, and IeM. Shih BRAF mutation is associated with a specific cell type with features suggestive of senescence in ovarian serous borderline (atypical proliferative) tumors Am J Surg Pathol 38 2014 1603 1611
15. K.P. Maniar, Y. Wang, K. Visvanathan, IeM. Shih, and R.J. Kurman Evaluation of microinvasion and lymph node involvement in ovarian serous borderline/atypical proliferative serous tumors: a morphologic and immunohistochemical analysis of 37 cases Am J Surg Pathol 38 2014 743 755
16. R.J. Kurman, R. Vang, J. Junge, C.G. Hannibal, S.K. Kjaer, and IeM. Shih Papillary tubal hyperplasia: the putative precursor of ovarian atypical proliferative (borderline) serous tumors, noninvasive implants, and endosalpingiosis Am J Surg Pathol 35 2011 1605 1614
17. R. Wu, N. Hendrix-Lucas, R. Kuick, Y. Zhai, D.R. Schwartz, A. Akyol, S. Hanash, D.E. Misek, H. Katabuchi, B.O. Williams, E.R. Fearon, and K.R. Cho Mouse model of human ovarian endometrioid adenocarcinoma based on somatic defects in the Wnt/beta-catenin and PI3K/Pten signaling pathways Cancer Cell 11 2007 321 333
18. M. Saegusa, M. Hashimura, T. Yoshida, and I. Okayasu beta- Catenin mutations and aberrant nuclear expression during endometrial tumorigenesis Br J Cancer 84 2001 209 217
19. L. Catasus, E. Bussaglia, I. Rodrguez, A. Gallardo, C. Pons, J.A. Irving, and J. Prat Molecular genetic alterations in endometrioid carcinomas of the ovary: similar frequency of beta-catenin abnormalities but lower rate of microsatellite instability and PTEN alterations than in uterine endometrioid carcinomas Hum Pathol 35 2004 1360 1368
20. K. Nakayama, N. Nakayama, R.J. Kurman, L. Cope, G. Pohl, Y. Samuels, V.E. Velculescu, T.L. Wang, and IeM. Shih Sequence mutations and amplification of PIK3CA and AKT2 genes in purified ovarian serous neoplasms Cancer Biol Ther 5 2006 779 785
21. S. Jones, T.L. Wang, IeM. Shih, T.L. Mao, K. Nakayama, R. Roden, R. Glas, D. Slamon, L.A. Diaz Jr., B. Vogelstein, K.W. Kinzler, V.E. Velculescu, and N. Papadopoulos Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma Science 330 2010 228 231
22. D. Mayr, A. Hirschmann, U. Lohrs, and J. Diebold KRAS and BRAF mutations in ovarian tumors: a comprehensive study of invasive carcinomas, borderline tumors and extraovarian implants Gynecol Oncol 103 2006 883 887
23. J. Willner, K. Wurz, K.H. Allison, V. Galic, R.L. Garcia, B.A. Goff, and E.M. Swisher Alternate molecular genetic pathways in ovarian carcinomas of common histological types Hum Pathol 38 2007 607 613
24. B. Guan, Y.S. Rahmanto, R.C. Wu, Y. Wang, Z. Wang, T.L. Wang, and IeM. Shih Roles of deletion of Arid1a, a tumor suppressor, in mouse ovarian tumorigenesis J Natl Cancer Inst 106 2014
25. R.L. Chandler, J.S. Damrauer, J.R. Raab, J.C. Schisler, M.D. Wilkerson, J.P. Didion, J. Starmer, D. Serber, D. Yee, J. Xiong, D.B. Darr, F. Pardo-Manuel de Villena, W.Y. Kim, and T. Magnuson Coexistent ARID1A-PIK3CA mutations promote ovarian clear-cell tumorigenesis through pro-tumorigenic inflammatory cytokine signalling Nat Commun 6 2015 6118
26. K. Yamaguchi, Z. Huang, N. Matsumura, M. Mandai, T. Okamoto, T. Baba, I. Konishi, A. Berchuck, and S.K. Murphy Epigenetic determinants of ovarian clear cell carcinoma biology Int J Cancer 135 2014 585 597
27. R.A. Soslow, G. Han, K.J. Park, K. Garg, N. Olvera, D.R. Spriggs, N.D. Kauff, and D.A. Levine Morphologic patterns associated with BRCA1 and BRCA2 genotype in ovarian carcinoma Mod Pathol 25 2012 625 636
28. C.H. Wu, T.L. Mao, R. Vang, A. Ayhan, T.L. Wang, R.J. Kurman, and IeM. Shih Endocervical-type mucinous borderline tumors are related to endometrioid tumors based on mutation and loss of expression of ARID1A Int J Gynecol Pathol 31 2012 297 303
29. R. Mackenzie, S. Kommoss, B.J. Winterhoff, B.R. Kipp, J.J. Garcia, J. Voss, K. Halling, A. Karnezis, J. Senz, W. Yang, E.S. Prigge, M. Reuschenbach, M.V. Doeberitz, B.C. Gilks, D.G. Huntsman, J. Bakkum-Gamez, J.N. McAlpine, and M.S. Anglesio Targeted deep sequencing of mucinous ovarian tumors reveals multiple overlapping RAS-pathway activating mutations in borderline and cancerous neoplasms BMC Cancer 15 2015 415
30. G.L. Ryland, S.M. Hunter, M.A. Doyle, S.M. Rowley, M. Christie, P.E. Allan, D.D. Bowtell Australian Ovarian Cancer Study Group K.L. Gorringe, and I.G. Campbell RNF43 is a tumour suppressor gene mutated in mucinous tumours of the ovary J Pathol 229 2013 469 476
31. N. Auersperg The origin of ovarian carcinomas: a unifying hypothesis Int J Gynecol Pathol 30 2011 12 21
32. E. Adler, P. Mhawech-Fauceglia, S.A. Gayther, and K. Lawrenson PAX8 expression in ovarian surface epithelial cells Hum Pathol 46 2015 948 956
33. E. Kuhn, A. Ayhan, A. Bahadirli-Talbott, C. Zhao, and IeM. Shih Molecular characterization of undifferentiated carcinoma associated with endometrioid carcinoma Am J Surg Pathol 38 2014 660 665
34. B.E. Howitt, S. Hanamornroongruang, D.I. Lin, J.E. Conner, S. Schulte, N. Horowitz, C.P. Crum, and E.E. Meserve Evidence for a dualistic model of high-grade serous carcinoma: BRCA mutation status, histology, and tubal intraepithelial carcinoma Am J Surg Pathol 39 2015 287 293
35. M. Kobel, S.E. Kalloger, S. Lee, M.A. Duggan, L.E. Kelemen, L. Prentice, K.R. Kalli, B.L. Fridley, D.W. Visscher, G.L. Keeney, R.A. Vierkant, J.M. Cunningham, C. Chow, R.B. Ness, K. Moysich, R. Edwards, F. Modugno, C. Bunker, E.L. Wozniak, E. Benjamin, S.A. Gayther, A. Gentry-Maharaj, U. Menon, C.B. Gilks, D.G. Huntsman, S.J. Ramus, E.L. Goode Ovarian Tumor Tissue Analysis Consortium Biomarker-based ovarian carcinoma typing: a histologic investigation in the ovarian tumor tissue analysis consortium Cancer Epidemiol Biomarkers Prev 22 2013 1677 1686
36. E.G. Silva, S.S. Robey-Cafferty, T.L. Smith, and D.M. Gershenson Ovarian carcinomas with transitional cell carcinoma pattern Am J Clin Pathol 93 1990 457 465
37. Cancer Genome Atlas Research Network Integrated genomic analyses of ovarian carcinoma Nature 474 2011 609 615
38. A.M. Patch, E.L. Christie, D. Etemadmoghadam, D.W. Garsed, J. George, S. Fereday, and et al. Whole-genome characterization of chemoresistant ovarian cancer Nature 521 2015 489 494
39. R. Vang, D.A. Levine, R.A. Soslow, C. Zaloudek, IeM. Shih, and R.J. Kurman Molecular alterations of TP53 are a defining feature of ovarian high-grade serous carcinoma: a rereview of cases lacking tp53 mutations in the Cancer Genome Atlas Ovarian Study Int J Gynecol Pathol 35 2016 48 55
40. R.W. Tothill, A.V. Tinker, J. George, R. Brown, S.B. Fox, S. Lade, D.S. Johnson, M.K. Trivett, D. Etemadmoghadam, B. Locandro, N. Traficante, S. Fereday, J.A. Hung, Y.E. Chiew, I. Haviv Australian Ovarian Cancer Study Group D. Gertig, A. DeFazio, and D.D. Bowtell Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome Clin Cancer Res 14 2008 5198 5208
41. A. Helland, M.S. Anglesio, J. George, P.A. Cowin, C.N. Johnstone, C.M. House, K.E. Sheppard, D. Etemadmoghadam, N. Melnyk, A.K. Rustgi, W.A. Phillips, H. Johnsen, R. Holm, G.B. Kristensen, M.J. Birrer Australian Ovarian Cancer Study Group R.B. Pearson, A.L. Borresen-Dale, D.G. Huntsman, A. deFazio, C.J. Creighton, G.K. Smyth, and D.D. Bowtell Deregulation of MYCN, LIN28B and LET7 in a molecular subtype of aggressive high-grade serous ovarian cancers PLoS One 6 2011 e18064
42. G.E. Konecny, C. Wang, H. Hamidi, B. Winterhoff, K.R. Kalli, J. Dering, C. Ginther, H.W. Chen, S. Dowdy, W. Cliby, B. Gostout, K.C. Podratz, G. Keeney, H.J. Wang, L.C. Hartmann, D.J. Slamon, and E.L. Goode Prognostic and therapeutic relevance of molecular subtypes in high-grade serous ovarian cancer J Natl Cancer Inst 106 2014
43. J. George, K. Alsop, D. Etemadmoghadam, H. Hondow, T. Mikeska, A. Dobrovic, A. deFazio Australian Ovarian Cancer Study Group G.K. Smyth, D.A. Levine, G. Mitchell, and D.D. Bowtell Nonequivalent gene expression and copy number alterations in high-grade serous ovarian cancers with BRCA1 and BRCA2 mutations Clin Cancer Res 19 2013 3474 3484
44. Z. Jin, S. Ogata, G. Tamura, Y. Katayama, M. Fukase, M. Yajima, and T. Motoyama Carcinosarcomas (malignant mullerian mixed tumors) of the uterus and ovary: a genetic study with special reference to histogenesis Int J Gynecol Pathol 22 2003 368 373
45. E.C. Abeln, V.T. Smit, J.W. Wessels, W.J. de Leeuw, C.J. Cornelisse, and G.J. Fleuren Molecular genetic evidence for the conversion hypothesis of the origin of malignant mixed mullerian tumours J Pathol 183 1997 424 431
46. G. Singer, R. Oldt 3rd, Y. Cohen, B.G. Wang, D. Sidransky, R.J. Kurman, and IeM. Shih Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma J Natl Cancer Inst 95 2003 484 486
47. K.T. Kuo, B. Guan, Y. Feng, T.L. Mao, X. Chen, N. Jinawath, Y. Wang, R.J. Kurman, I.M. Shih, and T.L. Wang Analysis of DNA copy number alterations in ovarian serous tumors identifies new molecular genetic changes in low-grade and high-grade carcinomas Cancer Res 69 2009 4036 4042
48. G. Pohl, C.L. Ho, R.J. Kurman, R. Bristow, T.L. Wang, and IeM. Shih Inactivation of the mitogen-activated protein kinase pathway as a potential target-based therapy in ovarian serous tumors with KRAS or BRAF mutations Cancer Res 65 2005 1994 2000
49. S. Jones, T.L. Wang, R.J. Kurman, K. Nakayama, V.E. Velculescu, B. Vogelstein, K.W. Kinzler, N. Papadopoulos, and IeM. Shih Low-grade serous carcinomas of the ovary contain very few point mutations J Pathol 226 2012 413 420
50. C. Emmanuel, Y.E. Chiew, J. George, D. Etemadmoghadam, M.S. Anglesio, R. Sharma, P. Russell, C. Kennedy, S. Fereday, J. Hung, L. Galletta, R. Hogg, G.V. Wain, A. Brand, R. Balleine, L. MacConaill, E. Palescandolo, S.M. Hunter, I. Campbell, A. Dobrovic, S.Q. Wong, H. Do, C.L. Clarke, P.R. Harnett, D.D. Bowtell, A. deFazio Australian Ovarian Cancer Study (AOCS) Genomic classification of serous ovarian cancer with adjacent borderline differentiates RAS pathway and TP53-mutant tumors and identifies NRAS as an oncogenic driver Clin Cancer Res 20 2014 6618 6630
51. C.L. Ho, R.J. Kurman, R. Dehari, T.-L. Wang, and IeM. Shih Mutations of BRAF and KRAS precede the development of ovarian serous borderline tumors Cancer Res 64 2004 6915 6918
52. J.J. Sheu, B. Guan, F.J. Tsai, E.Y. Hsiao, C.M. Chen, R. Seruca, T.L. Wang, and IeM. Shih Mutant BRAF induces DNA strand breaks, activates DNA damage response pathway, and up-regulates glucose transporter-1 in nontransformed epithelial cells Am J Pathol 180 2012 1179 1188
53. L. Ardighieri, F. Zeppernick, C.G. Hannibal, R. Vang, L. Cope, J. Junge, S.K. Kjaer, R.J. Kurman, and IeM. Shih Mutational analysis of BRAF and KRAS in ovarian serous borderline (atypical proliferative) tumours and associated peritoneal implants J Pathol 232 2014 16 22
54. D. Dankort, E. Filenova, M. Collado, M. Serrano, K. Jones, and M. McMahon A new mouse model to explore the initiation, progression, and therapy of BRAFV600E-induced lung tumors Genes Dev 21 2007 379 384
55. M. Kato, T. Paranjape, R.U. Muller, S. Nallur, E. Gillespie, K. Keane, A. Esquela-Kerscher, J.B. Weidhaas, and F.J. Slack The mir-34 microRNA is required for the DNA damage response in vivo in C. elegans and in vitro in human breast cancer cells Oncogene 28 2009 2419 2424
56. P.W. Schlosshauer, L. Deligdisch, F. Penault-Llorca, D. Fatemi, R. Qiao, S. Yao, M. Pearl, Z. Yang, T. Sheng, and J. Dong Loss of p16INK4A expression in low-grade ovarian serous carcinomas Int J Gynecol Pathol 30 2011 22 29
57. K.C. Wiegand, S.P. Shah, O.M. Al-Agha, Y. Zhao, K. Tse, T. Zeng, and et al. ARID1A mutations in endometriosis-associated ovarian carcinomas N Engl J Med 363 2010 1532 1543
58. A. Ayhan, T.L. Mao, T. Seckin, C.H. Wu, B. Guan, H. Ogawa, M. Futagami, H. Mizukami, Y. Yokoyama, R.J. Kurman, and IeM. Shih Loss of ARID1A expression is an early molecular event in tumor progression from ovarian endometriotic cyst to clear cell and endometrioid carcinoma Int J Gynecol Cancer 22 2012 1310 1315
59. N. Sato, H. Tsunoda, M. Nishida, Y. Morishita, Y. Takimoto, T. Kubo, and M. Noguchi Loss of heterozygosity on 10q23.3 and mutation of the tumor suppressor gene PTEN in benign endometrial cyst of the ovary: possible sequence progression from benign endometrial cyst to endometrioid carcinoma and clear cell carcinoma of the ovary Cancer Res 60 2000 7052 7056
60. H.W. Shappell, M.A. Riopel, A.E. Smith Sehdev, B.M. Ronnett, and R.J. Kurman Diagnostic criteria and behavior of ovarian seromucinous (endocervical-type mucinous and mixed cell-type) tumors: atypical proliferative (borderline) tumors, intraepithelial, microinvasive, and invasive carcinomas Am J Surg Pathol 26 2002 1529 1541
61. R. Vang, A.M. Gown, T.S. Barry, D.T. Wheeler, and B.M. Ronnett Ovarian atypical proliferative (borderline) mucinous tumors: gastrointestinal and seromucinous (endocervical-like) types are immunophenotypically distinctive Int J Gynecol Pathol 25 2006 83 89
62. S.C. Mok, D.A. Bell, R.C. Knapp, P.M. Fishbaugh, W.R. Welch, M.G. Muto, R.S. Berkowitz, and S.W. Tsao Mutation of K-ras protooncogene in human ovarian epithelial tumors of borderline malignancy Cancer Res 53 1993 1489 1492
63. M. Cuatrecasas, A. Villanueva, X. Matias-Guiu, and J. Prat K-ras mutations in mucinous ovarian tumors: a clinicopathologic and molecular study of 95 cases Cancer 79 1997 1581 1586
64. J.D. Seidman, and F. Khedmati Exploring the histogenesis of ovarian mucinous and transitional cell (Brenner) neoplasms and their relationship with Walthard cell nests: a study of 120 tumors Arch Pathol Lab Med 132 2008 1753 1760
65. Y. Wang, R.C. Wu, L.E. Shwartz, L. Haley, M.T. Lin, I.M. Shih, and R.J. Kurman Clonality analysis of combined Brenner and mucinous tumours of the ovary reveals their monoclonal origin J Pathol 237 2015 146 151
66. J.M. Piek, P.J. van Diest, R.P. Zweemer, J.W. Jansen, R.J. Poort-Keesom, F.H. Menko, J.J. Gille, A.P. Jongsma, G. Pals, P. Kenemans, and R.H. Verheijen Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer J Pathol 195 2001 451 456
67. J.M. Piek, P.J. van Diest, R.P. Zweemer, P. Kenemans, and R.H. Verheijen Tubal ligation and risk of ovarian cancer Lancet 358 2001 844
68. J.M. Piek, R.H. Verheijen, P. Kenemans, L.F. Massuger, H. Bulten, and P.J. van Diest BRCA1/2-related ovarian cancers are of tubal origin: a hypothesis Gynecol Oncol 90 2003 491
69. A. Finch, M. Beiner, J. Lubinski, H.T. Lynch, P. Moller, B. Rosen, J. Murphy, P. Ghadirian, E. Friedman, W.D. Foulkes, C. Kim-Sing, T. Wagner, N. Tung, F. Couch, D. Stoppa-Lyonnet, P. Ainsworth, M. Daly, B. Pasini, R. Gershoni-Baruch, C. Eng, O.I. Olopade, J. McLennan, B. Karlan, J. Weitzel, P. Sun, S.A. Narod Hereditary Ovarian Cancer Clinical Study Group Salpingo-oophorectomy and the risk of ovarian, fallopian tube, and peritoneal cancers in women with a BRCA1 or BRCA2 Mutation JAMA 296 2006 185 192
70. F. Medeiros, M.G. Muto, Y. Lee, J.A. Elvin, M.J. Callahan, C. Feltmate, J.E. Garber, D.W. Cramer, and C.P. Crum The tubal fimbria is a preferred site for early adenocarcinoma in women with familial ovarian cancer syndrome Am J Surg Pathol 30 2006 230 236
71. D.W. Kindelberger, Y. Lee, A. Miron, M.S. Hirsch, C. Feltmate, F. Medeiros, M.J. Callahan, E.O. Garner, R.W. Gordon, C. Birch, R.S. Berkowitz, M.G. Muto, and C.P. Crum Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship Am J Surg Pathol 31 2007 161 169
72. C.G. Przybycin, R.J. Kurman, B.M. Ronnett, IeM. Shih, and R. Vang Are all pelvic (nonuterine) serous carcinomas of tubal origin? Am J Surg Pathol 34 2010 1407 1416
73. J.C. Morrison, L.Z. Blanco Jr., R. Vang, and B.M. Ronnett Incidental serous tubal intraepithelial carcinoma and early invasive serous carcinoma in the nonprophylactic setting: analysis of a case series Am J Surg Pathol 39 2015 442 453
74. C.B. Gilks, J. Irving, M. Kobel, C. Lee, N. Singh, N. Wilkinson, and W.G. McCluggage 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 39 2015 357 364
75. J.E. Hirst, G.B. Gard, K. McIllroy, D. Nevell, and M. Field High rates of occult fallopian tube cancer diagnosed at prophylactic bilateral salpingo-oophorectomy Int J Gynecol Cancer 19 2009 826 829
76. J.T. Rabban, K. Garg, B. Crawford, L.M. Chen, and C.J. Zaloudek 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 38 2014 729 742
77. S. Tang, K. Onuma, P. Deb, E. Wang, A. Lytwyn, M. Sur, and D. Daya Frequency of serous tubal intraepithelial carcinoma in various gynecologic malignancies: a study of 300 consecutive cases Int J Gynecol Pathol 31 2012 103 110
78. E. Kuhn, R.J. Kurman, R. Vang, A.S. Sehdev, G. Han, R. Soslow, T.L. Wang, and I.M. Shih TP53 mutations in serous tubal intraepithelial carcinoma (STIC) and concurrent pelvic high-grade serous carcinoma- evidence supporting their clonal relationship J Pathol 226 2012 421 426
79. E. Kuhn, A. Meeker, T.L. Wang, A.S. Sehdev, and R.J. Kurman Shih Ie-M: Shortened telomeres in serous tubal intraepithelial carcinoma: an early event in ovarian high-grade serous carcinogenesis Am J Surg Pathol 34 2010 829 836
80. R. Perets, G.A. Wyant, K.W. Muto, J.G. Bijron, B.B. Poole, K.T. Chin, J.Y. Chen, A.W. Ohman, C.D. Stepule, S. Kwak, A.M. Karst, M.S. Hirsch, S.R. Setlur, C.P. Crum, D.M. Dinulescu, and R. Drapkin Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca;Tp53;Pten models Cancer Cell 24 2013 751 765
81. H. Falconer, L. Yin, H. Gronberg, and D. Altman Ovarian cancer risk after salpingectomy: a nationwide population-based study J Natl Cancer Inst 2015 107
82. J.N. McAlpine, G.E. Hanley, M.M. Woo, A.A. Tone, N. Rozenberg, K.D. Swenerton, C.B. Gilks, S.J. Finlayson, D.G. Huntsman, D.M. Miller Ovarian Cancer Research Program of British Columbia Opportunistic salpingectomy: uptake, risks, and complications of a regional initiative for ovarian cancer prevention Am J Obstet Gynecol 210 2014 471.e1 471.e11
83. K. Visvanathan, R. Vang, P. Shaw, A. Gross, R. Soslow, V. Parkash, IeM. Shih, and R.J. Kurman Diagnosis of serous tubal intraepithelial carcinoma based on morphologic and immunohistochemical features: a reproducibility study Am J Surg Pathol 35 2011 1766 1775
84. E. Jarboe, A. Folkins, M.R. Nucci, D. Kindelberger, R. Drapkin, A. Miron, Y. Lee, and C.P. Crum Serous carcinogenesis in the fallopian tube: a descriptive classification Int J Gynecol Pathol 27 2008 1 9
85. I. Espinosa, L. Catasus, B. Canet, E. D'Angelo, J. Munoz, and J. Prat Gene expression analysis identifies two groups of ovarian high-grade serous carcinomas with different prognosis Mod Pathol 24 2011 846 854
86. J.P. Gagner, and K. Mittal Malignant mixed Mullerian tumor of the fimbriated end of the fallopian tube: origin as an intraepithelial carcinoma Gynecol Oncol 97 2005 219 222
87. I.J. Jacobs, U. Menon, A. Ryan, A. Gentry-Maharaj, M. Burnell, J.K. Kalsi, and et al. Ovarian cancer screening and mortality in the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS): a randomised controlled trial Lancet 387 2016 945 956
88. S.S. Buys, E. Partridge, A. Black, C.C. Johnson, L. Lamerato, C. Isaacs, D.J. Reding, R.T. Greenlee, L.A. Yokochi, B. Kessel, E.D. Crawford, T.R. Church, G.L. Andriole, J.L. Weissfeld, M.N. Fouad, D. Chia, B. O'Brien, L.R. Ragard, J.D. Clapp, J.M. Rathmell, T.L. Riley, P. Hartge, P.F. Pinsky, C.S. Zhu, G. Izmirlian, B.S. Kramer, A.B. Miller, J.L. Xu, P.C. Prorok, J.K. Gohagan, C.D. Berg PLCO Project Team Effect of screening on ovarian cancer mortality: the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Randomized Controlled Trial JAMA 305 2011 2295 2303
89. M. Kobel, J. Madore, S.J. Ramus, B.A. Clarke, P.D. Pharoah, S. Deen, and et al. Evidence for a time-dependent association between FOLR1 expression and survival from ovarian carcinoma: implications for clinical testing. An Ovarian Tumour Tissue Analysis consortium study Br J Cancer 111 2014 2297 2307
90. I. Kinde, C. Bettegowda, Y. Wang, J. Wu, N. Agrawal, IeM. Shih, R. Kurman, F. Dao, D.A. Levine, R. Giuntoli, R. Roden, J.R. Eshleman, J.P. Carvalho, S.K. Marie, N. Papadopoulos, K.W. Kinzler, B. Vogelstein, and L.A. Diaz Jr. Evaluation of DNA from the Papanicolaou test to detect ovarian and endometrial cancers Sci Transl Med 5 2013 167ra4
91. J.G. Bijron, C.A. Seldenrijk, R.P. Zweemer, J.G. Lange, R.H. Verheijen, and P.J. van Diest Fallopian tube intraluminal tumor spread from noninvasive precursor lesions: a novel metastatic route in early pelvic carcinogenesis Am J Surg Pathol 37 2013 1123 1130
92. D.A. Fishman, L. Cohen, S.V. Blank, L. Shulman, D. Singh, K. Bozorgi, R. Tamura, I. Timor-Tritsch, and P.E. Schwartz The role of ultrasound evaluation in the detection of early-stage epithelial ovarian cancer Am J Obstet Gynecol 192 2005 1214 1221
93. C.B. Powell, E.M. Swisher, I. Cass, J. McLennan, B. Norquist, R.L. Garcia, J. Lester, B.Y. Karlan, and L. Chen Long term follow up of BRCA1 and BRCA2 mutation carriers with unsuspected neoplasia identified at risk reducing salpingo-oophorectomy Gynecol Oncol 129 2013 364 371
94. J.R. Conner, E. Meserve, E. Pizer, J. Garber, M. Roh, N. Urban, C. Drescher, B.J. Quade, M. Muto, B.E. Howitt, M.D. Pearlman, R.S. Berkowitz, N. Horowitz, C.P. Crum, and C. Feltmate Outcome of unexpected adnexal neoplasia discovered during risk reduction salpingo-oophorectomy in women with germ-line BRCA1 or BRCA2 mutations Gynecol Oncol 132 2014 280 286
95. W.H. Parker, D. Feskanich, M.S. Broder, E. Chang, D. Shoupe, C.M. Farquhar, J.S. Berek, and J.E. Manson Long-term mortality associated with oophorectomy compared with ovarian conservation in the nurses' health study Obstet Gynecol 121 2013 709 716
96. S.L. Wethington, K.J. Park, R.A. Soslow, N.D. Kauff, C.L. Brown, F. Dao, E. Otegbeye, Y. Sonoda, N.R. Abu-Rustum, R.R. Barakat, D.A. Levine, and G.J. Gardner Clinical outcome of isolated serous tubal intraepithelial carcinomas (STIC) Int J Gynecol Cancer 23 2013 1603 1611
97. Collaborative Group on Epidemiological Studies of Ovarian Cancer V. Beral, R. Doll, C. Hermon, R. Peto, and G. Reeves Ovarian cancer and oral contraceptives: collaborative reanalysis of data from 45 epidemiological studies including 23,257 women with ovarian cancer and 87,303 controls Lancet 371 2008 303 314
98. M. Habis, K. Wroblewski, M. Bradaric, N. Ismail, S.D. Yamada, L. Litchfield, E. Lengyel, and I.L. Romero Statin therapy is associated with improved survival in patients with non-serous-papillary epithelial ovarian cancer: a retrospective cohort analysis PLoS One 9 2014 e104521
99. Y. Kobayashi, H. Kashima, R.C. Wu, J.G. Jung, J.C. Kuan, J. Gu, J. Xuan, L. Sokoll, K. Visvanathan, I.M. Shih, and T.L. Wang Mevalonate pathway antagonist suppresses formation of serous tubal intraepithelial carcinoma and ovarian carcinoma in mouse models Clin Cancer Res 21 2015 4652 4662
100. D.T. Le, J.N. Uram, H. Wang, B.R. Bartlett, H. Kemberling, A.D. Eyring, A.D. Skora, B.S. Luber, N.S. Azad, D. Laheru, B. Biedrzycki, R.C. Donehower, A. Zaheer, G.A. Fisher, T.S. Crocenzi, J.J. Lee, S.M. Duffy, R.M. Goldberg, A. de la Chapelle, M. Koshiji, F. Bhaijee, T. Huebner, R.H. Hruban, L.D. Wood, N. Cuka, D.M. Pardoll, N. Papadopoulos, K.W. Kinzler, S. Zhou, T.C. Cornish, J.M. Taube, R.A. Anders, J.R. Eshleman, B. Vogelstein, and L.A. Diaz Jr. PD-1 blockade in tumors with mismatch-repair deficiency N Engl J Med 372 2015 2509 2520
101. B.G. Bitler, K.M. Aird, A. Garipov, H. Li, M. Amatangelo, A.V. Kossenkov, D.C. Schultz, Q. Liu, IeM. Shih, J.R. Conejo-Garcia, D.W. Speicher, and R. Zhang Synthetic lethality by targeting EZH2 methyltransferase activity in ARID1A-mutated cancers Nat Med 21 2015 231 238
102. J. Shen, Y. Peng, L. Wei, W. Zhang, L. Yang, L. Lan, P. Kapoor, Z. Ju, Q. Mo, IeM. Shih, I.P. Uray, X. Wu, P.H. Brown, X. Shen, G.B. Mills, and G. Peng ARID1A deficiency impairs the DNA damage checkpoint and sensitizes cells to PARP inhibitors Cancer Discov 5 2015 752 767
103. J.F. Liu, W.T. Barry, M. Birrer, J.M. Lee, R.J. Buckanovich, G.F. Fleming, B. Rimel, M.K. Buss, S. Nattam, J. Hurteau, W. Luo, P. Quy, C. Whalen, L. Obermayer, H. Lee, E.P. Winer, E.C. Kohn, S.P. Ivy, and U.A. Matulonis Combination cediranib and olaparib versus olaparib alone for women with recurrent platinum-sensitive ovarian cancer: a randomised phase 2 study Lancet Oncol 15 2014 1207 1214
104. K.P. Pennington, T. Walsh, M.I. Harrell, M.K. Lee, C.C. Pennil, M.H. Rendi, A. Thornton, B.M. Norquist, S. Casadei, A.S. Nord, K.J. Agnew, C.C. Pritchard, S. Scroggins, R.L. Garcia, M.C. King, and E.M. Swisher Germline and somatic mutations in homologous recombination genes predict platinum response and survival in ovarian, fallopian tube, and peritoneal carcinomas Clin Cancer Res 20 2014 764 775