Molecular alterations in mucinous ovarian tumors – a review

1 Cheasley D, Wakefield MJ, Ryland GL, Allan PE, Alsop K, Amarasinghe KC, et al. The molecular origin and taxonomy of mucinous ovarian carcinoma. Nat Commun. 2019;10(1). Search in Google Scholar

2 Mills AM, Shanes ED. Mucinous ovarian tumors. Surg Pathol Clin. 2019;12:565-85. Search in Google Scholar

3 Kubeček O, Laco J, Špaček J, Petera J, Kopecký J, Kubečková A, et al. The pathogenesis, diagnosis, and management of metastatic tumors to the ovary: a comprehensive review. Clin Exp Metastasis. 2017; 34:295-307. Search in Google Scholar

4 Dundr P, Singh N, Nožičková B, Němejcová K, Bártů M, Stružinská I. Primary mucinous ovarian tumors vs. ovarian metastases from gastrointestinal tract, pancreas and biliary tree: a review of current problematics. Diagn Pathol. 2021;16(1):20. Search in Google Scholar

5 Hollis RL. Molecular characteristics and clinical behaviour of epithelial ovarian cancers. Cancer Lett. 2023;555:216057. Search in Google Scholar

6 Ordulu Z, Watkins J, Ritterhouse LL. Molecular pathology of ovarian epithelial neoplasms: predictive, prognostic, and emerging biomarkers. Surg Pathol Clin. 2021;14:415-28. Search in Google Scholar

7 Dion L, Carton I, Jaillard S, Timoh KN, Henno S, Sardain H, et al. The landscape and therapeutic implications of molecular profiles in epithelial ovarian cancer. J Clin Med. 2020;9:1-12. Search in Google Scholar

8 Dundr P, Bártů M, Bosse T, Bui QH, Cibula D, Drozenová J, et al. Primary mucinous tumors of the ovary: An interobserver reproducibility and detailed molecular study reveals significant overlap between diagnostic categories. Mod Pathol. 2023;36(1): 100040. Search in Google Scholar

9 Mehra P, Aditi S, Prasad KM, Bariar NK. Histomorphological analysis of ovarian neoplasms according to the 2020 WHO classification of ovarian tumors: A distribution pattern in a tertiary care center. Cureus. 2023;15(4). Search in Google Scholar

10 Köbel M, Kang EY. The evolution of ovarian carcinoma subclassification. Cancers. 2022;14:416. Search in Google Scholar

11 Xu W, Rush J, Rickett K, Coward JIG. Mucinous ovarian cancer: A therapeutic review. Crit Rev Oncol Hematol. 2016;102:26-36. Search in Google Scholar

12 Talia KL, Parra-Herran C, McCluggage WG. Ovarian mucinous and seromucinous neoplasms: problematic aspects and modern diagnostic approach. Histopathology. 2022;80:255-78. Search in Google Scholar

13 Ledermann JA, Luvero D, Shafer A, O’Connor D, Mangili G, Friedlander M, et al. Gynecologic cancer intergroup (GCIG) Consensus review for mucinous ovarian carcinoma. Int J Gynecol Cancer. 2014;24:14-9. Search in Google Scholar

14 Hart WRMD. Mucinous tumors of the ovary: A review. Int J Gynecol Pathol. 2005;24(1):4-25. Search in Google Scholar

15 Babaier A, Ghatage P. Mucinous cancer of the ovary: Overview and current status. Diagnostics. 2020;10(1):52. Search in Google Scholar

16 Nistor S, El-Tawab S, Wong F, Zouridis A, Roux R, Manek S, et al. The clinicopathological characteristics and survival outcomes of primary expansile vs. infiltrative mucinous ovarian adenocarcinoma: a retrospective study sharing the experience of a tertiary centre. Transl Cancer Res. 2023;12(10):2682-92. Search in Google Scholar

17 Gershenson DM. Management of borderline ovarian tumours. Best Pract Res Clin Obstet Gynaecol. 2017;41:49-59. Search in Google Scholar

18 Song T, Lee YY, Choi CH, Kim TJ, Lee JW, Bae DS, et al. Histologic distribution of borderline ovarian tumors worldwide: A systematic review. J Gynecol Oncol. 2012;24(1):44-51. Search in Google Scholar

19 Muyldermans K, Moerman P, Amant F, Leunen K, Neven P, Vergote I. Primary invasive mucinous ovarian carcinoma of the intestinal type: Importance of the expansile versus infiltrative type in predicting recurrence and lymph node metastases. Eur J Cancer. 2013;49(7):1600-8. Search in Google Scholar

20 Huin M, Lorenzini J, Arbion F, Carcopino X, Touboul C, Dabi Y, et al. Presentation and prognosis of primary expansile and infiltrative mucinous carcinomas of the ovary. J Clin Med. 2022;11(20). Search in Google Scholar

21 Lee KR, Scully RE. Mucinous tumors of the ovary a clinicopathologic study of 196 borderline tumors (of intestinal type) and carcinomas, including an evaluation of 11 cases with “pseudomyxoma peritonei”. Am J Surg Path. 2000;24(11):1447-64. Search in Google Scholar

22 Cobb LP, Gershenson DM. Treatment of rare epithelial ovarian tumors. Hematol Oncol Clin North Am. 2018;32:1011-24. Search in Google Scholar

23 Shimada M, Kigawa J, Ohishi Y, Yasuda M, Suzuki M, Hiura M, et al. Clinicopathological characteristics of mucinous adenocarcinoma of the ovary. Gynecol Oncol. 2009;113(3):331-4. Search in Google Scholar

24 Kondi-Pafiti A, Kairi-Vasilatou E, Iavazzo C, Dastamani C, Bakalianou K, Liapis A, et al. Metastatic neoplasms of the ovaries: A clinicopathological study of 97 cases. Arch Gynecol Obstet. 2011;284(5):1283-8. Search in Google Scholar

25 Carr NJFrcp, Cecil TDM, Mohamed FM, Sobin LHM, Sugarbaker PHM, González-Moreno SMP, et al. A consensus for classification and pathologic reporting of pseudomyxoma peritonei and associated appendiceal neoplasia the results of the Peritoneal Surface Oncology Group International (PSOGI) Modified Delphi Process. Am J Surg Pathol. 2016;40(1):14-26. Search in Google Scholar

26 Kelemen LE, Köbel M. Mucinous carcinomas of the ovary and colorectum: different organ, same dilemma. Lancet Oncol. 2011;12(11):1071-80. Search in Google Scholar

27 Bassiouny D, Ismiil N, Dubé V, Han G, Cesari M, Lu FI, et al. Comprehensive clinicopathologic and updated immunohistochemical characterization of primary ovarian mucinous carcinoma. Int J Surg Pathol. 2018;26(4):306-17. Search in Google Scholar

28 Hu A, Li H, Zhang L, Ren C, Wang Y, Liu Y, et al. Differentiating primary and extragenital metastatic mucinous ovarian tumours: an algorithm combining PAX8 with tumour size and laterality. J Clin Pathol. 2015;68(7):522-8. Search in Google Scholar

29 Stelow EB, Yaziji H. Immunohistochemistry, carcinomas of unknown primary, and incidence rates. Semin Diagn Pathol. 2018;35(2):143-52. Search in Google Scholar

30 Li X, Beihua K. PAX8 is a novel marker for differentiating between various types of tumor, particularly ovarian epithelial carcinomas (review). Oncol Lett. 2013;5(3):735-8. Search in Google Scholar

31 Aldaoud N, Erashdi M, Alkhatib S, Abdo N, Al-Mohtaseb A, Graboski-Bauer A. The utility of PAX8 and SATB2 immunohistochemical stains in distinguishing ovarian mucinous neoplasms from colonic and appendiceal mucinous neoplasm. BMC Res Notes. 2019;12(1). Search in Google Scholar

32 Gouy S, Saidani M, Maulard A, Bach-Hamba S, Bentivegna E, Leary A, et al. Characteristics and prognosis of stage i ovarian mucinous tumors according to expansile or infiltrative type. Int J Gynecol Cancer. 2018;28(3):493-9. Search in Google Scholar

33 Yoshikawa N, Kajiyama H, Mizuno M, Shibata K, Kawai M, Nagasaka T, et al. Clinicopathologic features of epithelial ovarian carcinoma in younger vs. older patients: Analysis in Japanese women. J Gynecol Oncol. 2014;25(2):118-23. Search in Google Scholar

34 Brown J, Frumovitz M. Mucinous tumors of the ovary: Current thoughts on diagnosis and management. Curr Oncol Rep. 2014;16(6). Search in Google Scholar

35 Mackenzie R, Kommoss S, Winterhoff BJ, Kipp BR, Garcia JJ, Voss J, et al. Targeted deep sequencing of mucinous ovarian tumors reveals multiple overlapping RAS-pathway activating mutations in borderline and cancerous neoplasms. BMC Cancer. 2015;15(1). Search in Google Scholar

36 Hunter SM, Gorringe KL, Christie M, Rowley SM, Bowtell DD, Campbell IG. Pre-invasive ovarian mucinous tumors are characterized by CDKN2A and RAS pathway aberrations. Clin Cancer Res. 2012;18(19):5267-77. Search in Google Scholar

37 Morice P, Gouy S, Leary A. Mucinous ovarian carcinoma. N Eng J Med. 2019;380(13):1256-66. Search in Google Scholar

38 Lee YJ, Lee MY, Ruan A, Chen CK, Liu HP, Wang CJ, et al. Multipoint Kras oncogene mutations potentially indicate mucinous carcinoma on the entire spectrum of mucinous ovarian neoplasms. Oncotarget. 2016;7. Search in Google Scholar

39 Ryland GL, Hunter SM, Doyle MA, Caramia F, Li J, Rowley SM, et al. Mutational landscape of mucinous ovarian carcinoma and its neoplastic precursors. Genome Med. 2015;7(1). Search in Google Scholar

40 Bouri S, Simon P, D’Haene N, Catteau X, Noël JC. P53 and PIK3CA mutations in KRAS/HER2 negative ovarian intestinal-type mucinous carcinoma associated with mature teratoma. Case Rep Obstet Gynecol. 2020;2020. Search in Google Scholar

41 Mueller JJ, Schlappe BA, Kumar R, Olvera N, Dao F, Abu-Rustum N, et al. Massively parallel sequencing analysis of mucinous ovarian carcinomas: genomic profiling and differential diagnoses. Gynecol Oncol. 2018;150(1):127-35. Search in Google Scholar

42 Anglesio MS, Kommoss S, Tolcher MC, Clarke B, Galletta L, Porter H, et al. Molecular characterization of mucinous ovarian tumours supports a stratified treatment approach with HER2 targeting in 19% of carcinomas. J Pathol. 2013;229(1):111-20. Search in Google Scholar

43 Bashashati A, Ha G, Tone A, Ding J, Prentice LM, Roth A, et al. Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling. J Pathol. 2013;231(1):21-34. Search in Google Scholar

44 Bell D, Berchuck A, Birrer M, Chien J, Cramer DW, Dao F, et al. Integrated genomic analyses of ovarian carcinoma. Nature. 2011; 74(7353):609-15. Search in Google Scholar

45 Jones S, Wang TL, Kurman RJ, Nakayama K, Velculescu VE, Vogelstein B, et al. Low-grade serous carcinomas of the ovary contain very few point mutations. J Pathol. 2012;226(3):413-20. Search in Google Scholar

46 Iida Y, Okamoto A, Hollis RL, Gourley C, Herrington CS. Clear cell carcinoma of the ovary: A clinical and molecular perspective. Int J Gynecol Cancer. 2021;31:605-16. Search in Google Scholar

47 Itamochi H, Oishi T, Oumi N, Takeuchi S, Yoshihara K, Mikami M, et al. Whole-genome sequencing revealed novel prognostic biomarkers and promising targets for therapy of ovarian clear cell carcinoma. Br J Cancer. 2017;117(5):717-24. Search in Google Scholar

48 Bolton KL, Chen D, de la Fuente RC, Fu Z, Murali R, Köbel M, et al. Molecular subclasses of clear cell ovarian carcinoma and their impact on disease behavior and outcomes. Clin Cancer Res. 2022; 28(22):4947-56. Search in Google Scholar

49 Friedlander ML, Russell K, Millis S, Gatalica Z, Bender R, Voss A. Molecular profiling of clear cell ovarian cancers: Identifying potential treatment targets for clinical trials. Int J Gynecol Cancer. 2016;26(4):648-54. Search in Google Scholar

50 Cybulska P, Paula ADC, Tseng J, Leitao MM, Bashashati A, Huntsman DG, et al. Molecular profiling and molecular classification of endometrioid ovarian carcinomas. Gynecol Oncol. 2019;154(3): 516-23. Search in Google Scholar

51 Pierson WE, Peters PN, Chang MT, Chen L may, Quigley DA, Ashworth A, et al. An integrated molecular profile of endometrioid ovarian cancer. Gynecol Oncol. 2020;157(1):55-61. Search in Google Scholar

52 Crobach S, Ruano D, Van Eijk R, Fleuren GJ, Minderhout I, Snowdowne R, et al. Target-enriched next-generation sequencing reveals differences between primary and secondary ovarian tumors in formalin-fixed, paraffin-embedded tissue. J Mol Diagn. 2015;17(2): 193-200. Search in Google Scholar

53 Garg S, Nagaria TS, Clarke B, Freedman O, Khan Z, Schwock J, et al. Molecular characterization of gastric-type endocervical adenocarcinoma using next-generation sequencing. Mod Pathol. 2019;32(12):1823-33. Search in Google Scholar

54 Hodgson A, Howitt BE, Park KJ, Lindeman N, Nucci MR, Parra-Herran C. Genomic characterization of HPV-related and gastric-type endocervical adenocarcinoma: Correlation with subtype and clinical behavior. Int J Gynecol Pathol. 2020;39(6):578-86. Search in Google Scholar

55 Jang JYA, Yanaihara N, Pujade-Lauraine E, Mikami Y, Oda K, Bookman M, et al. Update on rare epithelial ovarian cancers: Based on the rare ovarian tumors young investigator conference. J Gynecol Oncol. 2017;28(4):e54. Search in Google Scholar

56 Craig O, Salazar C, Gorringe KL. Options for the treatment of mucinous ovarian carcinoma. Curr Treat Options Oncol. 2021;22(12): 114. Search in Google Scholar

57 Gorringe KL, Cheasley D, Wakefield MJ, Ryland GL, Allan PE, Alsop K, et al. Therapeutic options for mucinous ovarian carcinoma. Gynecol Oncol. 2020;156(3):552-60. Search in Google Scholar

58 Hurwitz HI, Tebbutt NC, Kabbinavar F, Giantonio BJ, Guan ZZ, Mitchell L, et al. Efficacy and safety of bevacizumab in metastatic colorectal cancer: Pooled analysis from seven randomized controlled trials. Oncologist. 2013;18(9):1004-12. Search in Google Scholar

59 Macedo LT, da Costa Lima AB, Sasse AD. Addition of bevacizumab to first-line chemotherapy in advanced colorectal cancer: A systematic review and meta-analysis, with emphasis on chemotherapy subgroups. BMC Cancer. 2012;12:89. Search in Google Scholar

60 Pujade-Lauraine E, Hilpert F, Weber B, Reuss A, Poveda A, Kristensen G, et al. Bevacizumab combined with chemotherapy for platinum-resistant recurrent ovarian cancer: The AURELIA open-label randomized phase III trial. J Clin Oncol. 2014;32(13):1302-8. Search in Google Scholar

61 Perren TJ, Swart AM, Pfisterer J, Ledermann JA, Pujade-Lauraine E, Kristensen G, et al. A phase 3 trial of bevacizumab in ovarian cancer. N Eng J Med. 2011;365(26):2484-96. Search in Google Scholar

62 Burger RA, Brady MF, Bookman MA, Fleming GF, Monk BJ, Huang H, et al. Incorporation of Bevacizumab in the Primary Treatment of Ovarian Cancer. N Eng J Med. 2011;365(26):2473-83. Search in Google Scholar

63 Aghajanian C, Blank S V., Goff BA, Judson PL, Teneriello MG, Husain A, et al. OCEANS: A randomized, double-blind, placebo-controlled phase III trial of chemotherapy with or without bevacizumab in patients with platinum-sensitive recurrent epithelial ovarian, primary peritoneal, or fallopian tube cancer. J Clin Oncol. 2012;30(17):2039-45. Search in Google Scholar

64 Schilder RJ, Pathak HB, Lokshin AE, Holloway RW, Alvarez RD, Aghajanian C, et al. Phase II trial of single agent cetuximab in patients with persistent or recurrent epithelial ovarian or primary peritoneal carcinoma with the potential for dose escalation to rash. Gynecol Oncol. 2009;113(1):21-7. Search in Google Scholar

65 Konner J, Schilder RJ, DeRosa FA, Gerst SR, Tew WP, Sabbatini PJ, et al. A phase II study of cetuximab/paclitaxel/carboplatin for the initial treatment of advanced-stage ovarian, primary peritoneal, or fallopian tube cancer. Gynecol Oncol. 2008;110(2):140-5. Search in Google Scholar

66 Sato N, Saga Y, Mizukami H, Wang D, Fujiwara H, Takei Y, et al. Cetuximab inhibits the growth of mucinous ovarian carcinoma tumor cells lacking KRAS gene mutations. Oncol Rep. 2012;27(5):1336-40. Search in Google Scholar

67 McAlpine JN, Wiegand KC, Vang R, Ronnett BM, Adamiak A, Köbel M, et al. HER2 overexpression and amplification is present in a subset of ovarian mucinous carcinomas and can be targeted with trastuzumab therapy. BMC Cancer. 2009;9:433. Search in Google Scholar

68 Zaino RJ, Brady MF, Lele SM, Michael H, Greer B, Bookman MA. Advanced stage mucinous adenocarcinoma of the ovary is both rare and highly lethal. Cancer. 2011;117(3):554-62. Search in Google Scholar