Features and complexity of treatment of BRCA-associated ovarian cancer, chronic disease: literature review
https://doi.org/10.17650/1994-4098-2024-20-3-44-51
Abstract
We analyzed literature data on the peculiarities of the clinical manifestation and therapeutic approaches ofB RCA-associated ovarian carcinomas. The ESMO-ESGO consensus emphasised the importance of determining BRCA1/2 status in ovarian cancer patients for planning the entire treatment strategy. BRCA-associated carcinomas differ significantly from sporadic forms in terms of clinical course, response to systemic therapy, spectrum of drugs which are used for treatment, mechanisms of chemoresistance development, and prognosis. This category of patients needs new therapeutic approaches, including the development of tactics to overcome chemoresistance and modification of the entire combined treatment programme.
Supporting agencies: This work was supported by the Russian Science Foundation, grant No. 19-75-10062
About the Authors
T. V. Gorodnova
N.N. Petrov National Medical Research Oncology Center, Ministry of Health of Russia
Russian Federation
Competing Interests:
Russian Federation
68 Leningradskaya St., Pesochnyy Settlement, Saint Petersburg 197758
Competing Interests:
The authors declare no conflict of interest
A. P. Sokolenko
N.N. Petrov National Medical Research Oncology Center, Ministry of Health of Russia; Saint Petersburg State Pediatric Medical University, Ministry of Health of Russia
Russian Federation
Competing Interests:
Russian Federation
68 Leningradskaya St., Pesochnyy Settlement, Saint Petersburg 197758; 2 Litovskaya St., Saint Petersburg 194100
Competing Interests:
The authors declare no conflict of interest
Kh. B. Kotiv
N.N. Petrov National Medical Research Oncology Center, Ministry of Health of Russia; I.I. Mechnikov North-Western State Medical University, Ministry of Health of Russia
Russian Federation
Competing Interests:
Russian Federation
Khristina Bogdanovna Kotiv
68 Leningradskaya St., Pesochnyy Settlement, Saint Petersburg 197758; 41 Kirochnaya St., Saint Petersburg 191015
Competing Interests:
The authors declare no conflict of interest
I. V. Berlev
N.N. Petrov National Medical Research Oncology Center, Ministry of Health of Russia; I.I. Mechnikov North-Western State Medical University, Ministry of Health of Russia
Russian Federation
Competing Interests:
Russian Federation
68 Leningradskaya St., Pesochnyy Settlement, Saint Petersburg 197758; 41 Kirochnaya St., Saint Petersburg 191015
Competing Interests:
The authors declare no conflict of interest
E. N. Imyanitov
N.N. Petrov National Medical Research Oncology Center, Ministry of Health of Russia; Saint Petersburg State Pediatric Medical University, Ministry of Health of Russia
Russian Federation
Competing Interests:
Russian Federation
68 Leningradskaya St., Pesochnyy Settlement, Saint Petersburg 197758; 2 Litovskaya St., Saint Petersburg 194100
Competing Interests:
The authors declare no conflict of interest
References
1. Jayson G.C., Kohn E.C., Kitchener H.C. et al. Ovarian cancer. Lancet 2014;384:1. DOI: 10.1016/S0140-6736(13)62146-7
2. Sundar S., Neal R.D., Kehoe S. Diagnosis of ovarian cancer. BMJ 2015;351:h4443. DOI: 10.1136/bmj.h4443
3. Matulonis U.A., Sood A.K., Fallowfield L. et al. Ovarian cancer. Nat Rev Dis Primers 2016;2:16061. DOI: 10.1038/nrdp.2016.61
4. Van der Velde N.M., Mourits M.J., Arts H.J. et al. Time to stop ovarian cancer screening in BRCA1/2 mutation carriers? Int J Cancer 2009;124:919-23. DOI: 10.1002/ijc.24038
5. Hartmann L.C., Lindor N.M. The role of risk-reducing surgery in hereditary breast and ovarian cancer. N Engl J Med 2016;374:454-68. DOI: 10.1056/NEJMra1503523
6. Kast K., Rhiem K., Wappenschmidt B. et al. Prevalence of BRCA1/2 germline mutations in 21,401 families with breast and ovarian cancer. J Med Genet 2016;53(7):465-71. DOI: 10.1136/jmedgenet-2015-103672
7. NHGRI: Breast Cancer Information Core. Available at: https://research.nhgri.nih.gov/bic/.
8. Gervas P.A., Molokov A.Yu., Panferova E.V. et al. Ethnic aspects of hereditary breast cancer. Sibirskiy onkologicheskiy zhurnal = Siberian Journal of Oncology 2019;18(2):102-8. (In Russ.). DOI: 10.21294/1814-4861-2019-18-2-102-108
9. Brovkina O.I., Gordiev M.G., Shigapova L.H. et al. BRCA1 and BRCA2 genes: population features of the development of breast cancer in Tatar women. Meditsinskaya genetika = Med Genetics 2016;15(10):50-2. (In Russ.).
10. Bogdanova N.V., Antonenkova N.N., Rogov Y.I. et al. High frequency and allele-specific differences of BRCA1 founder mutations in breast cancer and ovarian cancer patients from Belarus. Clin Genet 2010;78(4):364-72. DOI: 10.1111/j.1399-0004.2010.01473.x
11. Sokolenko A.P., Bakaeva E.K., Venina A.R. et al. Ethnicity-specific BRCA1, BRCA2, PALB2, and ATM pathogenic alleles in breast and ovarian cancer patients from the North Caucasus. Breast Cancer Res Treat 2024;203(2):307-15. DOI: 10.1007/s10549-023-07135-3
12. Colombo N., Sessa C., du Bois A. et al. ESMO-ESGO consensus conference recommendations on ovarian cancer: Pathology and molecular biology, early and advanced stages, borderline tumours and recurrent disease. Ann Oncol 2019;30(5):672-705. DOI: 10.1093/annonc/mdz062
13. Quinn J.E., Kennedy R., Mullan P. et al. BRCA1 functions as a differential modulator of chemotherapy-induced apoptosis. Cancer Res 2003;63(19):6221-8.
14. Martin L.P., Hamilton T.C., Schilder R.J. Platinum resistance: The role of DNA repair pathways. Clin Cancer Res 2008;14(5):1291-5. DOI: 10.1158/1078-0432.CCR-07-2238
15. 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(21):2654-63. DOI: 10.1200/JCO.2011.39.8545
16. Tan D.S.P., Yap T., Hutka M. et al. Implications of BRCA1 and BRCA2 mutations for the efficacy of paclitaxel monotherapy in advanced ovarian cancer. Eur Cancer 2013;49(6):1246-53. DOI: 10.1016/j.ejca.2012.11.016
17. Tan D.S.P., Kaye S.B. Chemotherapy for patients with BRCA1 and BRCA2-mutated ovarian cancer: Same or different? Am Soc Clin Oncol Educ B 2015;35:114-21. DOI: 10.14694/EdBook_AM.2015.35.114
18. Gorodnova T., Sokolenko A., Ni V. et al. BRCA1-associated and sporadic ovarian carcinomas: outcomes of primary cytoreductive surgery or neoadjuvant chemotherapy. Int J Gynecol Cancer 2019;29(4):779-86.
19. Reyes M.C., Arnold A.G., Kauff N.D. et al. Invasion patterns of metastatic high-grade serous carcinoma of ovary or fallopian tube associated with BRCA deficiency. Mod Pathol 2014;27:1405. DOI: 10.1038/modpathol.2013.237
20. Petrillo M., Marchetti C., De Leo R. et al. BRCA mutational status, initial disease presentation, and clinical outcome in high-grade serous advanced ovarian cancer: A multicenter study. Am J Obstet Gynecol 2017;217:334.e331-9. DOI: 10.1016/j.ajog.2017.05.036
21. Gourley C., Michie C.O., Roxburgh P. et al. Increased incidence of visceral metastases in Scottish patients with BRCA1/2-defective ovarian cancer: An extension of the ovarian BRCAness phenotype. JCO 2010;28:2505-11. DOI: 10.1200/JCO.2009.25.1082
22. Ratner E., Bala M., Louie-Ga M. et al. Increased risk of brain metastases in ovarian cancer patients with BRCA mutations. Gynecol Oncol 2019;153:568-73. DOI: 10.1016/j.ygyno.2019.03.004
23. Fagotti A., Ferrandina M.G., Vizzielli G. et al. Randomized trial of primary debulking surgery versus neoadjuvant chemotherapy for advanced epithelial ovarian cancer (SCORPION-NCT01461850). Int J Gynecol Cancer 2020;30(11):1657-64. DOI: 10.1136/ijgc-2020-001640
24. Harter P., Sehouli J., Vergote I. et al. DESKTOP III Investigators. Randomized trial of cytoreductive surgery for relapsed ovarian cancer. N Engl J Med 2021;385(23):2123-31. DOI: 10.1056/NEJMoa2103294. Erratum in: N Engl J Med 2022;386(7):704. DOI: 10.1056/NEJMx220002
25. Coleman R.L., Spirtos N.M., Enserro D. et al. Secondary surgical cytoreduction for recurrent ovarian cancer. N Engl J Med 2019;381(20):1929-39. DOI: 10.1056/NEJMoa1902626
26. Climent M.T., Serra A., Llueca M., Llueca A. Surgery in recurrent ovarian cancer: A meta-analysis. Cancers (Basel) 2023;15(13):3470. DOI: 10.3390/cancers15133470
27. Harter P., Sehouli J., Reuss A. et al. Prospective validation study of a predictive score for operability of recurrent ovarian cancer: the Multicenter Intergroup Study DESKTOP II. A project of the AGO Kommission OVAR, AGO Study Group, NOGGO, AGO-Austria, and MITO. Int J Gynecol Cancer 2011;21(2):289-95. DOI: 10.1097/IGC.0b013e31820aaafd
28. Chi D.S., McCaughty K., Diaz J.P. et al. Guidelines and selection criteria for secondary cytoreductive surgery in patients with recurrent, platinum-sensitive epithelial ovarian carcinoma. Cancer 2006;106(9):1933-9. DOI: 10.1002/cncr.21845
29. Roy R., Chun J., Powell S.N. BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nat Rev Cancer 2011;12(1):68-78. DOI: 10.1038/nrc3181
30. Yoshida K., Miki Y. Role of BRCA1 and BRCA2 as regulators of DNA repair, transcription, and cell cycle in response to DNA damage. Cancer Sci 2004;95(11):866-71. DOI: 10.1111/j.1349-7006.2004.tb02195.x
31. Imyanitov E.N., Kuligina E.S., Sokolenko A.P. et al. Hereditary cancer syndromes. World J Clin Oncol 2023;14(2):40-68. DOI: 10.5306/wjco.v14.i2.40
32. Gorodnova T.V., Sokolenko A.P., Ivantsov A.O. et al. High response rates to neoadjuvant platinum-based therapy in ovarian cancer patients carrying germ-line BRCA mutation. Cancer Lett 2015;369(2):363-7. DOI: 10.1016/j.canlet.2015.08.028
33. Clinical recommendations of the Ministry of Health of the Russian Federation “Ovarian cancer/fallopian tube cancer/primary peritoneal cancer”. Available at: https://cr.minzdrav.gov.ru/recomend/547. (In Russ.).
34. Bolton K.L., Chenevix-Trench G., Goh C. et al. Cancer Genome Atlas Research Network. Association between BRCA1 and BRCA2 mutations and survival in women with invasive epithelial ovarian cancer. JAMA 2012;307(4):382-90. DOI: 10.1001/jama.2012.20
35. Sun C., Li N., Ding D. et al. The role of BRCA status on the prognosis of patients with epithelial ovarian cancer: A systematic review of the literature with a meta-analysis. PLoS One 2014;9(5):e95285. DOI: 10.1371/journal.pone.0095285
36. Martin L.P., Hamilton T.C., Schilder R.J. Platinum resistance: The role of DNA repair pathways. Clin Cancer Res 2008;14(5):1291-5. DOI: 10.1158/1078-0432.CCR-07-2238
37. Siddik Z.H. Cisplatin: Mode of cytotoxic action and molecular basis of resistance. Oncogene 2003;22(47):7265-79. DOI: 10.1038/sj.onc.1206933
38. Quinn J.E., James C.R., Stewart G.E. et al. BRCA1 mRNA expression levels predict for overall survival in ovarian cancer after chemotherapy. Clin Cancer Res 2007;13(24):7413-20. DOI: 10.1158/1078-0432.CCR-07-1083
39. Gorodnova T.V., Kotiv K.B., Ivantsov A.O. et al. Efficacy of neoadjuvant therapy with cisplatin plus mitomycin c in BRCA1- mutated ovarian cancer. Int J Gynecol Cancer 2018;28(8): 1498-506. DOI: 10.1097/IGC.0000000000001352
40. Gorodnova T.V., Sokolenko A.P., Kondratiev S.V. et al. Mitomycin C plus cisplatin for systemic treatment of recurrent BRCA1-associated ovarian cancer. Invest New Drugs 202;38(6):1872-8. DOI: 10.1007/s10637-020-00965-8
41. Gorodnova T.V., Sokolenko A.P., Kotiv K.B. et al. Neoadjuvant therapy of BRCA1-driven ovarian cancer by combination of cisplatin, mitomycin C and doxorubicin. Hered Cancer Clin Pract 2021;19(1):14. DOI: 10.1186/s13053-021-00173-2
42. Gorodnova T.V., Sokolenko A.P., Kotiv Kh.B. et al. Prospective randomized study evaluating the effectiveness of mitomycin C and cisplatin (MP) regimen in comparison with standard first-line chemotherapy in patients with advanced BRCA1/2-associated ovarian cancer (NCT04747717). Voprosy onkologii = Oncology Issues 2022;68(5):628-38. (In Russ.). DOI: 10.37469/0507-3758-2022-68-5-628-638
43. Chen S., Parmigiani G. Meta-analysis of BRCA1 and BRCA2 penetrance. J Clin Oncol 2007;25(11):1329-33. DOI: 10.1200/JCO.2006.09.1066
44. Yang D., Khan S., Sun Y. et al. Association of BRCA1 and BRCA2 mutations with survival, chemotherapy sensitivity, and gene mutator phenotype in patients with ovarian cancer. JAMA 2011;306(14):1557-65. DOI: 10.1001/jama.2011.1456. Erratum in: JAMA 2012;307(4):363.
45. Ovejero-Sanchez M., Gonzalez-Sarmiento R., Herrero A.B. DNA damage response alterations in ovarian cancer: from molecular mechanisms to therapeutic opportunities. Cancers (Basel) 2023;15(2):448. DOI: 10.3390/cancers15020448
46. Hyman D.M., Zhou Q., Iasonos A. et al. Improved survival for BRCA2-associated serous ovarian cancer compared with both BRCA-negative and BRCA1-associated serous ovarian cancer. Cancer 2012;118(15):3703-9. DOI: 10.1002/cncr.26655
47. Sazonova E.V., Kopeina G.S., Imyanitov E.N., Zhivotovsky B. Platinum drugs and taxanes: Can we overcome resistance? Cell Death Discov 2021;7(1):155. DOI: 10.1038/s41420-021-00554-5
48. Iyevleva A.G., Imyanitov E.N. Cytotoxic and targeted therapy for hereditary cancers. Hered Cancer Clin Pract 2016;14(1):17. DOI: 10.1186/s13053-016-0057-2
49. Pettitt S.J., Frankum J.R., Punta M. et al. Clinical BRCA1/2 reversion analysis identifies hotspot mutations and predicted neoantigens associated with therapy resistance. Cancer Discov 2020;10:1475-88. DOI: 10.1158/2159-8290.CD-19-1485
50. Markman M., Rothman R., Hakes T. et al. Second-line platinum therapy in patients with ovarian cancer previously treated with cisplatin. J Clin Oncol 1991:389-93. DOI: 10.1200/JCO.1991.9.3.389
51. Lord C.J., Ashworth A. Mechanisms of resistance to therapies targeting BRCA-mutant cancers. Nat Med 2013;19(11):1381-8. DOI: 10.1038/nm.3369
52. Sokolenko A., Bizin I., Preobrazhenskaya E. et al. Molecular profiles of BRCA1-associated ovarian cancer treated by platinum-based therapy: Analysis of primary, residual and relapsed tumors. Int J Cancer 2020;146:1879-88.
53. Sokolenko A.P., Savonevich E.L., Ivantsov A.O. et al. Rapid selection of BRCA1-proficient tumor cells during neoadjuvant therapy for ovarian cancer in BRCA1 mutation carriers. Cancer Lett 2017;397:127-32. DOI: 10.1016/j.canlet.2017.03.036
54. Sokolenko A.P., Bizin I.V., Preobrazhenskaya E.V. et al. Molecular profiles of BRCA1-associated ovarian cancer treated by platinum-based therapy: Analysis of primary, residual and relapsed tumors. Int J Cancer 2020;146:1879-88. DOI: 10.1002/ijc.32776
55. Klotz D.M., Wimberger P. Overcoming PARP inhibitor resistance in ovarian cancer: What are the most promising strategies? Arch Gynecol Obstet 2020;302:1087-102. DOI: 10.1007/s00404-020-05677-1
56. Jiang X., Li X., Li W et al. PARP inhibitors in ovarian cancer: Sensitivity prediction and resistance mechanisms. J Cell Mol Med 2019;23:2303-13. DOI: 10.1111/jcmm.14133
57. Frenel J.S., Kim J.W., Aryal N. et al. Efficacy of subsequent chemotherapy for patients with BRCA1/2-mutated recurrent epithelial ovarian cancer progressing on olaparib versus placebo maintenance: Post-hoc analyses of the SOLO2/ENGOT Ov-21 trial. Ann Oncol 2022;33(10):1021-8. DOI: 10.1016/j.annonc.2022.06.011
58. Cecere S.C., Giannone G., Salutari V. et al. Olaparib as maintenance therapy in patients with BRCA1/2 mutated recurrent platinum sensitive ovarian cancer: Real world data and post progression outcome. Gynecol Oncol 2020;156:38-44. DOI: 10.1016/j.annonc.2022.06.011
59. Suprasert P., Manopunya M., Cheewakriangkrai C. Outcomes with single agent LIPO-DOX in platinum-resistant ovarian and fallopian tube cancers and primary peritoneal adenocarcinoma - Chiang Mai University Hospital experience. Asian Pac J Cancer Prev 2014;15(3):1145-8. DOI: 10.7314/apjcp.2014.15.3.1145
60. Gordon A.N., Fleagle J.T., Guthrie D. et al. Recurrent epithelial ovarian carcinoma: A randomized phase III study of pegylated liposomal doxorubicin versus topotecan. J Clin Oncol 2001;19:3312-22. DOI: 10.1200/JCO.2001.19.14.3312
61. Kaye S.B., Lubinski J., Matulonis U. et al. Phase II, open-label, randomized, multicenter study comparing the efficacy and safety of olaparib, a poly (ADP-ribose) polymerase inhibitor, and pegylated liposomal doxorubicin in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer. J Clin Oncol 2012;30:372-9. DOI: 10.1200/JCO.2011.36.9215
62. Gorodnova T.V., Sokolenko A.P., Kotiv Kh.B. et al. Platinum resistance after neoadjuvant chemotherapy. Voprosy onkologii = Oncology Issues 2024;70(1):82-8. (In Russ.). DOI: 10.37469/0507-3758-2024-70-1-82-87
63. Markman M. Why study third-, fourth-, fifth-, ...line chemotherapy of ovarian cancer? Gynecol Oncol 2001;83(3):449-50. DOI: 10.1006/gyno.2001.6458
64. Holstege H., Joosse S.A., van Oostrom C.T. et al. High incidence of protein-truncating TP53 mutations in BRCA1-related breast cancer. Cancer Res 2009;69(8):3625-33. DOI: 10.1158/0008-5472.CAN-08-3426
65. Sokolenko A.P., Gorodnova T.V., Bizin I.V. et al. Molecular predictors of the outcome of paclitaxel plus carboplatin neoadjuvant therapy in high-grade serous ovarian cancer patients. Cancer Chemother Pharmacol 2021;88(3):439-50. DOI: 10.5306/wjco.v14.i2.40
66. El-Husseiny Kh., Motawei H., Sayed Ali M. Continuous low-dose oral cyclophosphamide and methotrexate as maintenance therapy in patients with advanced ovarian carcinoma after complete clinical response to platinum and paclitaxel chemotherapy. Int J Gynecol Cancer 2016;26(3):437-42. DOI: 10.1097/IGC.0000000000000647
67. Chubenko V.A., Zagorskaya L.A., Chubenko V.S. et al. Metronomic therapy: place in the treatment of malignant tumors. Prakticheskaya onkologiya = Practical Oncology 2019;20(4):289-98. (In Russ.). DOI: 10.31917/2004289
68. Spiliopoulou P., Hinsley S., McNeish I.A. et al. Metronomic oral cyclophosphamide in relapsed ovarian cancer. Int J Gynecol Cancer 2021;31(7):1037-44. DOI: 10.1136/ijgc-2021-002467
69. Motoyoshi Y., Kaminoda K., Saitoh O. et al. Different mechanisms for anti-tumor effects of low- and high-dose cyclophosphamide. Oncol Rep 2006;16(1):141-6.
70. Ghiringhelli F., Menard C., Puig P.E. et al. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother 2007;56(5):641-8. DOI: 10.1007/s00262-006-0225-8
71. Sokolenko A., Ivantsov A., Gorodnova T. et al. Immune microenvironment in high-grade serous ovarian carcinomas: association with molecular characteristics and response to standard neoadjuvant therapy. Voprosy onkologii = Oncology Issues 2023;69(1):74-81. (In Russ.). DOI: 10.37469/0507-3758-2023-69-1-74-81
Review
For citations:
Gorodnova T.V., Sokolenko A.P., Kotiv Kh.B., Berlev I.V., Imyanitov E.N. Features and complexity of treatment of BRCA-associated ovarian cancer, chronic disease: literature review. Tumors of female reproductive system. 2024;20(3):44-51. (In Russ.) https://doi.org/10.17650/1994-4098-2024-20-3-44-51
Views:
180
Email this article 