Treatment options in recurrent ovarian cancer: Latest evidence and clinical potential

Therapeutic Advances in Medical Oncology

Volumn 6, Issue 5, 2014, Pages 229-239

  Luvero, Daniela ^a   Milani, Andrea ^b   Ledermann, Jonathan A ^c  

^a UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

bevacizumab; platinum resistant; platinum sensitive; poly ADP ribose polymerase inhibitors; relapsed ovarian cancer

Indexed keywords

BEVACIZUMAB; CARBOPLATIN; CEDIRANIB; CISPLATIN; ETOPOSIDE; GEMCITABINE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB; PACLITAXEL; RUCAPARIB; TOPOTECAN; TRABECTEDIN; TREBANANIB; VASCULOTROPIN; VINTAFOLIDE;

CANCER CHEMOTHERAPY; CANCER RECURRENCE; CANCER SURGERY; CANCER THERAPY; DRUG EFFICACY; DRUG SENSITIVITY; FEMALE; HUMAN; MOLECULARLY TARGETED THERAPY; OVARY CANCER; RETREATMENT; REVIEW; TREATMENT RESPONSE;

EID: 84908212684     PISSN: 17588340     EISSN: 17588359     Source Type: Journal    
DOI: 10.1177/1758834014544121     Document Type: Review

References (67)

1. Aghajanian C. Blank S. Goff B. Judson P. Teneriello M. Husain A. et al. (2012) 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 30: 2039–2045.
2. Alberts D. Liu P. Wilczynski S. Clouser M. Lopez A. Michelin D. et al. (2008) Randomized trial of pegylated liposomal doxorubicin (PLD) plus carboplatin versus carboplatin in platinum-sensitive (PS) patients with recurrent epithelial ovarian or peritoneal carcinoma after failure of initial platinum-based chemotherapy (Southwest Oncology Group Protocol S0200). Gynecol Oncol 108: 90–94.
3. Alsop K. Fereday S. Meldrum C. Defazio A. Emmanuel C. George J. et al. (2012) 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 Crit Oncol 30: 2654–2663.
4. Audeh M. Carmichael J. Penson R. Friedlander M. Powell B. Bell-Mcguinn K. et al. (2010) Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA 1 or BRCA 2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet 376: 245–251.
5. Bafaloukos D. Linardou H. Aravantinos G. Papadimitriou C. Bamias A. Fountzilas G. et al. (2010) A randomized phase II study of carboplatin plus pegylated liposomal doxorubicin versus carboplatin plus paclitaxel in platinum sensitive ovarian cancer patients: a Hellenic Cooperative Oncology Group Study. BMC Med 8: 3.
6. Bell D. Berchuck A. Birrer M. Chien J. Cramer D. Dao F. et al. (2011) Integrated genomic analyses of ovarian carcinoma. Nature 474: 609–615.
7. Bolis G. Scarfone G. Giardina G. Villa A. Mangili G. Melpignano M. et al. (2001) Carboplatin alone vs carboplatin plus epidoxorubicin as second-line therapy for cisplatin- or carboplatin-sensitive ovarian cancer. Gynecol Oncol 81: 3–9.
8. Bozas G. Bamias A. Koutsoukou V. Efstathiou E. Gika D. Papadimitriou C. et al. (2007) Biweekly gemcitabine and cisplatin in platinum-resistant/refractory, paclitaxel-pretreated, ovarian and peritoneal carcinoma. Gynecol Oncol 104: 580–585.
9. Bryant C. Kumar S. Spannuth W. Shah J. Munkarah A. Deppe G. et al. (2011) Feasibility of extension of platinum-free interval with weekly bolus topotecan and subsequent platinum retreatment outcomes in recurrent ovarian cancer. Arch Gynecol Obstet 283: 361–367.
10. Buda A. Floriani I. Rossi R. Colombo N. Torri V. Conte P. et al. (2004) Randomised controlled trial comparing single agent paclitaxel vs epidoxorubicin plus paclitaxel in patients with advanced ovarian cancer in early progression after platinum-based chemotherapy: an Italian collaborative study from the Mario Negri Institute, Milan, G.O.N.O. (Gruppo Oncologico Nord Ovest) Group and I.O.R. (Istituto Oncologico Romagnolo) Group. Br J Cancer 90: 2112–2117.
11. Burger R. (2011) Overview of anti-angiogenic agents in development for ovarian cancer. Gynecol Oncol 121: 230–238.
12. Burger R. Sill M. Monk B. Greer B. Sorosky J. (2007) Phase II trial of bevacizumab in persistent or recurrent epithelial ovarian cancer or primary peritoneal cancer: a Gynecologic Oncology Group Study. J Clin Oncol 25: 5165–5171.
13. Colombo N. Kutarska E. Dimopoulos M. Bae D. Rzepka-Gorska I. Bidzinski M. et al. (2012) Randomized, open-label, phase III study comparing patupilone (EPO906) with pegylated liposomal doxorubicin in platinum-refractory or -resistant patients with recurrent epithelial ovarian, primary fallopian tube, or primary pritoneal cancer. J Clin Oncol 30: 3841–3847.
14. Eisenhauer E. Vermorken J. van Glabbeke M. (1997) Predictors of response to subsequent chemotherapy in platinum pretreated ovarian cancer: a multivariate analysis of 704 patients. Ann Oncol 8: 963–968.
15. Fong P. Boss D. Yap T. Tutt A. Wu P. Mergui-Roelvink M. et al. (2009) Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 361: 123–134.
16. Friedlander M. Trimble E. Tinker A. Alberts D. Avall-Lundqvist E. Brady M. et al. (2011) Clinical trials in recurrent ovarian cancer. Int J Gynecol Cancer 21: 771–775.
17. Garcia A. Hirte H. Fleming G. Yang D. Tsao-Wei D. Roman L. et al. (2008) Phase II clinical trial of bevacizumab and low-dose metronomic oral cyclophosphamide in recurrent ovarian cancer: a trial of the California, Chicago, and Princess Margaret Hospital Phase II Consortia. J Clin Oncol 26: 76–82.
18. Gelmon K. Tischkowitz M. Mackay H. Swenerton K. Robidoux A. Tonkin K. et al. (2011) Olaparib in patients with recurrent high-grade serous or poorly differentiated ovarian carcinoma or triple-negative breast cancer: a phase 2, multicentre, open-label, non-randomised study. Lancet Oncol 12: 852–861.
19. Gordon A. Fleagle J. Guthrie D. Parkin D. Gore M. Lacave A. (2001) Recurrent epithelial ovarian carcinoma: a randomized phase III study of pegylated liposomal doxorubicin versus topotecan. J Clin Oncol 19: 3312–3322.
20. Gore M. Fryatt I. Wiltshaw E. Dawson T. (1990) Treatment of relapsed carcinoma of the ovary with cisplatin or carboplatin following initial treatment with these compounds. Gynecol Oncol 36: 207–211.
21. Gotlieb W. Amant F. Advani S. Goswami C. Hirte H. Provencher D. et al. (2012) Intravenous aflibercept for treatment of recurrent symptomatic malignant ascites in patients with advanced ovarian cancer: a phase 2, randomised, double-blind, placebo-controlled study. Lancet Oncol 13: 154–62.
22. Han Y. Huang H. Xiao Z. Zhang W. Cao Y. Qu L. et al. (2012) Integrated analysis of gene expression profiles associated with response of platinum/paclitaxel-based treatment in epithelial ovarian cancer. PloS ONE 7: e52745.
23. Hanker L. Loibl S. Burchardi N. Pfisterer J. Meier W. Pujade-Lauraine E. et al. (2012) The impact of second to sixth line therapy on survival of relapsed ovarian cancer after primary taxane/platinum-based therapy. Ann Oncol 23: 2605–2612.
24. Harter P. Hahmann M. Lueck H. Poelcher M. Wimberger P. Ortmann O. et al. (2009) Surgery for recurrent ovarian cancer: role of peritoneal carcinomatosis: exploratory analysis of the desktop I trial about risk factors, surgical implications, and prognostic value of peritoneal carcinomatosis. Ann Surg Oncol 16: 1324–1330.
25. Horowitz N. Hua J. Gibb R. Mutch D. Herzog T. (2004) The role of topotecan for extending the platinum-free interval in recurrent ovarian cancer: an in vitro model. Gynecol Oncol 94: 67–73.
26. Katsumata N. Yasuda M. Isonishi S. Takahashi F. Michimae H. Kimura E. et al. (2013) Long-term results of dose-dense paclitaxel and carboplatin versus conventional paclitaxel and carboplatin for treatment of advanced epithelial ovarian, fallopian tube, or primary peritoneal cancer (JGOG 3016): a randomised, controlled, open-label trial. Lancet Oncol 14: 1020–1026.
27. Kavanagh J. Tresukosol D. Edwards C. Freedman R. Gonzalez de Leon C. Fishman A. et al. (1995) Carboplatin reinduction after taxane in patients with platinum-refractory epithelial ovarian cancer. J Clin Oncol 13: 1584–1588.
28. Kaye S. Colombo N. Monk B. Tjulandin S. Kong B. Roy M. et al. (2011) Trabectedin plus pegylated liposomal doxorubicin in relapsed ovarian cancer delays third-line chemotherapy and prolongs the platinum-free interval. Ann Oncol 22: 49–58.
29. Kerbel R. Kamen B. (2004) The anti-angiogenic basis of metronomic chemotherapy. Nat Rev Cancer 4: 423–436.
30. Ledermann J. Harter P. Gourley C. Friedlander M. Vergote I. Rustin G. et al. (2012) Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med 366: 1382–1392.
31. Ledermann J. Harter P. Gourley C. Friedlander M. Vergote I. Rustin G. et al. (2014) Olaparib maintenance therapy in patients with platinum sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of a randomised phase 2 trial. Lancet Oncol 15: 852–861.
32. Ledermann J. Perren T. Raja F. Embleton A. Rustin G. Jayson G. et al. (2013 a) Randomised double-blind phase III trial of cediranib (AZD 2171) in relapsed platinum sensitive ovarian cancer: results of the ICON 6 Trial. European Cancer Congress E J Cancer (Suppl. 3): LBA10S5.
33. Ledermann J. Raja F. Fotopoulou C. Gonzalez-Martin A. Colombo N. Sessa C. et al. (2013 b) Newly diagnosed and relapsed epithelial ovarian carcinoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 24(Suppl. 6): vi24–vi32
34. Markman M. (1998) ‘Recurrence within 6 months of platinum therapy’: an adequate definition of ‘platinum-refractory’ ovarian cancer? Gynecol Oncol 69: 91–92.
35. Markman M. Rothman R. Hakes T. Reichman B. Hoskins W. Rubin S. et al. (1991) Second-line platinum therapy in patients with ovarian cancer previously treated with cisplatin. J Clin Oncol 9: 389–393.
36. Martin L. Hamilton T. Schilder R. (2008) Platinum resistance: the role of DNA repair pathways. Clin Cancer Res 14: 1291–1295.
37. McCann G. Smith B. Backes F. Rath K. Chacko S. Salani R. et al. (2012) Recurrent ovarian cancer: is there a role for re-treatment with bevacizumab after an initial complete response to a bevacizumab-containing regimen? Gynecol Oncol 127: 362–366.
38. Meier W. Du Bois A. Reuss A. Kuhn W. Olbricht S. Gropp M. et al. (2009) Topotecan versus treosulfan, an alkylating agent, in patients with epithelial ovarian cancer and relapse within 12 months following 1st-line platinum / paclitaxel chemotherapy. A prospectively randomized phase III trial by the Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group (AGO-OVAR). Gynecol Oncol 114: 199–205.
39. Monk B. Herzog T. Kaye S. Krasner C. Vermorken J. Muggia F. et al. (2010) Trabectedin plus pegylated liposomal doxorubicin in recurrent ovarian cancer. J Clin Oncol 28: 3107–3114.
40. Monk B. Poveda A. Vergote I. Raspagliesi F. Fujiwara K. Bae D. et al. (2013) A phase III, randomized, double-blind trial of weekly paclitaxel plus the angiopoeitin 1 and 2 inhibitor, trebananib, or placebo in women with recurrent ovarian cancer: Trinova-1. European Cancer Congress. E J Cancer 49(Suppl. 3): LBA41S18.
41. Morgan R. Jr Alvarez R. Armstrong D. Burger R. Chen L. Copeland L. et al. (2013) Ovarian cancer, version 2.2013. J Natl Compr Canc Netw 11: 1199–1209.
42. Mutch D. Orlando M. Goss T. Teneriello M. Gordon A. McMeekin S. et al. (2007) Randomized phase III trial of gemcitabine compared with pegylated liposomal doxorubicin in patients with platinum-resistant ovarian cancer. J Clin Oncol 25: 2811–2818.
43. Naumann R. Coleman R. Burger R. Sausville E. Kutarska E. Ghamande S. et al. (2013) Precedent: a randomized phase II trial comparing vintafolide (EC145) and pegylated liposomal doxorubicin (PLD) in combination versus PLD alone in patients with platinum-resistant ovarian cancer. J Clin Oncol 31: 4400–4406.
44. Parmar M. Ledermann J. Colombo N. Du Bois A. Delaloye J. Kristensen G. et al. (2003) Paclitaxel plus platinum-based chemotherapy versus conventional platinum-based chemotherapy in women with relapsed ovarian cancer: the ICON4/AGO-OVAR-2.2 Trial. Lancet 361: 2099–2106.
45. Pfisterer J. Plante M. Vergote I. Du Bois A. Hirte H. Lacave A. et al. (2006) Gemcitabine plus carboplatin compared with carboplatin in patients with platinum-sensitive recurrent ovarian cancer: an intergroup trial of the AGO-OVAR, the NCIC CTG, and the EORTC GCG. J Clin Oncol 24: 4699–4707.
46. Piccart M. Green J. Lacave A. Reed N. Vergote I. Benedetti-Panici P. et al. (2000) Oxaliplatin or paclitaxel in patients with platinum-pretreated advanced ovarian cancer: a randomized phase II study of the European Organization for Research and Treatment of Cancer Gynecology Group. J Clin Oncol 18: 1193–1202.
47. Pinato D. Graham J. Gabra H. Sharma R. (2013) Evolving concepts in the management of drug resistant ovarian cancer: dose dense chemotherapy and the reversal of clinical platinum resistance. Cancer Treat Rev 39: 153–160.
48. Pujade-Lauraine E. Hilpert F. Weber B. Reuss A. Poveda A. Kristensen G. et al. (2014) Bevacizumab combined with chemotherapy for platinum-resistant recurrent ovarian cancer: the AURELIA open-label randomized phase III trial. J Clin Oncol 32: 1302–8.
49. Pujade-Lauraine E. Wagner U. Aavall-Lundqvist E. Gebski V. Heywood M. Vasey P. et al. (2010) Pegylated liposomal doxorubicin and carboplatin compared with paclitaxel and carboplatin for patients with platinum-sensitive ovarian cancer in late relapse. J Clin Oncol 28: 3323–3329.
50. Raja F. Counsell N. Colombo N. Pfisterer J. Du Bois A. Parmar M. et al. (2013) Platinum versus platinum-combination chemotherapy in platinum-sensitive recurrent ovarian cancer: a meta-analysis using individual patient data. Ann Oncol 24: 3028–3034.
51. Rose P. Mossbruger K. Fusco N. Smrekar M. Eaton S. Rodriguez M. (2003) Gemcitabine reverses cisplatin resistance: demonstration of activity in platinum- and multidrug-resistant ovarian and peritoneal carcinoma. Gynecol Oncol 88: 17–21.
52. Rosenberg P. Andersson H. Boman K. Ridderheim M. Sorbe B. Puistola U. et al. (2002) Randomized trial of single agent paclitaxel given weekly versus every three weeks and with peroral versus intravenous steroid premedication to patients with ovarian cancer previously treated with platinum. Acta Oncol 41: 418–424.
53. Rustin G. Reed N. Jayson G. Ledermann J. Adams M. Perren T. et al. (2011) A phase II trial evaluating two schedules of sagopilone (ZK-EPO), a novel epothilone, in patients with platinum-resistant ovarian cancer. Ann Oncol 22: 2411–2416.
54. Rustin G. van der Burg MEL. Griffin CL. Guthrie D. Lamont A. Jayson GC. et al. (2010) Early versus delayed treatment of relapsed ovarian cancer (MRC OV05/EORTC 55955): a randomised trial. Lancet 376: 1155–63.
55. Rustin G. Vergote I. Eisenhauer E. Pujade-Lauraine E. Quinn M. Thigpen T. et al. (2011) Definitions for response and progression in ovarian cancer clinical trials incorporating RECIST 1.1 and CA 125 agreed by the Gynecological Cancer Intergroup (GCIG). Int J Gynecol Cancer 21: 419–423.
56. Sharma R. Graham J. Mitchell H. Brooks A. Blagden S. Gabra H. (2009) Extended weekly dose-dense paclitaxel / carboplatin is feasible and active in heavily pre-treated platinum-resistant recurrent ovarian cancer. Br J Cancer 100: 707–712.
57. Stockler M. Hilpert F. Friedlander M. King M. Wenzel L. Lee C. et al. (2013) Health-related quality of life (HRQOL) results from the Aurelia Trial Evaluating Bevacizumab (BEV) plus chemotherapy (CT) for platinum-resistant recurrent ovarian cancer (OC). J Clin Oncol 31(Suppl.): abstract 5542.
58. Stuart G. Kitchener H. Bacon M. Dubois A. Friedlander M. Ledermann J. et al. (2011) 2010 Gynecologic Cancer Intergroup (GCIG) consensus statement on clinical trials in ovarian cancer: report from the Fourth Ovarian Cancer Consensus Conference. Int J Gynecol Cancer 21: 750–755.
59. Tanguay J. Ansari J. Buckley L. Fernando I. (2009) Epithelial ovarian cancer: role of pegylated liposomal doxorubicin in prolonging the platinum-free interval and cancer antigen 125 trends during treatment. Int J Gynecol Cancer 19: 361–366.
60. Ten Bokkel Huinink W. Gore M. Carmichael J. Gordon A. Malfetano J. Hudson I. et al. (1997) Topotecan versus paclitaxel for the treatment of recurrent epithelial ovarian cancer. J Clin Oncol 15: 2183–2193.
61. Trent Cancer Registry (2012) Overview of Ovarian Cancer in England: incidence, Mortality and Survival. www.ncin.org.uk
62. van der Burg M. de Wit R. van Putten W. Logmans A. Kruit W. Stoter G. et al. (2002) Weekly cisplatin and daily oral etoposide is highly effective in platinum pretreated ovarian cancer. Br J Cancer 86: 19–25.
63. Vergote I. Calvert H. Kania M. Kaiser C. Zimmermann A. Sehouli J. (2009) A randomised, double-blind, phase II study of two doses of pemetrexed in the treatment of platinum-resistant, epithelial ovarian or primary peritoneal cancer. Eur J Cancer 45: 1415–1423.
64. Verhaak R. Tamayo P. Yang J. Hubbard D. Zhang H. Creighton C. et al. (2013) Prognostically relevant gene signatures of high-grade serous ovarian carcinoma. J Clin Invest 123: 517–525.
65. Wagner U. Marth C. Largillier R. Kaern J. Brown C. Heywood M. et al. (2012) Final overall survival results of phase III GCIG CALYPSO trial of pegylated liposomal doxorubicin and carboplatin vs paclitaxel and carboplatin in platinum-sensitive ovarian cancer patients. Br J Cancer 107: 588–591.
66. Yap T. Sandhu S. Carden C. de Bono J. (2011) Poly(ADP-ribose) polymerase (PARP) inhibitors: exploiting a synthetic lethal strategy in the clinic. CA Cancer J Clin 61: 31–49.
67. Zang R. Harter P. Chi D. Sehouli J. Jiang R. Trope C. et al. (2011) Predictors of survival in patients with recurrent ovarian cancer undergoing secondary cytoreductive surgery based on the pooled analysis of an international collaborative cohort. Br J Cancer 105: 890–896.