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Meta-Analysis
. 2022 Sep 26;9(9):CD015048.
doi: 10.1002/14651858.CD015048.pub2.

Impact of residual disease as a prognostic factor for survival in women with advanced epithelial ovarian cancer after primary surgery

Andrew Bryant  1 , Shaun Hiu  1 , Patience T Kunonga  1 , Ketankumar Gajjar  2 , Dawn Craig  1 , Luke Vale  1 , Brett A Winter-Roach  3 , Ahmed Elattar  4 , Raj Naik  5
Affiliations
Meta-Analysis

Impact of residual disease as a prognostic factor for survival in women with advanced epithelial ovarian cancer after primary surgery

Andrew Bryant et al. Cochrane Database Syst Rev. .

Abstract

Background: Ovarian cancer is the seventh most common cancer among women and a leading cause of death from gynaecological malignancies. Epithelial ovarian cancer is the most common type, accounting for around 90% of all ovarian cancers. This specific type of ovarian cancer starts in the surface layer covering the ovary or lining of the fallopian tube. Surgery is performed either before chemotherapy (upfront or primary debulking surgery (PDS)) or in the middle of a course of treatment with chemotherapy (neoadjuvant chemotherapy (NACT) and interval debulking surgery (IDS)), with the aim of removing all visible tumour and achieving no macroscopic residual disease (NMRD). The aim of this review is to investigate the prognostic impact of size of residual disease nodules (RD) in women who received upfront or interval cytoreductive surgery for advanced (stage III and IV) epithelial ovarian cancer (EOC).

Objectives: To assess the prognostic impact of residual disease after primary surgery on survival outcomes for advanced (stage III and IV) epithelial ovarian cancer. In separate analyses, primary surgery included both upfront primary debulking surgery (PDS) followed by adjuvant chemotherapy and neoadjuvant chemotherapy followed by interval debulking surgery (IDS). Each residual disease threshold is considered as a separate prognostic factor.

Search methods: We searched CENTRAL (2021, Issue 8), MEDLINE via Ovid (to 30 August 2021) and Embase via Ovid (to 30 August 2021).

Selection criteria: We included survival data from studies of at least 100 women with advanced EOC after primary surgery. Residual disease was assessed as a prognostic factor in multivariate prognostic models. We excluded studies that reported fewer than 100 women, women with concurrent malignancies or studies that only reported unadjusted results. Women were included into two distinct groups: those who received PDS followed by platinum-based chemotherapy and those who received IDS, analysed separately. We included studies that reported all RD thresholds after surgery, but the main thresholds of interest were microscopic RD (labelled NMRD), RD 0.1 cm to 1 cm (small-volume residual disease (SVRD)) and RD > 1 cm (large-volume residual disease (LVRD)).

Data collection and analysis: Two review authors independently abstracted data and assessed risk of bias. Where possible, we synthesised the data in meta-analysis. To assess the adequacy of adjustment factors used in multivariate Cox models, we used the 'adjustment for other prognostic factors' and 'statistical analysis and reporting' domains of the quality in prognosis studies (QUIPS) tool. We also made judgements about the certainty of the evidence for each outcome in the main comparisons, using GRADE. We examined differences between FIGO stages III and IV for different thresholds of RD after primary surgery. We considered factors such as age, grade, length of follow-up, type and experience of surgeon, and type of surgery in the interpretation of any heterogeneity. We also performed sensitivity analyses that distinguished between studies that included NMRD in RD categories of < 1 cm and those that did not. This was applicable to comparisons involving RD < 1 cm with the exception of RD < 1 cm versus NMRD. We evaluated women undergoing PDS and IDS in separate analyses.

Main results: We found 46 studies reporting multivariate prognostic analyses, including RD as a prognostic factor, which met our inclusion criteria: 22,376 women who underwent PDS and 3697 who underwent IDS, all with varying levels of RD. While we identified a range of different RD thresholds, we mainly report on comparisons that are the focus of a key area of clinical uncertainty (involving NMRD, SVRD and LVRD). The comparison involving any visible disease (RD > 0 cm) and NMRD was also important. SVRD versus NMRD in a PDS setting In PDS studies, most showed an increased risk of death in all RD groups when those with macroscopic RD (MRD) were compared to NMRD. Women who had SVRD after PDS had more than twice the risk of death compared to women with NMRD (hazard ratio (HR) 2.03, 95% confidence interval (CI) 1.80 to 2.29; I2 = 50%; 17 studies; 9404 participants; moderate-certainty). The analysis of progression-free survival found that women who had SVRD after PDS had nearly twice the risk of death compared to women with NMRD (HR 1.88, 95% CI 1.63 to 2.16; I2 = 63%; 10 studies; 6596 participants; moderate-certainty). LVRD versus SVRD in a PDS setting When we compared LVRD versus SVRD following surgery, the estimates were attenuated compared to NMRD comparisons. All analyses showed an overall survival benefit in women who had RD < 1 cm after surgery (HR 1.22, 95% CI 1.13 to 1.32; I2 = 0%; 5 studies; 6000 participants; moderate-certainty). The results were robust to analyses of progression-free survival. SVRD and LVRD versus NMRD in an IDS setting The one study that defined the categories as NMRD, SVRD and LVRD showed that women who had SVRD and LVRD after IDS had more than twice the risk of death compared to women who had NMRD (HR 2.09, 95% CI 1.20 to 3.66; 310 participants; I2 = 56%, and HR 2.23, 95% CI 1.49 to 3.34; 343 participants; I2 = 35%; very low-certainty, for SVRD versus NMRD and LVRD versus NMRD, respectively). LVRD versus SVRD + NMRD in an IDS setting Meta-analysis found that women who had LVRD had a greater risk of death and disease progression compared to women who had either SVRD or NMRD (HR 1.60, 95% CI 1.21 to 2.11; 6 studies; 1572 participants; I2 = 58% for overall survival and HR 1.76, 95% CI 1.23 to 2.52; 1145 participants; I2 = 60% for progression-free survival; very low-certainty). However, this result is biased as in all but one study it was not possible to distinguish NMRD within the < 1 cm thresholds. Only one study separated NMRD from SVRD; all others included NMRD in the SVRD group, which may create bias when comparing with LVRD, making interpretation challenging. MRD versus NMRD in an IDS setting Women who had any amount of MRD after IDS had more than twice the risk of death compared to women with NMRD (HR 2.11, 95% CI 1.35 to 3.29, I2 = 81%; 906 participants; very low-certainty).

Authors' conclusions: In a PDS setting, there is moderate-certainty evidence that the amount of RD after primary surgery is a prognostic factor for overall and progression-free survival in women with advanced ovarian cancer. We separated our analysis into three distinct categories for the survival outcome including NMRD, SVRD and LVRD. After IDS, there may be only two categories required, although this is based on very low-certainty evidence, as all but one study included NMRD in the SVRD category. The one study that separated NMRD from SVRD showed no improved survival outcome in the SVRD category, compared to LVRD. Further low-certainty evidence also supported restricting to two categories, where women who had any amount of MRD after IDS had a significantly greater risk of death compared to women with NMRD. Therefore, the evidence presented in this review cannot conclude that using three categories applies in an IDS setting (very low-certainty evidence), as was supported for PDS (which has convincing moderate-certainty evidence).

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Conflict of interest statement

  1. Andrew Bryant: none known

  2. Ahmed Elattar: none known

  3. Patience Kunonga: none known

  4. Brett A Winter‐Roach: none known

  5. Shaun Hiu: none known

  6. Dawn Craig: none known

  7. Luke Vale: none known

  8. Ketankumar Gajjar: none known

  9. Raj Naik: none known

Figures

1
1
Study flow diagram.
2
2
Funnel plot of comparison: 1 SVRD (< 1 cm) versus NMRD, outcome: 1.2 Overall survival
3
3
Funnel plot of comparison: 4 LVRD (> 1 cm) versus NMRD, outcome: 2.2 Overall survival
4
4
Funnel plot of comparison: 1 SVRD (< 1 cm) versus NMRD, outcome: 1.5 Progression‐free survival
1.1
1.1. Analysis
Comparison 1: PDS: SVRD (< 1 cm) versus NMRD, Outcome 1: Overall survival
1.2
1.2. Analysis
Comparison 1: PDS: SVRD (< 1 cm) versus NMRD, Outcome 2: Overall survival ‐ sensitivity analysis using fixed‐effect model
1.3
1.3. Analysis
Comparison 1: PDS: SVRD (< 1 cm) versus NMRD, Outcome 3: Overall survival ‐ sensitivity analysis excluding Klar 2016
1.4
1.4. Analysis
Comparison 1: PDS: SVRD (< 1 cm) versus NMRD, Outcome 4: Progression‐free survival
1.5
1.5. Analysis
Comparison 1: PDS: SVRD (< 1 cm) versus NMRD, Outcome 5: Progression‐free survival ‐ sensitivity analysis using fixed‐effect model
1.6
1.6. Analysis
Comparison 1: PDS: SVRD (< 1 cm) versus NMRD, Outcome 6: Progression‐free survival ‐ sensitivity analysis excluding Klar 2016
2.1
2.1. Analysis
Comparison 2: PDS: LVRD (> 1 cm) versus NMRD, Outcome 1: Overall survival
2.2
2.2. Analysis
Comparison 2: PDS: LVRD (> 1 cm) versus NMRD, Outcome 2: Overall survival ‐ sensitivity analysis using fixed effects model
2.3
2.3. Analysis
Comparison 2: PDS: LVRD (> 1 cm) versus NMRD, Outcome 3: Overall survival ‐ sensitivity analysis excluding Melamed 2017b and Winter 2007
2.4
2.4. Analysis
Comparison 2: PDS: LVRD (> 1 cm) versus NMRD, Outcome 4: Progression‐free survival
3.1
3.1. Analysis
Comparison 3: PDS: LVRD (> 1 cm) versus SVRD (< 1 cm), Outcome 1: Overall survival
3.2
3.2. Analysis
Comparison 3: PDS: LVRD (> 1 cm) versus SVRD (< 1 cm), Outcome 2: Overall survival sensitivity analysis excluding Klar 2016
3.3
3.3. Analysis
Comparison 3: PDS: LVRD (> 1 cm) versus SVRD (< 1 cm), Outcome 3: Overall survival sensitivity analysis excluding 0 cm
3.4
3.4. Analysis
Comparison 3: PDS: LVRD (> 1 cm) versus SVRD (< 1 cm), Outcome 4: Overall survival sensitivity analysis including studies that included 0 cm
3.5
3.5. Analysis
Comparison 3: PDS: LVRD (> 1 cm) versus SVRD (< 1 cm), Outcome 5: Progression‐free survival
4.1
4.1. Analysis
Comparison 4: PDS: RD > 0 cm versus NMRD, Outcome 1: Overall survival
4.2
4.2. Analysis
Comparison 4: PDS: RD > 0 cm versus NMRD, Outcome 2: Progression‐free survival
5.1
5.1. Analysis
Comparison 5: PDS: LVRD 1 cm to 2 cm versus NMRD (stage IIIC), Outcome 1: Overall survival
6.1
6.1. Analysis
Comparison 6: PDS: LVRD (> 2 cm) versus NMRD (stage IIIC), Outcome 1: Overall survival
7.1
7.1. Analysis
Comparison 7: PDS: LVRD 1 cm to 5 cm versus NMRD (stage IV disease), Outcome 1: Overall survival
7.2
7.2. Analysis
Comparison 7: PDS: LVRD 1 cm to 5 cm versus NMRD (stage IV disease), Outcome 2: Progression‐free survival
8.1
8.1. Analysis
Comparison 8: PDS: LVRD (> 5 cm) versus NMRD (stage IV disease), Outcome 1: Overall survival
8.2
8.2. Analysis
Comparison 8: PDS: LVRD (> 5 cm) versus NMRD (stage IV disease), Outcome 2: Progression‐free survival
9.1
9.1. Analysis
Comparison 9: PDS: LVRD 1 cm to 2 cm versus SVRD (< 1 cm), Outcome 1: Overall survival
10.1
10.1. Analysis
Comparison 10: PDS: LVRD (> 2 cm) versus SVRD (< 1 cm), Outcome 1: Overall survival
11.1
11.1. Analysis
Comparison 11: PDS: LVRD (> 2 cm) versus RD < 2 cm (stage IV disease), Outcome 1: Overall survival
11.2
11.2. Analysis
Comparison 11: PDS: LVRD (> 2 cm) versus RD < 2 cm (stage IV disease), Outcome 2: Progression‐free survival
12.1
12.1. Analysis
Comparison 12: IDS: SVRD (< 1 cm) versus NMRD, Outcome 1: Overall survival
12.2
12.2. Analysis
Comparison 12: IDS: SVRD (< 1 cm) versus NMRD, Outcome 2: Progression‐free survival
13.1
13.1. Analysis
Comparison 13: IDS: LVRD (> 1 cm) versus NMRD, Outcome 1: Overall survival
14.1
14.1. Analysis
Comparison 14: IDS: LVRD (> 1 cm) versus SVRD (< 1 cm), Outcome 1: Overall survival
14.2
14.2. Analysis
Comparison 14: IDS: LVRD (> 1 cm) versus SVRD (< 1 cm), Outcome 2: Overall survival sensitivity analysis including 0 cm
14.3
14.3. Analysis
Comparison 14: IDS: LVRD (> 1 cm) versus SVRD (< 1 cm), Outcome 3: Overall survival sensitivity analysis excluding Phillips 2018
14.4
14.4. Analysis
Comparison 14: IDS: LVRD (> 1 cm) versus SVRD (< 1 cm), Outcome 4: Progression‐free survival
15.1
15.1. Analysis
Comparison 15: IDS: RD > 0 cm versus NMRD, Outcome 1: Overall survival
15.2
15.2. Analysis
Comparison 15: IDS: RD > 0 cm versus NMRD, Outcome 2: Progression‐free survival
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Wimberger 2010 {published data only}
    1. Wimberger P, Wehling M, Lehmann N, Kimmig R, Schmalfeldt B, Burges A. Influence of residual tumor on outcome in ovarian cancer patients with FIGO stage IV disease: an exploratory analysis of the AGO-OVAR (Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group). Annals of Surgical Oncology 2010;17(6):1642-8. - PubMed
Winter 2007 {published data only}
    1. Armstrong DK, Bundy BW, Wenzel L, Huang HQ, Baergen RL, Shashikant L, et al, the Gynecologic Oncology Group. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. New England Journal of Medicine 2006;354(1):34-43. - PubMed
    1. Markman M, Bundy BM, Alberts DS, Fowler JM, Clark-Pearson DL, Carson LF, et al. Phase III trial of standard-dose intravenous cisplatin plus paclitaxel versus moderately high-dose carboplatin followed by intravenous paclitaxel and intraperitoneal cisplatin in small-volume stage III ovarian carcinoma: An Intergroup Study of the Gynecologic Oncology Group, Southwestern Oncology Group, and Eastern Cooperative Oncology Group. Journal of Clinical Oncology 2001;19(4):1001-7. - PubMed
    1. McGuire WP, Hoskins WJ, Brady MF, Kucera PR, Partridge EE, Look KY, et al. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. New England Journal of Medicine 1996;334(1):1-6. - PubMed
    1. Muggia FM, Braly PS, Brady MF, Sutton GN, Theodore HL, Samuel LA, et al. Phase III randomized study of cisplatin versus paclitaxel versus cisplatin and paclitaxel in patients with suboptimal stage III or IV ovarian cancer: a Gynecologic Oncology Group Study. Journal of Clinical Oncology 2000;18(1):106-15. - PubMed
    1. Ozols RF, Bundy BN, Greer BE, Fowler JM, Clarke-Pearson DB, Robert AM, et al. Phase III trial of carboplatin and paclitaxel compared with cisplatin and paclitaxel in patients with optimally Resected stage III ovarian cancer: a Gynecologic Oncology Group Study. Journal of Clinical Oncology 2003;21(17):3194-200. - PubMed
Winter 2008 {published data only}
    1. McGuire WP, Hoskins WJ, Brady MF, Kucera PR, Partridge EE, Look KY, et al. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. New England Journal of Medicine 1996;334(1):1-6. - PubMed
    1. Muggia FM, Braly PS, Brady MF, Sutton G, Niemann HL, Lentz SL, et al. Phase III randomized study of cisplatin versus paclitaxel versus cisplatin and paclitaxel in patients with suboptimal stage III or IV ovarian cancer: a Gynecologic Oncology Group Study. Journal of Clinical Oncology 2000;18(1):106-15. - PubMed
    1. Rose PG, Nerenstone S, Brady MF, Clarke-Pearson D, Olt G, Rubin SC, et al. Secondary surgical cytoreduction for advanced ovarian carcinoma. New England Journal of Medicine 2004;351(24):2489-97. - PubMed
    1. Spriggs DR, Brady MF, Vaccarello L, Clarke-Pearson DL, Burger RA, Mannel R, et al. Phase III randomized trial of intravenous cisplatin plus a 24- or 96-hour infusion of paclitaxel in epithelial ovarian cancer: a Gynecologic Oncology Group Study. Journal of Clinical Oncology 2007;25(28):4466-71. - PubMed
    1. Winter WE, Maxwell GL, Tian C, Sundborg MJ, Rose GS, Rose PG, et al. Tumor residual after surgical cytoreduction in prediction of clinical outcome in stage IV epithelial ovarian cancer: a Gynecologic Oncology Group Study. Journal of Clinical Oncology 2008;26(1):83-9. - PubMed
Zhang 2018 {published data only}
    1. Zhang J, Ning L, Zhang A, Xiangxiang B. Potential risk factors associated with prognosis of neoadjuvant chemotherapy followed by interval debulking surgery in stage IIIc-IV high-grade serous ovarian carcinoma patients. Journal of Obstetrics and Gynaecology Research 2018;44(9):1808-16. - PubMed
Zhu 2016 {published data only}
    1. Zhu J, Wang H, Cheng-Cheng L, Lu Y, Tang H. The Glasgow Prognostic Score (GPS) is a novel prognostic indicator in advanced epithelial ovarian cancer: a multicenter retrospective study. Journal of Cancer Research and Clinical Oncology 2016;142(11):2339-45. - PMC - PubMed

References to studies excluded from this review

Alberts 1993 {published data only}
    1. Alberts DS, Dahlberg S, Green SJ, Garcia D, Hannigan EV, O'Toole R, et al. Analysis of patient age as an independent prognostic factor for survival in a phase III study of cisplatin-cyclophosphamide versus carboplatin-cyclophosphamide in stages III (suboptimal) and IV ovarian cancer. A Southwest Oncology Group study. Cancer 1993;71(2 Suppl):618-27. - PubMed
Alberts 1996 {published data only}
    1. Alberts DS, Liu PY, Hannigan EEV, O'Toole RW, Stephen DY, James AF, et al. Intraperitoneal cisplatin plus intravenous cyclophosphamide versus intravenous cisplatin plus intravenous cyclophosphamide for stage III ovarian cancer. New England Journal of Medicine 1996;335(26):1950-5. - PubMed
Alphs 2006 {published data only}
    1. Alphs HH, Zahurak ML, Bristow RE, Diaz-Montes TP. Predictors of surgical outcome and survival among elderly women diagnosed with ovarian and primary peritoneal cancer. Gynecologic Oncology 2006;103(3):1048-53. - PubMed
Altman 2012 {published data only}
    1. Altman AD, Nelson G, Chu P, Nation J, Ghatage P. Optimal debulking targets in women with advanced stage ovarian cancer: a retrospective study of immediate versus interval debulking surgery. Journal of Obstetrics and Gynaecology Canada 2012;34(6):558-66. - PubMed
Andersen Soegaard 2005 {published data only}
    1. Andersen ES, Knudsen A, Svarrer T, Lund B, Nielsen K, Grove A, et al. The results of treatment of epithelial ovarian cancer after centralisation of primary surgery. Results from North Jutland, Denmark. Gynecologic Oncology 2005;99(3):552-6. - PubMed
Anuradha 2016 {published data only}
    1. Anuradha S, Donovan PJ, Webb PM, Brand AH, Goh J, Friedlander M, et al. Variations in adjuvant chemotherapy and survival in women with epithelial ovarian cancer–a population-based study. Acta Oncologica 2016;55(2):226-33. - PubMed
Bailey 2006 {published data only}
    1. Bailey J, Murdoch J, Anderson R, Weeks J, Foy C. Stage III and IV ovarian cancer in the South West of England: five-year outcome analysis for cases treated in 1998. International Journal of Gynecological Cancer 2006;1:25-9. - PubMed
Baker 1994 {published data only}
    1. Baker TR, Piver MS, Hempling RE. Long term survival by cytoreductive surgery to less than 1 cm, induction weekly cisplatin and monthly cisplatin, doxorubicin, and cyclophosphamide therapy in advanced ovarian adenocarcinoma. Cancer 1994;74(2):656-63. - PubMed
Barda 2004 {published data only}
    1. Barda G, Menczer J, Chetrit A, Lubin F, Beck D, Piura B, et al. Comparison between primary peritoneal and epithelial ovarian carcinoma: a population-based study. American Journal of Obstetrics and Gynecology 2004;190(4):1039-45. - PubMed
Benedetti‐Panici 1996 {published data only}
    1. Benedetti-Panici P, Maneschi F, Scambia G, Cutillo G, Greggi S, Mancuso S. The pelvic retroperitoneal approach in the treatment of advanced ovarian carcinoma. Obstetrics & Gynecology 1996;87(4):532-8. - PubMed
Bertelsen 1990 {published data only}
    1. Bertelsen K. Tumor reduction surgery and long-term survival in advanced ovarian cancer: a DACOVA study. Gynecologic Oncology 1990;38(2):203-9. - PubMed
Bertelsen 1993 {published data only}
    1. Bertelsen K, Jakobsen A, Strøyer J, Nielsen K, Sandberg E, Andersen JE, et al. A prospective randomized comparison of 6 and 12 cycles of cyclophosphamide, adriamycin, and cisplatin in advanced epithelial ovarian cancer: a Danish Ovarian Study Group Trial (DACOVA). Gynecologic Oncology 1993;49:30-6. - PubMed
Bian 2016 {published data only}
    1. Bian C, Yao K, Li L, Yi T, Zhao X. Primary debulking surgery vs. neoadjuvant chemotherapy followed by interval debulking surgery for patients with advanced ovarian cancer. Archives of Gynecology and Obstetrics 2016;293(1):163-8. - PubMed
Bonnefoi 1999 {published data only}
    1. Bonnefoi H, A'Hern RP, Fisher C, Macfarlane V, Barton D, Blake P, et al. Natural history of stage IV epithelial ovarian cancer [see comment]. Journal of Clinical Oncology 1999;17(3):767-75. - PubMed
Brinkhuis 1996a {published data only}
    1. Brinkhuis M, Baak JPA, Van Diest PJ, Lund B, Wils J. In Dutch and Danish patients with FIGO III ovarian carcinoma, geographic survival differences are associated with differences in quantitative pathologic features. International Journal of Gynecological Cancer 1996;6(2):108-14.
Brinkhuis 1996b {published data only}
    1. Brinkhuis M, Lund B, Meijer GA, Baak JPA. Quantitative pathological variables as prognostic factors for overall survival in Danish patients with FIGO stage III ovarian cancer. International Journal of Gynecological Cancer 1996;6(3):168-74.
Bristow 1999 {published data only}
    1. Bristow RE, Montz FJ, Lagasse LD, Leuchter RS, Karlan BY. Survival impact of surgical cytoreduction in stage IV epithelial ovarian cancer. Gynecologic Oncology 1999;72(3):278-87. - PubMed
Cai 2007 {published data only}
    1. Cai HB, Zhou YF, Chen HZ, Hou HY. The role of bowel surgery with cytoreduction for epithelial ovarian cancer. Clinical Oncology 2007;19(10):757-62. - PubMed
Ceresoli 2018 {published data only}
    1. Ceresoli M, Verrengia A, Montori G, Busci L, Coccolini F, Ansaloni L, et al. Effect of cytoreductive surgery and hyperthermic intraperitoneal chemotherapy on relapse pattern in primary epithelial ovarian cancer: a propensity score based case-control study. Journal of Gynecologic Oncology 2018;29(3):e53. - PMC - PubMed
Chekman 2015 {published data only}
    1. Chekman C, Layoune R, Hocine O, Raissi N, Ferhat HA, Ali Khodja H, et al. An open prospective randomized trial comparing primary complete cytoreduction surgery to debulking surgery after chemotherapy in advanced stage (FIGO's IIIC) ovarian carcinoma. In: 19th International Meeting of the European Society of Gynaecological Oncology, ESGO 2015; 2015 Oct 24-27; Nice, France. 2015:1316. [12185451]
Clamp 2018 {published data only}
    1. Clamp AR, McNeish IA, Dean A, Gallardo-Rincon D, Kim JW, O'Donnell DM, et al. Response to neoadjuvant chemotherapy in ICON8: a GCIG phase III randomised trial evaluating weekly dose-dense chemotherapy integration in first-line epithelial ovarian/fallopian tube/primary peritoneal carcinoma (EOC) treatment. In: Annals of Oncology. Vol. 29. 2018:viii336.
Colozza 1997 {published data only}
    1. Colozza M, Mosconi AM, Gori S, Belsanti V, Basurto C, De Angelis V, et al. Long-term results in patients with advanced epithelial ovarian carcinoma treated with a combination of cisplatin, doxorubicin, and cyclophosphamide. American Journal of Clinical Oncology 1997;20(5):522-6. - PubMed
Conte 1991 {published data only}
    1. Conte PF, Bruzzone M, Carnino F, Chiara S, Donadio M, Facchini V, et al. Carboplatin, doxorubicin, and cyclophosphamide versus cisplatin, doxorubicin, and cyclophosphamide: a randomized trial in stage III-IV epithelial ovarian carcinoma. Journal of Clinical Oncology 1991;9(4):658-63. - PubMed
Conte 1996 {published data only}
    1. Conte PF, Bruzzone M, Carnino F, Gadducci A, Algeri R, Bellini A, et al. High-dose versus low-dose cisplatin in combination with cyclophosphamide and epidoxorubicin in suboptimal ovarian cancer: a randomized study of the Gruppo Oncologico Nord-Ovest. Journal of Clinical Oncology 1996;14(2):351-6. - PubMed
Crawford 2005 {published data only}
    1. Crawford SC, Vasey PA, Paul J, Hay A, Davis JA, Kaye SB. Does aggressive surgery only benefit patients with less advanced ovarian cancer? Results from an international comparison within the SCOTROC-1 trial. Journal of Clinical Oncology 2005;23(34):8802-11. - PubMed
Creasman 1990 {published data only}
    1. Creasman WT, Omura GA, Brady MF, Yordan E, DiSaia PJ, Beecham J. A randomized trial of cyclophosphamide, doxorubicin, and cisplatin with or without bacillus Calmette-Guerin in patients with suboptimal stage III and IV ovarian cancer: a Gynecologic Oncology Group Study. Gynecologic Oncology 1990;39(3):239-43. - PubMed
Cummins 2019 {published data only}
    1. Cummins C, Hannah P, Long J, Kumar S, Sundar S, Bramley G. VP100 Ultraradical ovarian cancer surgery comparative clinical effectiveness. International Journal of Technology Assessment in Health Care 2019;35(S1):97.
Dao 2016 {published data only}
    1. Dao F, Schlappe BA, Tseng J, Lester J, Nick AM, Lutgendorf SK, et al. Characteristics of 10-year survivors of high-grade serous ovarian carcinoma. Gynecologic Oncology 2016;141:260-3. - PMC - PubMed
Del Campo 1994 {published data only}
    1. Del Campo JM, Felip E, Rubio D, Bermejo B, Colomer R, Zanon V. Long-term survival in advanced ovarian cancer after cytoreduction and chemotherapy treatment. Gynecologic Oncology 1994;53(1):27-32. - PubMed
de Oliviera 1990 {published data only}
    1. Oliveira CF, Lacave AJ, Villani C, Wolff JP, di Re F, Namer M, et al. Randomized comparison of cyclophosphamide, doxorubicin and cisplatin (CAP) versus cyclophosphamide and doxorubicin (CA) for the treatment of advanced ovarian cancer (ADOVCA). A EORTC Gynecological Cancer Cooperative Group Study. European Journal of Gynaecologic Oncology 1990;11(5):323-30. - PubMed
di Re 1996 {published data only}
    1. di Re F, Baiocchi G, Fontanelli R, Grosso G, Cobellis L, Raspagliesi F, et al. Systematic pelvic and paraaortic lymphadenectomy for advanced ovarian cancer: prognostic significance of node metastases. Gynecologic Oncology 1996;62(3):360-5. - PubMed
Elgamal 2019 {published data only}
    1. Elgamal M, Saha S, Cherry M, Saharan V, Buttar R, Wiese D, et al. Prognostic implications of lymph node metastasis in advanced ovarian cancer: analysis of the National Cancer Database 2006 to 2014. Journal of Clinical Oncology 2019;0:e17042.
Fagotti 2020 {published data only}
    1. Fagotti A, Ferrandina G, Vizzielli G, Fanfani F, Gallotta V, Chiantera V, et al. Phase III randomised clinical trial comparing primary surgery versus neoadjuvant chemotherapy in advanced epithelial ovarian cancer with high tumour load (SCORPION trial): final analysis of peri-operative outcome. European Journal of Cancer 2016;59:22-33. [12185453] - PubMed
    1. Fagotti A, Ferrandina MG, Vizzielli G, Pasciuto T, Fanfani F, Gallotta V, et al. Randomized trial of primary debulking surgery versus neoadjuvant chemotherapy for advanced epithelial ovarian cancer (SCORPION-NCT01461850). International Journal of Gynecological Cancer 2020;30(11):1657-64. [PMID: 10.1136/ijgc-2020- 001640] - PubMed
    1. Fagotti A, Vizzielli G, Ferrandina G, Fanfani F, Gallotta V, Chiantera V, et al. Survival analyses from a randomized trial of primary debulking surgery versus neoadjuvant chemotherapy for advanced epithelial ovarian cancer with high tumor load (SCORPION trial). Journal of Clinical Oncology 2018;36(15):5516. [12185454]
Gao 2001 {published data only}
    1. Gao J, Zheng A, Chen W, Peng Z, Cao Z. A study of prognostic factors of stage IV epithelial ovarian cancer [Chinese]. Journal of West China University of Medical Sciences 2001;32(2):309-12. - PubMed
Gasimli 2016 {published data only}
    1. Gasimli K, Braicu EI, Nassir M, Richter R, Babayeva A, Chekerov R, et al. Lymph node involvement pattern and survival differences of FIGO IIIC and FIGO IIIA1 ovarian cancer patients after primary complete tumor debulking surgery: a 10-year retrospective analysis of the tumor bank ovarian cancer network. Annals of Surgical Oncology 2016;23(4):1279-86. - PubMed
Geisler 2004 {published data only}
    1. Geisler JP, Tammela JE, Manahan KJ, Geisler HE, Miller GA, Zhou Z, et al. HSP27 in patients with ovarian carcinoma: still an independent prognostic indicator at 60 months follow-up. European Journal of Gynaecological Oncology 2004;25(2):165-8. - PubMed
Gershenson 1989 {published data only}
    1. Gershenson DM, Wharton J, Taylor C, Stringer LJ, Edwards CA, Creighton L, et al. Treatment of advanced epithelial ovarian cancer with cisplatin and cyclophosphamide. Gynecologic Oncology 1989;32(3):336-41. - PubMed
Gershenson 1992 {published data only}
    1. Gershenson DM, Mitchell MF, Atkinson N, Elvio G, Kavanagh J, Burke M, et al. The effect of prolonged cisplatin-based chemotherapy on progression-free survival in patients with optimal epithelial ovarian cancer: maintenance therapy reconsidered. Gynecologic Oncology 1992;47(1):7-13. - PubMed
Gershenson 1995 {published data only}
    1. Gershenson DM, Morris M, Burke TW, Levenback C, Kavanagh JJ, Fromm GL. Combined cisplatin and carboplatin chemotherapy for treatment of advanced epithelial ovarian cancer. Gynecologic Oncology 1995;58(3):349-55. - PubMed
Greggi 2016 {published data only}
    1. Greggi S, Falcone F, Carputo R, Raspagliesi F, Scaffa C, Laurelli G, et al. Primary surgical cytoreduction in advanced ovarian cancer: an outcome analysis within the MITO (Multicentre Italian Trials in Ovarian Cancer and Gynecologic Malignancies) Group. Gynecologic Oncology 2016;140(3):425-9. - PubMed
Grem 1991 {published data only}
    1. Grem J, O'Dwyer P, Elson P, Simon N, Trump D, Frontiera M, et al. Cisplatin, carboplatin, and cyclophosphamide combination chemotherapy in advanced-stage ovarian carcinoma: an Eastern Cooperative Oncology Group pilot study. Journal of Clinical Oncology 1989;9(10):1793-800. - PubMed
Hainsworth 1990 {published data only}
    1. Hainsworth JD, Burnett LS, Jones HW 3rd, Grosh WW, Johnson DH, Greco FA. High-dose cisplatin combination chemotherapy in the treatment of advanced epithelial ovarian carcinoma. Journal of Clinical Oncology 1990;8(3):502-8. - PubMed
Hakes 1992 {published data only}
    1. Hakes TB, Chalas E, Hoskins WJ, Jones WB, Markman M, Rubin SC, et al. Randomized prospective trial of 5 versus 10 cycles of cyclophosphamide, doxorubicin, and cisplatin in advanced ovarian carcinoma. Gynecologic Oncology 1992;45(3):284-9. - PubMed
Hamid 2002 {published data only}
    1. Hamid D, Rohr S, Baldauf JJ, Ritter J, Kurtz E, Dufour P, et al. Interest of intestinal resection for treatment of advanced ovarian carcinoma [Intérét des exéréses digestives dans le traitement des cancers écolués de l'ovaire]. Annales de Chirurgie 2002;127(1):40-7. - PubMed
Hardy 1991 {published data only}
    1. Hardy JR, Wiltshaw E, Blake PR, Harper P, Slevin M, Perren TJ, et al. Cisplatin and carboplatin in combination for the treatment of stage IV ovarian carcinoma. Annals of Oncology 1991;2(2):131-6. - PubMed
Heitz 2016 {published data only}
    1. Heitz F, Harter P, Alesina PF, Walz MK, Lorenz D, Groeben H, et al. Pattern of and reason for postoperative residual disease in patients with advanced ovarian cancer following upfront radical debulking surgery. Gynecologic Oncology 2016;141(2):264-70. - PubMed
Hoskins 1992 {published data only}
    1. Hoskins WJ, Bundy BN, Thigpen JT, Omura GA. The influence of cytoreductive surgery on recurrence-free interval and survival in small-volume stage III epithelial ovarian cancer: a Gynecologic Oncology Group study. Gynecologic Oncology 1992;47(2):159-66. - PubMed
Hoskins 1996 {published data only}
    1. Hoskins PJ, Swenerton KD, Pike JA, McMurtrie EM, Lee N. "MECCA": a developmental, dose-intensive, non-cross-resistant platinum-based chemotherapy for advanced ovarian cancer. Gynecologic Oncology 1996;63(3):345-51. - PubMed
Hoskins 1997 {published data only}
    1. Hoskins WJ, McGuire WP, Brady MF, Kucera PR, Partridge EE, Look KY, et al. Combination paclitaxel (Taxol(R))-cisplatin vs cyclophosphamide-cisplatin as primary therapy in patients with suboptimally debulked advanced ovarian cancer. International Journal of Gynecological Cancer 1997;7:9-13.
Itamochi 2002 {published data only}
    1. Itamochi H, Kigawa J, Sugiyama T, Kikuchi Y, Suzuki M, Terakawa N. Low proliferation activity may be associated with chemoresistance in clear cell carcinoma of the ovary. Obstetrics & Gynecology 2002;100(2):281-7. - PubMed
Kaern 2005 {published data only}
    1. Kaern J, Aghmesheh M, Nesland JM, Danielsen HE, Sandstad B, Friedlander M, et al. Prognostic factors in ovarian carcinoma stage III patients. Can biomarkers improve the prediction of short- and long-term survivors? International Journal of Gynecological Cancer 2005;15(6):1014-22. - PubMed
Kehoe 2015 {published data only}
    1. Kehoe S, Hook J, Nankivell M, Jayson GC, Kitchener H, Lopes T, et al. Primary chemotherapy versus primary surgery for newly diagnosed advanced ovarian cancer (CHORUS): an open-label, randomised, controlled, non-inferiority trial. Lancet 2015;386(9990):249-57. [12185455] - PubMed
    1. Kehoe S, Hook J, Nankivell M. Chemotherapy or upfront surgery for newly diagnosed advanced ovarian cancer: results from the MRC CHORUS trial. Journal of Clinical Oncology 2013;31 Suppl(15):Abstract 5500. [12185456]
    1. Kehoe S, Wheeler S. CHORUS (Chemotherapy or Upfront Surgery). A randomised feasibility trial to determine the impact of timing of surgery and chemotherapy in newly diagnosed patients with advanced epithelial ovarian, primary peritoneal or fallopian tube carcinoma. www.ctu.mrc.ac.uk/plugins/StudyDisplay/protocols/CHORUS protocol Version 2.0 - 05 June 2008.pdf; and http://www.ctu.mrc.ac.uk/research_areas/study_details.aspx?s=9 (accessed 18/6/2012). [12185457]
    1. Law K, Murray C, Kehoe S. CHORUS - a randomised study to determine the impact of timing of surgery and chemotherapy in newly diagnosed patients with advanced epithelial ovarian, primary peritoneal or fallopian tube carcinoma. In: Annual Meeting of the British Gynaecological Cancer Society; 2006 Nov 30-Dec 1; Manchester, UK. 2006:90. [12185459]
    1. Vergote I, Coens C, Nankivell M, Kristensen GB, Parmar MK, Ehlen T, et al. Neoadjuvant chemotherapy versus debulking surgery in advanced tubo-ovarian cancers: pooled analysis of individual patient data from the EORTC 55971 and CHORUS trials. Lancet Oncology 2018;19:1680-7. [12185460] - PubMed
Kessous 2017 {published data only}
    1. Kessous R, Laskov I, Abitbol J, Bitharas J, Yasmeen A, Salvador S, et al. Clinical outcome of neoadjuvant chemotherapy for advanced ovarian cancer. Gynecologic Oncology 2017;144(3):474-9. - PubMed
Keyver‐Paik 2016 {published data only}
    1. Keyver-Paik MD, Abramian A, Domröse C, Döser A, Höller T, Friedrich M, et al. Integrated care in ovarian cancer “IgV Ovar”: results of a German pilot for higher quality in treatment of ovarian cancer. Journal of Cancer Research and Clinical Oncology 2016;142(2):481-7. - PMC - PubMed
Kirmani 1994 {published data only}
    1. Kirmani S, Braly PS, McClay EF, Saltzstein SL, Plaxe SC, Kim S et al. A comparison of intravenous versus intraperitoneal chemotherapy for the initial treatment of ovarian cancer. Gynecologic Oncology 1994;54(3):338-44. - PubMed
Kristensen 1995 {published data only}
    1. Kristensen GB, Baekelandt M, Vergote IB, Trope C. A phase II study of carboplatin and hexamethylmelamine as induction chemotherapy in advanced epithelial ovarian carcinoma. European Journal of Cancer 1995;31(11):1778-80. - PubMed
Le 1997 {published data only}
    1. Le T, Krepart GV, Lotocki R J, Heywood MS. Does debulking surgery improve survival in biologically aggressive ovarian carcinoma? Gynecologic Oncology 1997;67(2):208-14. - PubMed
Lee 2018 {published data only}
    1. Lee YY, Lee JW, Lu L, Xu W, Kollara A, Brown T, et al. Impact of interval from primary cytoreductive surgery to initiation of adjuvant chemotherapy in advanced epithelial ovarian cancer. International Journal of Gynaecology and Obstetrics 2018;143(3):325-32. - PubMed
Loizzi 2016 {published data only}
    1. Fumarulo VV, Loizzi V, Cormio G, Murgia F, Vecchio V, Minicucci V, et al. Neoadjuvant chemotherapy in advanced ovarian cancer: a single institution experience and a review of the literature. In: International Journal of Gynecological Cancer. Vol. 26. 2016:1-1193.
    1. Loizzi V, Leone L, Camporeale A, Resta L, Selvaggi L, Cicinelli E, et al. Neoadjuvant chemotherapy in advanced ovarian cancer: a single-institution experience and a review of the literature. Oncology 2016;91(4):211-6. - PubMed
Lorusso 1998 {published data only}
    1. Lorusso V, Leone B, Di Vagno G, Manzione L, Palmeri S, Vallejo C. Combined carboplatin plus ifosfamide and cisplatin in patients with advanced ovarian carcinoma. A phase I-II study. Gynecologic Oncology 1998;68(2):172-7. - PubMed
Malik 1998 {published data only}
    1. Malik IM, Khan ZK, Khan WA, Hussain M, Moid I, Rizvi J. Continuous infusion of ifosfamide and cisplatin as first-line therapy of patients with suboptimally debulked stage III/IV epithelial ovarian cancer. International Journal of Gynecological Cancer 1998;8(2):138-43.
Marchetti 1993 {published data only}
    1. Marchetti DL, Lele SB, Priore RL, McPhee ME, Hreshchyshyn MM. Treatment of advanced ovarian carcinoma in the elderly. Gynecologic Oncology 1993;49(1):86-91. - PubMed
McGuire 1996 {published data only}
    1. McGuire WP, Hoskins WJ, Brady MF, Kucera PR, Partridge EE, Look KY, et al. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. New England Journal of Medicine 1996;334(1):1-6. - PubMed
Michaan 2018 {published data only}
    1. Michaan N, Chong WY, Han NY, Lim MC, Park SY. Prognostic value of pathologic chemotherapy response score in patients with ovarian cancer after neoadjuvant chemotherapy. International Journal of Gynecologic Cancer 2018;28(9):1676-82. - PubMed
Ngan 1989 {published data only}
    1. Ngan HY, Choo YC, Cheung M, Wong LC, Ma HK, Collins R. A randomized study of high-dose versus low-dose cis-platinum combined with cyclophosphamide in the treatment of advanced ovarian cancer. Chemotherapy 1989;35(3):221-7. - PubMed
Omura 1989 {published data only}
    1. Omura GA, Bundy BN, Berek JS, Curry S, Delgado G Mortel R. Randomized trial of cyclophosphamide plus cisplatin with or without doxorubicin in ovarian carcinoma: a Gynecologic Oncology Group Study. Journal of Clinical Oncology 1989;7(4):457-65. - PubMed
Onda 2020 {published data only}
    1. Onda T, Matsumoto K, Shibata T, Sato A, Fukuda H, Konishi I, et al. Phase III trial of upfront debulking surgery versus neoadjuvant chemotherapy for stage III/IV ovarian, tubal and peritoneal cancers: Japan Clinical Oncology Group Study JCOG0602. Japanese Journal of Clinical Oncology 2008;38(1):74-7. [12185462] - PubMed
    1. Onda T, Satoh T, Ogawa G, Saito T, Kasamatsu T, Nakanishi T, et al, Japan Clinical Oncology Group. Comparison of survival between primary debulking surgery and neoadjuvant chemotherapy for stage III/IV ovarian, tubal and peritoneal cancers in phase III randomised trial. European Journal of Cancer 2020;130:114-25. - PubMed
    1. Onda T, Satoh T, Saito T, Kasamatsu T, Nakanishi T, Nakamura K, et al. Comparison of treatment invasiveness between upfront debulking surgery versus interval debulking surgery following neoadjuvant chemotherapy for stage III/IV ovarian, tubal, and peritoneal cancers in a phase III randomised trial: Japan Clinical Oncology Group Study JCOG0602. European Journal of Cancer 2016;64:22-31. [12185463] - PubMed
    1. Onda T, Satoh T, Saito T, Kasamatsu T, Nakanishi T, Takehara K, et al. Comparison of survival between upfront primary debulking surgery versus neoadjuvant chemotherapy for stage III/IV ovarian, tubal and peritoneal cancers in phase III randomized trial: JCOG0602. Journal of Clinical Oncology 2018;36(15 Suppl). [12185464]
Palmer 1992 {published data only}
    1. Palmer MC, Shepert E, Schepansky A, MacLean GD. Novel, dose intensive, single-agent cisplatin in the first-line management of advanced stage ovarian cancer. International Journal of Gynecological Cancer 1992;2(6):301-6. - PubMed
Piver 1991 {published data only}
    1. River MS, Fanning J, Sprance HE. Five-year survival for cisplatin-based chemotherapy versus single-agent melphalan in patients with advanced ovarian cancer and optimal debulking surgery. Journal of Surgical Oncology 1991;48(1):39-44. - PubMed
Raspagliesi 2018 {published data only}
    1. Raspagliesi F, Bogani G, Matteucci L, Casarin J, Sabatucci I, Tamberi S, et al. Surgical efforts might mitigate difference in response to neoadjuvant chemotherapy in stage IIIC–IV unresectable ovarian cancer: a case-control multi-institutional study. International Journal of Gynecologic Cancer 2018;28(9):1706-13. - PubMed
Redman 1986 {published data only}
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Risum 2012 {published data only}
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