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Meta-Analysis
. 2021 Jul 30;7(7):CD005343.
doi: 10.1002/14651858.CD005343.pub6.

Neoadjuvant chemotherapy before surgery versus surgery followed by chemotherapy for initial treatment in advanced ovarian epithelial cancer

Sarah L Coleridge  1 , Andrew Bryant  2 , Sean Kehoe  3 , Jo Morrison  4
Affiliations
Meta-Analysis

Neoadjuvant chemotherapy before surgery versus surgery followed by chemotherapy for initial treatment in advanced ovarian epithelial cancer

Sarah L Coleridge et al. Cochrane Database Syst Rev. .

Update in

Abstract

Background: Epithelial ovarian cancer presents at an advanced stage in the majority of women. These women require a combination of surgery and chemotherapy for optimal treatment. Conventional treatment has been to perform surgery first and then give chemotherapy. However, there may be advantages to using chemotherapy before surgery.

Objectives: To assess whether there is an advantage to treating women with advanced epithelial ovarian cancer with chemotherapy before debulking surgery (neoadjuvant chemotherapy (NACT)) compared with conventional treatment where chemotherapy follows debulking surgery (primary debulking surgery (PDS)).

Search methods: We searched the following databases up to 9 October 2020: the Cochrane Central Register of Controlled Trials (CENTRAL), Embase via Ovid, MEDLINE (Silver Platter/Ovid), PDQ and MetaRegister. We also checked the reference lists of relevant papers that were identified to search for further studies. The main investigators of relevant trials were contacted for further information.

Selection criteria: Randomised controlled trials (RCTs) of women with advanced epithelial ovarian cancer (Federation of International Gynaecologists and Obstetricians (FIGO) stage III/IV) who were randomly allocated to treatment groups that compared platinum-based chemotherapy before cytoreductive surgery with platinum-based chemotherapy following cytoreductive surgery.

Data collection and analysis: Two review authors independently extracted data and assessed risk of bias in each included trial. We extracted data of overall (OS) and progression-free survival (PFS), adverse events, surgically-related mortality and morbidity and quality of life outcomes. We used GRADE methods to determine the certainty of evidence.

Main results: We identified 2227 titles and abstracts through our searches, of which five RCTs of varying quality and size met the inclusion criteria. These studies assessed a total of 1774 women with stage IIIc/IV ovarian cancer randomised to NACT followed by interval debulking surgery (IDS) or PDS followed by chemotherapy. We pooled results of the four studies where data were available and found little or no difference with regard to overall survival (OS) (Hazard Ratio (HR) 0.96, 95% CI 0.86 to 1.08; participants = 1692; studies = 4; high-certainty evidence) or progression-free survival in four trials where we were able to pool data (Hazard Ratio 0.98, 95% CI 0.88 to 1.08; participants = 1692; studies = 4; moderate-certainty evidence). Adverse events, surgical morbidity and quality of life (QoL) outcomes were variably and incompletely reported across studies. There are probably clinically meaningful differences in favour of NACT compared to PDS with regard to overall postoperative serious adverse effects (SAE grade 3+): 6% in NACT group, versus 29% in PDS group, (risk ratio (RR) 0.22, 95% CI 0.13 to 0.38; participants = 435; studies = 2; heterogeneity index (I2) = 0%; moderate-certainty evidence). NACT probably results in a large reduction in the need for stoma formation: 5.9% in NACT group, versus 20.4% in PDS group, (RR 0.29, 95% CI 0.12 to 0.74; participants = 632; studies = 2; I2 = 70%; moderate-certainty evidence), and probably reduces the risk of needing bowel resection at the time of surgery: 13.0% in NACT group versus 26.6% in PDS group (RR 0.49, 95% CI 0.30 to 0.79; participants = 1565; studies = 4; I2 = 79%; moderate-certainty evidence). NACT reduces postoperative mortality: 0.6% in NACT group, versus 3.6% in PDS group, (RR 0.16, 95% CI 0.06 to 0.46; participants = 1623; studies = 5; I2 = 0%; high-certainty evidence). QoL on the European Organization for the Research and Treatment of Cancer Quality of Life Questionnaire (EORTC QLQ-C30) scale produced inconsistent and imprecise results in three studies (MD -0.29, 95% CI -2.77 to 2.20; participants = 524; studies = 3; I2 = 81%; very low-certainty evidence) but the evidence is very uncertain and should be interpreted with caution.

Authors' conclusions: The available high to moderate-certainty evidence suggests there is little or no difference in primary survival outcomes between PDS and NACT. NACT probably reduces the risk of serious adverse events, especially those around the time of surgery, and reduces the risk of postoperative mortality and the need for stoma formation. These data will inform women and clinicians (involving specialist gynaecological multidisciplinary teams) and allow treatment to be tailored to the person, taking into account surgical resectability, age, histology, stage and performance status. Data from an unpublished study and ongoing studies are awaited.

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Conflict of interest statement

Sarah Coleridge: no conflict of interest Andrew Bryant: no conflict of interest Sean Kehoe: principle investigator of included study, therefore excluded from title screening, data extraction and all analyses/GRADE decisions Jo Morrison: no conflict of interest

Figures

1
1
Risk of bias summary: review authors' judgements about each risk of bias item for each included study.
2
2
Study flow diagram of the search (up to October 2020).
3
3
Forest plot of comparison: 1 NACT vs PDS, outcome: 1.1 Overall survival.
4
4
In the PDS group 757 people out of 1000 had died over 4 years compared to 743 (95% CI 704 to 783) out of 1000 for the NACT group.  Green = alive at 4 years with PDS/chemo; yellow = additional people alive at 4 years with NACT/IDS; red = people who had died by 4 years with either NACT/PDS or PDS/chemo.
5
5
Forest plot of comparison: 1 NACT vs PDS, outcome: 1.4 Progression‐free survival.
6
6
In the PDS group 858 people out of 1000 had ovarian cancer that had recurred by 2 years compared to 852 (95% CI 821 to 879) out of 1000 for the NACT group.  Green = not had recurrent disease by 2 years with PDS/chemo; yellow = additional people without recurrent disease by 2 years with NACT/IDS; red = peopel with recurrent disease by 2 years with either NACT/PDS or PDS/chemo.
7
7
In the PDS group 29 people out of 100 had G3+ post op serious adverse events (SAE) compared to 6 (95% CI 4 to 20) out of 100 for the NACT group.  Green = no post op G3+ SAE with PDS/chemo; yellow = additional people who were better with NACT/IDS; red = people with G3+ SAEs with either NACT/PDS or PDS/chemo.
8
8
In the control group 20 people out of 100 had stoma formation following initial surgery compared to 6 (95% CI 2 to 15) out of 100 for the active treatment group. Green = no stoma with PDS/chemo; yellow = additional people who didn't require a stoma with NACT/IDS; red = people who required a stoma with either NACT/PDS or PDS/chemo.
9
9
In the PDS group 36 people out of 1000 died in the post‐operative period compared to 6 (95% CI 2 to 17) out of 1000 for the NACT group. Green = alive at the end of the post‐operative period with  PDS/chemo; yellow = additional people who were alive with NACT/IDS; red = people who died in the post‐operative period with either NACT/PDS or PDS/chemo.
1.1
1.1. Analysis
Comparison 1: NACT vs PDS, Outcome 1: Overall survival
1.2
1.2. Analysis
Comparison 1: NACT vs PDS, Outcome 2: Overall survival by age
1.3
1.3. Analysis
Comparison 1: NACT vs PDS, Outcome 3: Overall survival by residual disease
1.4
1.4. Analysis
Comparison 1: NACT vs PDS, Outcome 4: Overall survival by stage
1.5
1.5. Analysis
Comparison 1: NACT vs PDS, Outcome 5: Progression‐free survival
1.6
1.6. Analysis
Comparison 1: NACT vs PDS, Outcome 6: Surgically‐related severe adverse effects (grade 3+)
1.7
1.7. Analysis
Comparison 1: NACT vs PDS, Outcome 7: Postoperative mortality
1.8
1.8. Analysis
Comparison 1: NACT vs PDS, Outcome 8: Chemotherapy‐related SAEs (G3+)
1.9
1.9. Analysis
Comparison 1: NACT vs PDS, Outcome 9: EORTC QLQ‐C30 QoL at 6 months
1.10
1.10. Analysis
Comparison 1: NACT vs PDS, Outcome 10: EORTC QLQ‐C30 QoL at 12 months
See this image and copyright information in PMC

Update of

References

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Robova 2003 {published data only}
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Rowland 2013 {published data only}
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Rowland 2015 {published data only}
    1. Rowland MR, Lesnock JL, Farris C, Kelley JL, Krivak TC. Cost-utility comparison of neoadjuvant chemotherapy versus primary debulking surgery for treatment of advanced-stage ovarian cancer in patients 65 years old or older. American Journal of Obstetrics and Gynecology 2015;212(6):763.e1-8. - PubMed
Rutten 2012 {published data only}
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Salzer 1990 {published data only}
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Sayyah‐Melli 2013 {published data only}
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Schorge 2014 {published data only}
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Schwartz 1994 {published data only}
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Shibata 2003 {published data only}
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Shimizu 1993 {published data only}
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    1. Steed H, Oza AM, Murphy J, Laframboise S, Lockwood G, Petrillo D, et al. A retrospective analysis of neoadjuvant platinum-based chemotherapy versus up-front surgery in advanced ovarian cancer. International Journal of Gynecological Cancer 2006;16(Suppl 1):47-53. - PubMed
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Surwit 1999 {published data only}
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Taskin 2013 {published data only}
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Taylor 2015 {published data only}
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Tran 2018 {published data only}
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Trope 1997 {published data only}
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Van der Burg 1995 {published data only}
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Van Meurs 2013 {published data only}
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Varma 1990 {published data only}
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Vergote 1998 {published data only}
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Vergote 2018 {published data only}
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Vergote 2019 {published data only}
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    1. Wright J, Ananth C, Tsui J, Glied S, Burke W, Lu Y, et al. Comparative effectiveness of upfront treatment strategies in elderly women with ovarian cancer. Cancer 2014;120(8):1246-54. - PMC - PubMed
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    1. Xiao Y, Xie S, Zhang N, Wang J, Lv C, Guo J, et al. Platinum-based neoadjuvant chemotherapy versus primary surgery in ovarian carcinoma International Federation of Gynecology and Obstetrics Stages IIIc and IV: a systematic review and meta-analysis. Gynecologic and Obstetric Investigation 2017;83(3):209-18. - PubMed
Yang 2017 {published data only}
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Zamagni 2014 {published data only}
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Zeng 2016 {published data only}
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References to studies awaiting assessment

Jiang 2018 {published data only}
    1. Jiang Y, He W, Yang H, Su Z, Sun L. Analysis of clinical effects of neoadjuvant chemotherapy in advanced epithelial ovarian cance. Journal of the Balkan Union of Oncology 2018;23:3. - PubMed

References to ongoing studies

Kumar 2009 {published and unpublished data}
    1. Janga D, Kumar L, Kumar S, Shukla NK, Thulkar S, Singh R. Neoadjuvant chemotherapy (CT) followed by debulking surgery vs upfront surgery followed by chemotherapy in advanced epithelial ovarian carcinoma (EOC): a prospective, randomized study. Proceedings of the American Society of Clinical Oncology 2003;22:487.
    1. Kumar L, Hariprasad R, Kumar S, Bhatla N, Shukla N, Thulkar S, et al. Neoadjuvant chemotherapy in advanced epithelial ovarian cancer (EOC): a phase III randomized study. Journal of Clinical Oncology (ASCO Annual Meeting Proceedings Part I 2006 (June 20 Supplement)) 2006;24(Suppl):18.
    1. Kumar L, Hariprasad R, Kumar S, Bhatla N, Thulkar S, Shukla NJ. Neo-adjuvant chemotherapy in advanced epithelial ovarian cancer (EOC): a prospective, randomized study. Indian Journal of Medical and Paediatric Oncology 2009;30(1):15.
    1. Kumar L, Hariprasad R, Kumar S, Bhatla N, Thulkar S, Vijayaraghavan M, et al. Neoadjuvant chemotherapy followed by interval debulking surgery versus upfront surgery followed by chemotherapy in advanced epithelial ovarian carcinoma: a prospective randomized study - interim results. Journal of Clinical Oncology (ASCO Annual Meeting Proceedings Part I. 2007) 2007;25(18S Suppl):5531.
    1. Kumar L, Hariprasad R, Kumar S, Bhatla N, Thulkar S, Vijayaraghavan M. Neoadjuvant chemotherapy followed by interval debulking surgery versus upfront surgery followed by chemotherapy in advanced epithelial ovarian carcinoma: a prospective randomized study - interim results. Journal of Clinical Oncology (ASCO Annual Meeting Proceedings Part I) 2007;25(18 Suppl):5531.
Mahner 2017 {published data only}
    1. Mahner S, Heitz F, Burges A, Reuss A, Kraemer B, Schmalfeldt B, et al. TRUST: trial of radical upfront surgical therapy in advanced ovarian cancer (ENGOT ov33/AGO-OVAR OP7). Journal of Clinical Oncology (Annual Meeting of the American Society of Clinical Oncology, ASCO, 2017; United States 912 0139) 2017;35 (15 Supplement 1)(15 Suppl 1):(no pagination).
    1. Mahner S, Heitz F, Burges A, Reuss A, Kramer B, Schmalfeldt B, et al. Role of neoadjuvant chemotherapy in advanced ovarian cancer: TRUST-trial of radical upfront surgical therapy in advanced ovarian cancer (ENGOT ov33/AGO-OVAR OP7). In: Oncology Research and Treatment Conference (Jahrestagung der Deutschen, Osterreichischen und Schweizerischen); Annual Meeting of German, Austrian and Swiss Societies for Hematology and Medical Oncology 2017; Germany. Vol. 40 (Suppl 3). Berlin: Karger AG 0142 825, 2017.
    1. Reuss A, Du Bois A, Harter P, Fotopoulou C, Sehouli J, Aletti G, et al. TRUST: Trial of Radical Upfront Surgical Therapy in advanced ovarian cancer (ENGOT ov33/AGO-OVAR OP7). International Journal of Gynecological Cancer 2019;29(8):1327-31. - PubMed
NCT04257786 {published data only}
    1. NCT04257786. Primary cyto-reductive surgery vs neo-adjuvant chemotherapy (NAC) in epithelial ovarian cancer. Clinicaltrials.gov.
NCT04515602 {published data only}
    1. NCT04515602. Stratified evaluation of PDS and NACT-IDS in ovarian cancer. Clinicaltrials.gov.
SUNNY {published data only}
    1. NCT02859038. Study of upfront surgery versus neoadjuvant chemotherapy in patients with advanced ovarian cancer (SUNNY). ClinicalTrials.gov.

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References to other published versions of this review

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