Prognostic impact of cytoreductive surgery conducted with primary intent, versus cytoreductive surgery after neoadjuvant chemotherapy, in the management of patients with advanced epithelial ovarian cancers: a multicentre, propensity score-matched study from the FRANCOGYN group.

epithelial ovarian cancer interval cytoreductive surgery neoadjuvant chemotherapy primary cytoreductive surgery propensity score

Journal

BJOG : an international journal of obstetrics and gynaecology
ISSN: 1471-0528
Titre abrégé: BJOG
Pays: England
ID NLM: 100935741

Informations de publication

Date de publication:
Nov 2023
Historique:
revised: 05 04 2023
received: 10 02 2023
accepted: 15 04 2023
pubmed: 11 5 2023
medline: 11 5 2023
entrez: 11 5 2023
Statut: ppublish

Résumé

To compare survival and morbidity rates between primary cytoreductive surgery (pCRS) and interval cytoreductive surgery (iCRS) for epithelial ovarian cancer (EOC), using a propensity score. We conducted a propensity score-matched cohort study, using data from the FRANCOGYN cohort. Retrospective, multicentre study of data from patients followed in 15 French department specialized in the treatment of ovarian cancer. Patients included were those with International Federation of Gynaecology and Obstetrics (FIGO) stage III or IV EOC, with peritoneal carcinomatosis, having undergone CRS. The propensity score was designed using pre-therapeutic variables associated with both treatment allocation and overall survival (OS). The primary outcome was OS. Secondary outcomes included recurrence-free survival (RFS), quality of CRS and other variables related to surgical morbidity. A total of 513 patients were included. Among these, 334 could be matched, forming 167 pairs. No difference in OS was found (hazard ratio, HR = 0.8, p = 0.32). There was also no difference in RFS (median = 26 months in both groups) nor in the rate of CRS leaving no macroscopic residual disease (pCRS 85%, iCRS 81.4%, p = 0.76). The rates of gastrointestinal tract resections, stoma, postoperative complications and hospital stay were significantly higher in the pCRS group. Analysis of groups of patients made comparable by propensity score matching showed no difference in survival, but lower postoperative morbidity in patients treated with iCRS.

Identifiants

pubmed: 37165717
doi: 10.1111/1471-0528.17524
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1511-1520

Informations de copyright

© 2023 John Wiley & Sons Ltd.

Références

Policy brief: ovarian cancer in the EU (2022). Eurohealth; 2018 [cited 2022 Jul 8]. Available from: https://eurohealth.ie/policy-brief-women-and-ovarian-cancer-in-the-eu-2018/
SPF. Survie des personnes atteintes de cancer en France métropolitaine 1989-2013. Etude à partir des registres des cancers du réseau Francim. Partie 1: tumeurs solides. [cited 2022 Feb 8]. Available from: https://www.santepubliquefrance.fr/notices/survie-des-personnes-atteintes-de-cancer-en-france-metropolitaine-1989-2013.-etude-a-partir-des-registres-des-cancers-du-reseau-francim.-partie-1
Argento M, Hoffman P, Gauchez AS. Ovarian cancer detection and treatment: current situation and future prospects. Anticancer Res. 2008;28(5B):3135-8.
Munnell EW. The changing prognosis and treatment in cancer of the ovary: a report of 235 patients with primary ovarian carcinoma 1952-1961. Am J Obstet Gynecol. 1968;100(6):790-805. https://doi.org/10.1016/S0002-9378(15)33580-8
Bertelsen K. Tumor reduction surgery and long-term survival in advanced ovarian cancer: a DACOVA study. Gynecol Oncol. 1990;38(2):203-9. https://doi.org/10.1016/0090-8258(90)90042-j
Eisenkop SM, Friedman RL, Wang HJ. Complete cytoreductive surgery is feasible and maximizes survival in patients with advanced epithelial ovarian cancer: a prospective study. Gynecol Oncol. 1998;69(2):103-8. https://doi.org/10.1006/gyno.1998.4955
von Georgi R, Franke FE, Münstedt K. Influence of surgery and postoperative therapy and tumor characteristics on patient prognosis in advanced ovarian carcinomas. Eur J Obstet Gynecol Reprod Biol. 2003;111(2):189-96. https://doi.org/10.1016/s0301-2115(03)00239-2
Bristow RE, Tomacruz RS, Armstrong DK, Trimble EL, Montz FJ. Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis. J Clin Oncol. 2002;20(5):1248-59. https://doi.org/10.1200/JCO.2002.20.5.1248
Lavoue V, Huchon C, Akladios C, Alfonsi P, Bakrin N, Ballester M, et al. Management of epithelial cancer of the ovary, fallopian tube, primary peritoneum. Long text of the joint French clinical practice guidelines issued by FRANCOGYN, CNGOF, SFOG, GINECO-ARCAGY, endorsed by INCa (part 2: systemic, intraperitoneal treatment, elderly patients, fertility preservation, follow-up). J Gynecol Obstet Hum Reprod. 2019;48(6):379-86. https://doi.org/10.1016/j.jogoh.2019.03.018
Vergote I, Tropé CG, Amant F, Kristensen GB, Ehlen T, Johnson N, et al. Neoadjuvant chemotherapy or primary surgery in stage IIIC or IV ovarian cancer. N Engl J Med. 2010;363(10):943-53.
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. https://doi.org/10.1016/S0140-6736(14)62223-6
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). Int J Gynecol Cancer. 2020;30(11):1657-64. https://doi.org/10.1136/ijgc-2020-001640
Aletti GD, Dowdy SC, Podratz KC, Cliby WA. Relationship among surgical complexity, short-term morbidity, and overall survival in primary surgery for advanced ovarian cancer. Am J Obstet Gynecol. 2007;197(6):676.e1-7. https://doi.org/10.1016/j.ajog.2007.10.495
Sugarbaker PH. Successful management of microscopic residual disease in large bowel cancer. Cancer Chemother Pharmacol. 1999;43(Suppl):S15-25. https://doi.org/10.1007/s002800051093
Dabi Y, Thubert T, Fuchs F, Barjat T, Belaisch-Allart J, Ceccaldi PF, et al. How is functionning the Ethical Review Board « Comité d'Ethique Pour La Recherche En Obstétrique Et Gynécologie » (CEROG)? J Gynecol Obstet Hum Reprod. 2022;51(4):102352. https://doi.org/10.1016/j.jogoh.2022.102352
Ayaz-Alkaya S. Overview of psychosocial problems in individuals with stoma: a review of literature. Int Wound J. 2019;16(1):243-9. https://doi.org/10.1111/iwj.13018
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. Eur J Cancer. 2016;64:22-31. https://doi.org/10.1016/j.ejca.2016.05.017
Elies A, Rivière S, Pouget N, Becette V, Dubot C, Donnadieu A, et al. The role of neoadjuvant chemotherapy in ovarian cancer. Expert Rev Anticancer Ther. 2018;18(6):555-66. https://doi.org/10.1080/14737140.2018.1458614
Vergote I, Coens C, Nankivell M, Kristensen GB, Parmar MKB, 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 Oncol. 2018;19(12):1680-7. https://doi.org/10.1016/S1470-2045(18)30566-7
Cantrell LA, Pfisterer J, Boggess J, Duska LR. Interpreting randomized clinical trials in gynecologic oncology surgery: does one size fit all? Am Soc Clin Oncol Educ Book. 2019;39:342-50. https://doi.org/10.1200/EDBK_237945
Coleridge SL, Bryant A, Kehoe S, Morrison J. Neoadjuvant chemotherapy before surgery versus surgery followed by chemotherapy for initial treatment in advanced ovarian epithelial cancer. Cochrane Database Syst Rev. 2021;7:CD005343. https://doi.org/10.1002/14651858.CD005343.pub6
Chiva L, Lapuente F, Castellanos T, Alonso S, Gonzalez-Martin A. What should we expect after a complete cytoreduction at the time of interval or primary debulking surgery in advanced ovarian cancer? Ann Surg Oncol. 2016;23(5):1666-73. https://doi.org/10.1245/s10434-015-5051-9
Falconer H, Joneborg U, Krawiec K, Palsdottir K, Bottai M, Salehi S. Ultra-radical upfront surgery does not improve survival in women with advanced epithelial ovarian cancer; a natural experiment in a complete population. Gynecol Oncol. 2020;159(1):58-65. https://doi.org/10.1016/j.ygyno.2020.07.009
Cummings M, Nicolais O, Shahin M. Surgery in advanced ovary cancer: primary versus interval cytoreduction. Diagnostics. 2022;12(4):988. https://doi.org/10.3390/diagnostics12040988
Russell B, Hawarden A, Gee M, Edmondson RJ. Propensity score matching confirms that primary surgery or neoadjuvant chemotherapy result in equivalent survival within a comprehensive cohort of patients with high-grade serous ovarian cancer. Gynecol Oncol. 2021;160(1):24-31. https://doi.org/10.1016/j.ygyno.2020.10.035
Seagle BLL, Graves S, Strohl AE, Shahabi S. Survival after primary debulking surgery compared with neoadjuvant chemotherapy in advanced ovarian cancer: a National Cancer Database Study. Int J Gynecol Cancer. 2017;27(8):1610-8. https://doi.org/10.1097/IGC.0000000000001072
Lyons YA, Reyes HD, McDonald ME, Newtson A, Devor E, Bender DP, et al. Interval debulking surgery is not worth the wait: a National Cancer Database study comparing primary cytoreductive surgery versus neoadjuvant chemotherapy. Int J Gynecol Cancer. 2020;30(6):845-52. https://doi.org/10.1136/ijgc-2019-001124
Melamed A, Rauh-Hain JA, Gockley AA, Nitecki R, Ramirez PT, Hershman DL, et al. Association between overall survival and the tendency for cancer programs to administer neoadjuvant chemotherapy for patients with advanced ovarian cancer. JAMA Oncol. 2021;7(12):1782-90. https://doi.org/10.1001/jamaoncol.2021.4252
Fagotti A, Ferrandina G, Fanfani F, Ercoli A, Lorusso D, Rossi M, et al. A laparoscopy-based score to predict surgical outcome in patients with advanced ovarian carcinoma: a pilot study. Ann Surg Oncol. 2006;13(8):1156-61. https://doi.org/10.1245/ASO.2006.08.021
Hall M, Savvatis K, Nixon K, Kyrgiou M, Hariharan K, Padwick M, et al. Maximal-effort cytoreductive surgery for ovarian cancer patients with a high tumor burden: variations in practice and impact on outcome. Ann Surg Oncol. 2019;26(9):2943-51. https://doi.org/10.1245/s10434-019-07516-3
Liu YL, Filippova OT, Zhou Q, Iasonos A, Chi DS, Zivanovic O, et al. Characteristics and survival of ovarian cancer patients treated with neoadjuvant chemotherapy but not undergoing interval debulking surgery. J Gynecol Oncol. 2020;31(1):e17. https://doi.org/10.3802/jgo.2020.31.e17
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). Int J Gynecol Cancer. 2019;29(8):1327-31. https://doi.org/10.1136/ijgc-2019-000682

Auteurs

Henri Wohrer (H)

Department of Gynaecological Oncological and Breast Surgery, Assistance Publique des Hôpitaux de Paris (AP-HP), Hôpital Européen Georges-Pompidou, Paris, France.

Meriem Koual (M)

Department of Gynaecological Oncological and Breast Surgery, Assistance Publique des Hôpitaux de Paris (AP-HP), Hôpital Européen Georges-Pompidou, Paris, France.
INSERM UMR-S 1124, University of Paris Cité, Centre Universitaire des Saint-Père, Paris, France.

Enrica Bentivegna (E)

Department of Gynaecological Oncological and Breast Surgery, Assistance Publique des Hôpitaux de Paris (AP-HP), Hôpital Européen Georges-Pompidou, Paris, France.

Louise Benoit (L)

Department of Gynaecological Oncological and Breast Surgery, Assistance Publique des Hôpitaux de Paris (AP-HP), Hôpital Européen Georges-Pompidou, Paris, France.
INSERM UMR-S 1124, University of Paris Cité, Centre Universitaire des Saint-Père, Paris, France.

Marie Metairie (M)

Department of Gynaecological Oncological and Breast Surgery, Assistance Publique des Hôpitaux de Paris (AP-HP), Hôpital Européen Georges-Pompidou, Paris, France.

Pierre-Adrien Bolze (PA)

Department of Gynecologic and Oncologic Surgery and Obstetrics, Lyon Sud University Hospital, Hospices Civils de Lyon, Université Lyon 1, Lyon, France.

Yohan Kerbage (Y)

CHU Lille, Service de Chirurgie Gynécologique, Université Lille, Lille, France.

Emilie Raimond (E)

Department of Obstetrics and Gynaecology, Institute Alix de Champagne University Hospital, Reims, France.

Cherif Akladios (C)

Department of Gynaecology, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.

Xavier Carcopino (X)

Department of Obstetrics and Gynaecology, Hôpital Nord, APHM, Aix-Marseille University (AMU), Univ Avignon, CNRS, IRD, IMBE UMR 7263, Marseille, France.

Geoffroy Canlorbe (G)

Department of Gynecological and Breast Surgery and Oncology, Pitié-Salpêtrière, Assistance Publique-Hôpitaux de Paris (AP-HP), University Hospital, Paris, France.
Centre de Recherche Saint-Antoine (CRSA), INSERM UMR_S_938, Cancer Biology and Therapeutics, Sorbonne University, Paris, France.
University Institute of Cancer, Sorbonne University, Paris, France.

Jennifer Uzan (J)

Department of Obstetrics Gynecology and Reproductive Medicine, University Paris Est Créteil, Centre Hospitalier Inter-Communal de Créteil, Creteil, France.

Vincent Lavoue (V)

Service de Gynécologie, INSERM 1242, Oncogenesis, Stress and Signaling, CRLC Eugène Marquis, Université de Rennes 1, Hopital Sud, CHU de Rennes, Rennes, France.

Camille Mimoun (C)

Service de Chirurgie Gynécologique - Université de Paris, Hôpital Lariboisière, Paris, France.

Cyrille Huchon (C)

Service de Chirurgie Gynécologique - Université de Paris, Hôpital Lariboisière, Paris, France.

Martin Koskas (M)

Division of Gynaecologic Oncology, Bichat University Hospital, Paris, France.

Hélène Costaz (H)

Department of Surgical Oncology, Georges-Francois Leclerc Centre, Dijon, France.

François Margueritte (F)

Department of Gynaecology, Centre Hospitalier Intercommunal de Poissy-Saint-Germain-en-Laye Site Hospitalier de Poissy, Poissy, France.

Yohann Dabi (Y)

Department of Gynaecology and Obstetrics, Hôpital Tenon, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.

Cyril Touboul (C)

Department of Gynaecology and Obstetrics, Hôpital Tenon, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.

Sofiane Bendifallah (S)

Department of Gynaecology and Obstetrics, Hôpital Tenon, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.

Lobna Ouldamer (L)

Department of Gynaecology, Hôpital Universitaire de Tours, Tours, France.

Nicolas Delanoy (N)

Institut du Cancer Paris CARPEM, Université de Paris Cité, Paris, France.
Department of Medical Oncology, AP-HP Centre, Hopital Européen Georges Pompidou, Paris, France.

Huyen-Thu Nguyen-Xuan (HT)

Department of Gynaecological Oncological and Breast Surgery, Assistance Publique des Hôpitaux de Paris (AP-HP), Hôpital Européen Georges-Pompidou, Paris, France.

Anne-Sophie Bats (AS)

Department of Gynaecological Oncological and Breast Surgery, Assistance Publique des Hôpitaux de Paris (AP-HP), Hôpital Européen Georges-Pompidou, Paris, France.
Institut du Cancer Paris CARPEM, Université de Paris Cité, Paris, France.
INSERM UMR-S 1147, Centre de Recherche des Cordeliers, University of Paris Cité, Paris, France.

Henri Azaïs (H)

Department of Gynaecological Oncological and Breast Surgery, Assistance Publique des Hôpitaux de Paris (AP-HP), Hôpital Européen Georges-Pompidou, Paris, France.
Institut du Cancer Paris CARPEM, Université de Paris Cité, Paris, France.
INSERM UMR-S 1147, Centre de Recherche des Cordeliers, University of Paris Cité, Paris, France.

Classifications MeSH