Minimally Invasive Surgery in the Management of Advanced Epithelial Ovarian Cancer: A Comprehensive Analysis of Current Evidence and Clinical Applications
Abstract
1. Introduction
2. Materials and Methods
3. Results
3.1. Role of Laparoscopic Surgery in Primary Debulking and in Its Planning
3.2. Laparoscopy in Interval Debulking Surgery
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
| EOC | Epithelial ovarian cancer |
| PDS | Primary debulking surgery |
| IDS | Interval debulking surgery |
| MIS | Minimally invasive surgery |
| OS | Overall survival |
| PFS | Progression-free survival |
| NACT | Neoadjuvant chemotherapy |
| R0 | no residual tumor |
References
- Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2020. CA Cancer J. Clin. 2020, 70, 7–30. [Google Scholar] [CrossRef]
- Bristow, R.E.; Santillan, A.; Diaz-Montes, T.P.; Gardner, G.J.; Giuntoli, R.L.; Meisner, B.C.; Frick, K.D.; Armstrong, D.K. Centralization of care for patients with advanced-stage ovarian cancer: A cost-effectiveness analysis. Cancer 2007, 109, 1513–1522. [Google Scholar] [CrossRef]
- Mandato, V.D.; Abrate, M.; De Iaco, P.; Pirillo, D.; Ciarlini, G.; Leoni, M.; Comerci, G.; Ventura, A.; Lenzi, B.; Amadori, A.; et al. Clinical governance network for clinical audit to improve quality in epithelial ovarian cancer management. J. Ovarian Res. 2013, 6, 19. [Google Scholar] [CrossRef]
- Bogani, G.; Coleman, R.L.; Vergote, I.; van Gorp, T.; Ray-Coquard, I.; Oaknin, A.; Matulonis, U.; O’Malley, D.; Raspagliesi, F.; Scambia, G.; et al. Mirvetuximab soravtansine-gynx: First antibody/antigen-drug conjugate (ADC) in advanced or recurrent ovarian cancer. Int. J. Gynecol. Cancer 2024, 34, 469–477. [Google Scholar] [CrossRef] [PubMed]
- Chang, S.-J.; Hodeib, M.; Chang, J.; Bristow, R.E. Survival impact of complete cytoreduction to no gross residual disease for advanced-stage ovarian cancer: A meta-analysis. Gynecol. Oncol. 2013, 130, 493–498. [Google Scholar] [CrossRef]
- Vergote, I.; Tropé, C.G.; Amant, F.; Kristensen, G.B.; Ehlen, T.; Johnson, N.; Verheijen, R.H.M.; van der Burg, M.E.L.; Lacave, A.J.; Panici, P.B.; et al. Neoadjuvant chemotherapy or primary surgery in stage IIIC or IV ovarian cancer. N. Engl. J. Med. 2010, 363, 943–953. [Google Scholar] [CrossRef] [PubMed]
- Kehoe, S.; Hook, J.; Nankivell, M.; Jayson, G.C.; Kitchener, H.; Lopes, T.; Luesley, D.; Perren, T.; Bannoo, S.; Mascarenhas, M.; et al. Primary chemotherapy versus primary surgery for newly diagnosed advanced ovarian cancer (CHORUS): An open-label, randomised, controlled, non-inferiority trial. Lancet Lond. Engl. 2015, 386, 249–257. [Google Scholar] [CrossRef]
- Fagotti, A.; Ferrandina, M.G.; Vizzielli, G.; Pasciuto, T.; Fanfani, F.; Gallotta, V.; Margariti, P.A.; Chiantera, V.; Costantini, B.; Gueli Alletti, S.; et al. Randomized trial of primary debulking surgery versus neoadjuvant chemotherapy for advanced epithelial ovarian cancer (SCORPION-NCT01461850). Int. J. Gynecol. Cancer 2020, 30, 1657–1664. [Google Scholar] [CrossRef]
- Gómez-Hidalgo, N.R.; Martinez-Cannon, B.A.; Nick, A.M.; Lu, K.H.; Sood, A.K.; Coleman, R.L.; Ramirez, P.T. Predictors of optimal cytoreduction in patients with newly diagnosed advanced-stage epithelial ovarian cancer: Time to incorporate laparoscopic assessment into the standard of care. Gynecol. Oncol. 2015, 137, 553–558. [Google Scholar] [CrossRef] [PubMed]
- Corrado, G.; Mancini, E.; Cutillo, G.; Baiocco, E.; Vici, P.; Sergi, D.; Patrizi, L.; Saltari, M.; Baffa, A.; Vizza, E. Laparoscopic Debulking Surgery in the Management of Advanced Ovarian Cancer After Neoadjuvant Chemotherapy. Int. J. Gynecol. Cancer 2015, 25, 1253–1257. [Google Scholar] [CrossRef]
- Fagotti, A.; Gueli Alletti, S.; Corrado, G.; Cola, E.; Vizza, E.; Vieira, M.; Andrade, C.E.; Tsunoda, A.; Favero, G.; Zapardiel, I.; et al. The INTERNATIONAL MISSION study: Minimally invasive surgery in ovarian neoplasms after neoadjuvant chemotherapy. Int. J. Gynecol. Cancer 2019, 29, 5–9. [Google Scholar] [CrossRef]
- Tozzi, R.; Noventa, M.; Saccardi, C.; Spagnol, G.; De Tommasi, O.; Coldebella, D.; Marchetti, M. Feasibility of laparoscopic Visceral-Peritoneal Debulking (L-VPD) in patients with stage III-IV ovarian cancer: The ULTRA-LAP trial pilot study. J. Gynecol. Oncol. 2024, 35, e14. [Google Scholar] [CrossRef]
- Ceccaroni, M.; Roviglione, G.; Bruni, F.; Dababou, S.; Venier, M.; Zorzi, C.; Salgarello, M.; Ruffo, G.; Alongi, F.; Gori, S.; et al. “Things Have Changed”-Laparoscopic Cytoreduction for Advanced and Recurrent Ovarian Cancer: The Experience of a Referral Center on 108 Patients. Cancers 2023, 15, 5726. [Google Scholar] [CrossRef]
- Fagotti, A.; Fanfani, F.; Ludovisi, M.; Lo Voi, R.; Bifulco, G.; Testa, A.C.; Scambia, G. Role of laparoscopy to assess the chance of optimal cytoreductive surgery in advanced ovarian cancer: A pilot study. Gynecol. Oncol. 2005, 96, 729–735. [Google Scholar] [CrossRef] [PubMed]
- Harrison, R.F.; Cantor, S.B.; Sun, C.C.; Villanueva, M.; Westin, S.N.; Fleming, N.D.; Toumazis, I.; Sood, A.K.; Lu, K.H.; Meyer, L.A. Cost-effectiveness of laparoscopic disease assessment in patients with newly diagnosed advanced ovarian cancer. Gynecol. Oncol. 2021, 161, 56–62. [Google Scholar] [CrossRef] [PubMed]
- Gallotta, V.; Cicero, C.; Conte, C.; Vizzielli, G.; Petrillo, M.; Fagotti, A.; Chiantera, V.; Costantini, B.; Scambia, G.; Ferrandina, G. Robotic Versus Laparoscopic Staging for Early Ovarian Cancer: A Case-Matched Control Study. J. Minim. Invasive Gynecol. 2017, 24, 293–298. [Google Scholar] [CrossRef] [PubMed]
- Certelli, C.; Russo, S.A.; Palmieri, L.; Foresta, A.; Pedone Anchora, L.; Vargiu, V.; Santullo, F.; Fagotti, A.; Scambia, G.; Gallotta, V. Minimally-Invasive Secondary Cytoreduction in Recurrent Ovarian Cancer. Cancers 2023, 15, 4769. [Google Scholar] [CrossRef]
- Brun, J.-L.; Rouzier, R.; Uzan, S.; Daraï, E. External validation of a laparoscopic-based score to evaluate resectability of advanced ovarian cancers: Clues for a simplified score. Gynecol. Oncol. 2008, 110, 354–359. [Google Scholar] [CrossRef]
- Fagotti, A.; Vizzielli, G.; De Iaco, P.; Surico, D.; Buda, A.; Mandato, V.D.; Petruzzelli, F.; Ghezzi, F.; Garzarelli, S.; Mereu, L.; et al. A multicentric trial (Olympia-MITO 13) on the accuracy of laparoscopy to assess peritoneal spread in ovarian cancer. Am. J. Obstet. Gynecol. 2013, 209, 462.E1–462.E11. [Google Scholar] [CrossRef]
- Gueli Alletti, S.; Petrillo, M.; Vizzielli, G.; Bottoni, C.; Nardelli, F.; Costantini, B.; Quagliozzi, L.; Gallotta, V.; Scambia, G.; Fagotti, A. Minimally invasive versus standard laparotomic interval debulking surgery in ovarian neoplasm: A single-institution retrospective case-control study. Gynecol. Oncol. 2016, 143, 516–520. [Google Scholar] [CrossRef]
- Gueli Alletti, S.; Bottoni, C.; Fanfani, F.; Gallotta, V.; Chiantera, V.; Costantini, B.; Cosentino, F.; Ercoli, A.; Scambia, G.; Fagotti, A. Minimally invasive interval debulking surgery in ovarian neoplasm (MISSION trial-NCT02324595): A feasibility study. Am. J. Obstet. Gynecol. 2016, 214, e1–e503. [Google Scholar] [CrossRef]
- Vizzielli, G.; Costantini, B.; Tortorella, L.; Pitruzzella, I.; Gallotta, V.; Fanfani, F.; Gueli Alletti, S.; Cosentino, F.; Nero, C.; Scambia, G.; et al. A laparoscopic risk-adjusted model to predict major complications after primary debulking surgery in ovarian cancer: A single-institution assessment. Gynecol. Oncol. 2016, 142, 19–24. [Google Scholar] [CrossRef]
- Ackroyd, S.A.; Thomas, S.; Angel, C.; Moore, R.; Meacham, P.J.; DuBeshter, B. Interval robotic cytoreduction following neoadjuvant chemotherapy in advanced ovarian cancer. J. Robot. Surg. 2018, 12, 245–250. [Google Scholar] [CrossRef]
- Brown, J.; Drury, L.; Crane, E.K.; Anderson, W.E.; Tait, D.L.; Higgins, R.V.; Naumann, R.W. When Less Is More: Minimally Invasive Surgery Compared with Laparotomy for Interval Debulking After Neoadjuvant Chemotherapy in Women with Advanced Ovarian Cancer. J. Minim. Invasive Gynecol. 2019, 26, 902–909. [Google Scholar] [CrossRef] [PubMed]
- Davidson, B.A.; Broadwater, G.; Crim, A.; Boccacio, R.; Bixel, K.; Backes, F.; Previs, R.A.; Salinaro, J.; Salani, R.; Moore, K.; et al. Surgical complexity score and role of laparoscopy in women with advanced ovarian cancer treated with neoadjuvant chemotherapy. Gynecol. Oncol. 2019, 152, 554–559. [Google Scholar] [CrossRef]
- Zhang, Y.; Grant, M.S.; Zhang, X.; Paraghamian, S.E.; Tan, X.; Clark, L.H. Comparing Laparotomy with Robot-assisted Interval Debulking Surgery for Patients with Advanced Epithelial Ovarian Cancer Receiving Neoadjuvant Chemotherapy. J. Minim. Invasive Gynecol. 2021, 28, 1237–1243. [Google Scholar] [CrossRef] [PubMed]
- Morton, M.; Chambers, L.M.; Costales, A.B.; Chichura, A.; Gruner, M.; Horowitz, M.P.; Rose, P.G.; Yao, M.; Debernardo, R.; Michener, C. Assessing feasibility and perioperative outcomes with minimally invasive surgery compared with laparotomy for interval debulking surgery with hyperthermic intraperitoneal chemotherapy for advanced epithelial ovarian cancer. Gynecol. Oncol. 2021, 160, 45–50. [Google Scholar] [CrossRef]
- Pomel, C.; Akladios, C.; Lambaudie, E.; Rouzier, R.; Ferron, G.; Lecuru, F.; Classe, J.-M.; Fourchotte, V.; Paillocher, N.; Wattiez, A.; et al. Laparoscopic management of advanced epithelial ovarian cancer after neoadjuvant chemotherapy: A phase II prospective multicenter non-randomized trial (the CILOVE study). Int. J. Gynecol. Cancer 2021, 31, 1572–1578. [Google Scholar] [CrossRef] [PubMed]
- Lecointre, L.; Pellerin, M.; Venkatasamy, A.; Fabacher, T.; Eberst, L.; Gantzer, J.; Jochum, F.; Faller, E.; Boisrame, T.; Querleu, D.; et al. Complete Laparoscopic Interval Debulking Surgery for Advanced Ovarian Cancer Achieves Similar Survival Outcomes to Open Approach: A Propensity-Matched Study. J. Investig. Surg. Off. J. Acad. Surg. Res. 2022, 35, 1394–1401. [Google Scholar] [CrossRef]
- Lee, Y.J.; Chung, Y.S.; Lee, J.-Y.; Nam, E.J.; Kim, S.W.; Kim, Y.T.; Kim, S. Role of diagnostic laparoscopy in deciding primary treatment in advanced-stage ovarian cancer. J. Gynecol. Oncol. 2023, 34, e17. [Google Scholar] [CrossRef]
- Jorgensen, K.; Melamed, A.; Wu, C.-F.; Nitecki, R.; Pareja, R.; Fagotti, A.; Schorge, J.O.; Ramirez, P.T.; Rauh-Hain, J.A. Minimally invasive interval debulking surgery for advanced ovarian cancer after neoadjuvant chemotherapy. Gynecol. Oncol. 2023, 172, 130–137. [Google Scholar] [CrossRef]
- Rauh-Hain, J.A.; Melamed, A.; Pareja, R.; May, T.; Sinno, A.; McNally, L.; Horowitz, N.S.; De Iaco, P.; Michener, C.M.; Van Lonkhuijzen, L.; et al. Laparoscopic Cytoreduction After Neoadjuvant Chemotherapy in High-Grade Epithelial Ovarian Cancer: A LANCE Randomized Clinical Trial. JAMA Netw. Open 2024, 7, e2446325. [Google Scholar] [CrossRef]
- Uwins, C.; Assalaarachchi, H.; Bennett, K.; Read, J.; Tailor, A.; Crawshaw, J.; Chatterjee, J.; Ellis, P.; Skene, S.S.; Michael, A.; et al. MIRRORS: A prospective cohort study assessing the feasibility of robotic interval debulking surgery for advanced-stage ovarian cancer. Int. J. Gynecol. Cancer 2024, 34, 886–897. [Google Scholar] [CrossRef] [PubMed]
- van de Vrie, R.; Rutten, M.J.; Asseler, J.D.; Leeflang, M.M.; Kenter, G.G.; Mol, B.W.J.; Buist, M. Laparoscopy for diagnosing resectability of disease in women with advanced ovarian cancer. Cochrane Database Syst. Rev. 2019, 3, CD009786. [Google Scholar] [CrossRef] [PubMed]
- Lheureux, S.; Braunstein, M.; Oza, A.M. Epithelial ovarian cancer: Evolution of management in the era of precision medicine. CA Cancer J. Clin. 2019, 69, 280–304. [Google Scholar] [CrossRef]
- Tozzi, R.; Ferrari, F.; Nieuwstad, J.; Campanile, R.G.; Soleymani Majd, H. Tozzi classification of diaphragmatic surgery in patients with stage IIIC–IV ovarian cancer based on surgical findings and complexity. J. Gynecol. Oncol. 2020, 31, e14. [Google Scholar] [CrossRef]
- Ceccaroni, M.; Roviglione, G.; Bruni, F.; Clarizia, R.; Ruffo, G.; Salgarello, M.; Peiretti, M.; Uccella, S. Laparoscopy for primary cytoreduction with multivisceral resections in advanced ovarian cancer: Prospective validation. “The times they are a-changin”? Surg. Endosc. 2018, 32, 2026–2037. [Google Scholar] [CrossRef]
- Nagarsheth, N.P.; Rahaman, J.; Cohen, C.J.; Gretz, H.; Nezhat, F. The incidence of port-site metastases in gynecologic cancers. Jpn. Soc. Lang. Sci. 2004, 8, 133–139. [Google Scholar]
- Nitecki, R.; Rauh-Hain, J.A.; Melamed, A.; Scambia, G.; Pareja, R.; Coleman, R.L.; Ramirez, P.T.; Fagotti, A. Laparoscopic cytoreduction After Neoadjuvant ChEmotherapy (LANCE). Int. J. Gynecol. Cancer 2020, 30, 1450–1454. [Google Scholar] [CrossRef]
| Authors | Year | Country | Study Objective | Study Type | N | Intervention | Key Findings | Significant Oncologic Outcomes |
|---|---|---|---|---|---|---|---|---|
| Fagotti et al. [14] | 2005 | Italy | MIS vs. laparotomy in assessing the chance of optimal cytoreduction | Prospective | 61 | Laparoscopic assessment IDS | In the final model, a predictive index score > or =8 identified patients undergoing suboptimal surgery with a specificity of 100% | Not evaluated |
| Brun et al. [18] | 2008 | France | MIS vs. laparotomy in assessing the chance of optimal cytoreduction | Retrospective | 55 | Laparoscopic assessment PDS | The proposed laparoscopic 7 items score demonstrated a sensitivity, specificity, PPV, NPV, and accuracy of 46%, 89%, 89%, 44%, and 60% to predict resectability | Not evaluated |
| Fagotti et al. (Olympia-MITO13) [19] | 2013 | Italy | Role of MIS in assessing the chance of optimal cytoreduction | Prospective multicenter | 168 | Laparoscopic assessment PDS | The worst laparoscopic feature was mesenteric retraction; Cohen’s kappa and the p value for overall predictive index value were 0.685 and 0.01 | Not evaluated |
| Gueli Alletti et al. [20] | 2016 | Italy | Compare MIS vs. laparotomy | Retrospective case–control | 95 | Laparoscopic IDS | Less blood loss, shorter stay with MIS | Better PFS with Bevacizumab; OS comparable in MIS group |
| Gueli Alletti et al. (MISSION) [21] | 2016 | Italy | Feasibility of laparoscopic IDS | Prospective feasibility | 52 | Laparoscopic IDS | Minimal complications, high feasibility | Not evaluated |
| Vizzielli et al. [22] | 2016 | Italy | Laparoscopic score to predict major postoperative complications after PDS | Retrospective multicenter | 555 | Laparoscopic assessment PDS | High laparoscopic tumor load was a significant predictor | Not evaluated |
| Ackroyd et al. [23] | 2017 | USA | Feasibility of robotic IDS | Retrospective single-center | 29 | Robotic IDS | R0: 66%; shorter hospital stay | PFS: 21.2 mo; OS: 39.7 mo |
| Brown et al. [24] | 2019 | USA | Compare MIS and laparotomy | Retrospective comparative | 157 | Laparoscopic IDS | Higher R0 in MIS; shorter stay | R0 higher in MIS; OS/PFS not reported |
| Davidson et al. [25] | 2019 | Canada | Complexity score and survival outcomes | Retrospective multicenter | 282 | Laparoscopic IDS + complexity score | R0: 76%; higher complexity = worse DSS | R0: 76%; OS/PFS not reported |
| Fagotti et al. (INTERNATIONAL MISSION) [11] | 2019 | Italy | Evaluate MIS safety after NACT | Retrospective multicenter | 127 | Laparoscopic IDS | R0: 96.1%; major complications < 5% | PFS: 23 mo; OS at 5 yrs: 52% |
| Zhang et al. [26] | 2021 | China | Compare robotic and open surgery + impact of NACT cycles | Retrospective | 93 | Robotic IDS | R0: 63% vs. 52%; fewer complications in robotic group | PFS: 16.7 vs. 15.4 mo; OS: 35.6 vs. 38.2 mo |
| Morton et al. [27] | 2021 | USA | Compare MIS vs. open surgery + HIPEC | Retrospective | 50 | MIS IDS + HIPEC | R0: 70% vs. 77.5%; shorter stay with MIS | PFS: 15 (MIS) vs. 17.2 (open); OS not reported |
| Pomel et al. (CILOVE) [28] | 2021 | France | Feasibility of laparoscopic IDS in NACT responders | Prospective phase II | 48 | Laparoscopic IDS | R0: 97%; low conversion and complication rates | PFS: 87.5% at 12 months |
| Lecointre et al. [29] | 2022 | France | Compare MIS and laparotomy | Retrospective propensity-score-matched | 37 | Laparoscopic IDS | Less early postoperative complications (6 versus 17, p = 0.01) and shorter hospital stay (7.6 days versus 12.1, p < 0.001) in MIS | No difference in terms of OS and PFS |
| Lee et al. [30] | 2023 | Korea | MIS vs. CT to assess PDS feasibility | Retrospective | 614 | Laparoscopic assessment PDS | Lower rate of suboptimal cytoreduction and lower postoperative morbidity in MIS group | No difference in terms of OS and PFS |
| Ceccaroni et al. [13] | 2023 | Italy | Feasibility of MIS in IDS | Retrospective, single-center | 108 | Laparoscopic IDS, PDS | R0: ~95%; major complications < 10% | 3-yr OS: 66–84%; PFS not reported |
| Jorgensen et al. [31] | 2023 | USA | Compare MIS vs. laparotomy in IDS | Retrospective cohort | 7897 | Laparoscopic IDS | Shorter stay; lower 30- and 90-day mortality in MIS | OS: 35.9 vs. 37.4 mo (not significant) |
| Rauh-Hain et al. [32] | 2023 | International | Evaluate feasibility of RCT comparing MIS vs. open IDS after NAC | Randomized pilot trial | 100 | Laparoscopic IDS | R0: 88% (MIS) vs. 83% (open); conversion < 12.5%; better peri-op profile | OS/PFS not yet reported |
| Tozzi et al. (ULTRA-LAP) [12] | 2023 | Italy | Test safety, side effects and efficacy of laparoscopic Visceral-Peritoneal Debulking | Non-randomized prospective clinical trial | 208 | Laparoscopic IDS, PDS | Intra- and post-operative morbidity was very low in the MIS group. CR rate was 98% in MIS group and 94% in LPT group. | OS/PFS not yet reported |
| Uwins et al. (MIRRORS) [33] | 2024 | UK | Feasibility and safety of robotic IDS | Prospective cohort study | 24 | Robotic IDS | All patients achieved R < 1 (robotic R0 = 47.4%, open R0 = 0%). No patients had conversion to open | OS/PFS not yet reported |
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Ferrari, F.A.; Pavone, M.; Cuccu, I.; Ferrari, F.; Bogani, G.; Ceccaroni, M. Minimally Invasive Surgery in the Management of Advanced Epithelial Ovarian Cancer: A Comprehensive Analysis of Current Evidence and Clinical Applications. Medicina 2025, 61, 2201. https://doi.org/10.3390/medicina61122201
Ferrari FA, Pavone M, Cuccu I, Ferrari F, Bogani G, Ceccaroni M. Minimally Invasive Surgery in the Management of Advanced Epithelial Ovarian Cancer: A Comprehensive Analysis of Current Evidence and Clinical Applications. Medicina. 2025; 61(12):2201. https://doi.org/10.3390/medicina61122201
Chicago/Turabian StyleFerrari, Filippo Alberto, Matteo Pavone, Ilaria Cuccu, Federico Ferrari, Giorgio Bogani, and Marcello Ceccaroni. 2025. "Minimally Invasive Surgery in the Management of Advanced Epithelial Ovarian Cancer: A Comprehensive Analysis of Current Evidence and Clinical Applications" Medicina 61, no. 12: 2201. https://doi.org/10.3390/medicina61122201
APA StyleFerrari, F. A., Pavone, M., Cuccu, I., Ferrari, F., Bogani, G., & Ceccaroni, M. (2025). Minimally Invasive Surgery in the Management of Advanced Epithelial Ovarian Cancer: A Comprehensive Analysis of Current Evidence and Clinical Applications. Medicina, 61(12), 2201. https://doi.org/10.3390/medicina61122201

