Peritoneal Carcinomatosis of Rare Ovarian Origin Treated by Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy: A Multi-Institutional Cohort from PSOGI and BIG-RENAPE

  • Frédéric Mercier
  • Naoual Bakrin
  • David L. Bartlett
  • Diane Goere
  • François Quenet
  • Frédéric Dumont
  • Bruno Heyd
  • Karine Abboud
  • Christelle Marolho
  • Laurent Villeneuve
  • Olivier Glehen
  • the PSOGI Working Group
  • the BIG-RENAPE Working Group
Gynecologic Oncology

Abstract

Purpose

Ovarian cancer is the most common deadly cancer of gynecologic origin. Patients often are diagnosed at advanced stage with peritoneal metastasis. There are many rare histologies of ovarian cancer; some have outcomes worse than serous ovarian cancer. Cytoreductive surgery (CRS) and hyperthermic intraperitoneal chemotherapy (HIPEC) can be considered for patients with recurrence. This study was designed to assess the impact of CRS and HIPEC on survival of patient with peritoneal metastasis from rare ovarian malignancy.

Methods

A prospective, multicentric, international database was retrospectively searched to identify all patients with rare ovarian tumor (mucinous, clear cells, endometrioid, small cell hypercalcemic, and other) and peritoneal metastasis who underwent CRS and HIPEC through the Peritoneal Surface Oncology Group International (PSOGI) and BIG-RENAPE working group. The postoperative complications, long-term results, and principal prognostic factors were analyzed.

Results

The analysis included 210 patients with a median follow-up of 43.5 months. Median overall survival (OS) was 69.3 months, and the 5-year OS was 57.7%. For mucinous tumors, median OS and DFS were not reached at 5 years. For granulosa tumors, median overall survival was not reached at 5 years, and median DFS was 34.6 months. Teratoma or germinal tumor showed median overall survival and DFS that were not reached at 5 years. Differences in OS were not statistically significant between histologies (p = 0.383), whereas differences in DFS were (p < 0.001).

Conclusions

CRS and HIPEC may increases long-term survival in selected patients with peritoneal metastasis from rare ovarian tumors especially in mucinous, granulosa, or teratoma histological subtypes.

Notes

Acknowledgment

The authors thank Peggy Jourdan-Enfer and Anaïs Poulet for their help with data collection.

Disclosure

The authors report no conflicts of interest relevant to this article.

Collaborators

The collaborators of the BIG-RENAPE Working Group include the following: J. Abba (Department of Surgical Oncology, CHU Grenoble University, Grenoble, France); C. Arvieux (Department of Surgical Oncology, CHU Grenoble University, Grenoble, France); J-M. Bereder (Department of Surgical Oncology, CHU L’Archet 2, Nice, France); D. Bouzard (Department of Surgical Oncology, CHU Louis Mourier, Colombes, France); C. Brigand (Department of Surgical Oncology, CHRU Hautepierre, Strasbourg, France); S. Carrère (Department of Surgical Oncology, Institut du Cancer de Montpellier, Montpellier, France); C. Eveno (Department of Surgical Oncology, CHU Lariboisière, Paris, France); O. Facy (Department of Surgical Oncology, CHU Dijon, Dijon, France); G. Ferron (Department of Surgical Oncology, IUCT Oncopole, Toulouse, France); F. Guyon (Department of Surgical Oncology, Institut Bergonié, Bordeaux, France); R. Kianmanesh (Department of Surgical Oncology, CHU Robert Debré, Reims, France); R. Lo Dico (Department of Surgical Oncology, CHU Lariboisière, Paris, France); G. Lorimier (Department of Surgical Oncology, ICO-Paul Papin, Angers, France); F. Marchal (Department of Surgical Oncology, Institut de Cancérologie de Lorraine, Vandoeuvre-lès-Nancy, France); P. Mariani (Department of Surgical Oncology, Institut Curie, Paris, France); P. Meeus (Department of Surgical Oncology, Centre Léon Bérard, Lyon, France); S. Msika (Department of Surgical Oncology, CHU Louis Mourier, Colombes, France); P. Ortega-Deballon (Department of Surgical Oncology, CHU Dijon, Dijon, France); B. Paquette (Department of Digestive Surgery, Minjoz University Hospital, Besançon, France); N. Pirro (Department of Surgical Oncology, CHU La Timône, Marseille, France); M. Pocard (Department of Surgical Oncology, CHU Lariboisière, Paris, France); P. Rat (Department of Surgical Oncology, CHU Dijon, Dijon, France); O. Sgarbura (Department of Surgical Oncology, Institut du Cancer de Montpellier, Montpellier, France); E. Thibaudeau (Department of Surgical Oncology, ICO–René Gauducheau, St Herblain, France); F. Zinzindohoue (Department of Surgical Oncology, Hôpital Européen Georges Pompidou, Paris, France).

The collaborators of the PSOGI Working Group included the following: S. A. Ahrendt (Department of Surgical Oncology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA); E. Akaishi (Department of Surgical Oncology, Centro de Oncologia Hospital Sirio Libanes, Sao Paulo, Brazil); A. Bhatt (Department of Surgical Oncology, Fortis Hospitals Limited, Bangalore, India); P. Cachin (Department of Surgery, Akademiska sjukhuset, Uppsala University Hospital, Uppasala, Sweden); W. Ceelen (Department of Gastrointestinal Surgery, Gent University Hospital, Ghent, Belgium); R. P. Edwards (Department of Surgical Oncology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA); M. P. Holtzman (Department of Surgical Oncology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA); D. Kecmanovic (Department of Surgery, First Surgical Clinic, Clinical Center of Serbia, Belgrade, Serbia); K. W. Lee (Department of Surgical Oncology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA); E. A. Levine (Department of Surgical Sciences-Oncology, Wake Forest Baptist Medical Center, Winston Salem, USA); S. Mehta (Division of Peritoneal Surface Oncology, Saifee Hospital, Mumbai, India); D. L. Morris (Department of Surgery, University of New South Wales, Sidney, Australia); P. K. Pande (Department of Surgical Oncology, BLK Superspeciality Hospital, New Delhi, India); P. Piso (Department of Surgery, University of Regensburg, Regensburg, Germany); S. O’Dwyer (Department of Colorectal Surgery, Christie Cancer Center, Manchester, United Kingdom); J. F. Pingpank (Department of Surgical Oncology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA); F. Rajan (Department of Surgical Oncology, Kovai Medical Centre, Coimbatore, India); B. Rau (Department of Surgical Oncology, Charite Campus Mitte University of Berlin, Berlin, Germany); J. Spiliotis (First Department of Surgical Oncology, Metaxa Cancer Memorial Hospital, Piraeus, Greece); P. Sugarbaker (Department of Surgical Oncology, Washington Hospital Center, United States); M. Teo (Department of Surgical Oncology, National Cancer Centre Singapore, Singapore, Singapore); R. Yarema (Department of Oncology and Medical Radiology Danylo Halytsky Lviv National Medical University, Lviv, Ukraine); Y. Yonemura (Department of Surgical Oncology, Organization to Support Peritoneal Dissemination Treatment, Osaka, Japan); H. J. Zeh (Department of Surgical Oncology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA).

Supplementary material

10434_2018_6464_MOESM1_ESM.pptx (56 kb)
Supplementary material 1 (PPTX 55 kb)
10434_2018_6464_MOESM2_ESM.docx (77 kb)
Supplementary material 2 (DOCX 76 kb)

References

  1. 1.
    Neijt JP. New therapy for ovarian cancer. N Engl J Med. 1996;334:50–1.CrossRefPubMedGoogle Scholar
  2. 2.
    Bhatt A, Glehen O. The role of cytoreductive surgery and hyperthermic intraperitoneal chemotherapy (HIPEC) in ovarian cancer: a review. Indian J Surg Oncol. 2016;7(2):188–97.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Sehouli J, Senyuva F, Fotopoulou C, Neumann U, Denkert C,Werner L, Gülten O. Intra-abdominal tumor dissemination pattern and surgical outcome in 214 patients with primary ovarian cancer. J Surg Oncol. 2009;99(7):424–7.CrossRefPubMedGoogle Scholar
  4. 4.
    Bamias A, Psaltopoulou T, Sotiropoulou M et al. Mucinous but not clear cell histology is associated with inferior survival in patients with advanced stage ovarian carcinoma treated with platinum-paclitaxel chemotherapy. Cancer. 2010;116:1462–8.CrossRefPubMedGoogle Scholar
  5. 5.
    Fung-Kee-Fung M, Oliver T, Elit L, et al. Optimal chemotherapy treatment for women with recurrent ovarian cancer. Curr Oncol. 2007;14:195–208.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Winter WE III, Maxwell GL, Tian C, et al. Prognostic factors for stage III epithelial ovarian cancer: a Gynecologic Oncology Group Study. J Clin Oncol. 2007;25:3621–7.CrossRefPubMedGoogle Scholar
  7. 7.
    Efstathoiou E, Dimopoulos MA, Bozas G, et al. Advanced epithelial ovarian cancer in the elderly. Anticancer Res. 2007;27:611–7.Google Scholar
  8. 8.
    Pectasides D, Fountzilas G, Aravantinos G, et al. Advanced stage clear-cell epithelial ovarian cancer: the Hellenic Cooperative Oncology Group experience. Gynecol Oncol. 2006;102:285–91.CrossRefPubMedGoogle Scholar
  9. 9.
    Itamochi H, Kigawa J, Terakawa N. Mechanisms of chemoresistance and poor prognosis in ovarian clear cell carcinoma. Cancer Sci. 2008;99:653–8.CrossRefPubMedGoogle Scholar
  10. 10.
    Witkowski L, Goudie C, Foulkes WD and McCluggage GW. Small-cell carcinoma of the ovary of hypercalcemic type (malignant rhabdoid tumor of the ovary) a review with recent developments on pathogenesis. Surg Pathol. 2016;9:215–26.CrossRefGoogle Scholar
  11. 11.
    Huo YR, Richards A, Liauw W, Morris DL. Hyperthermic intraperitoneal chemotherapy (HIPEC) and cytoreductive surgery (CRS) in ovarian cancer: a systematic review and meta-analysis. Eur J Surg Oncol. 2015;41(12):1578–89.CrossRefPubMedGoogle Scholar
  12. 12.
    Jacquet P, Sugarbaker PH. Current methodologies for clinical assessment of patients with peritoneal carcinomatosis. J Exp Clin Cancer Res. 1996;15:49–58.Google Scholar
  13. 13.
    Jacquet P, Sugarbaker PH. Clinical research methodologies in diagnosis and staging of patients with peritoneal carcinomatosis. Cancer Treat Res. 1996;82:359–74.CrossRefPubMedGoogle Scholar
  14. 14.
    Glehen O, Mohammed F, Gilly FN. Peritoneal carcinomatosis from digestive tract cancer: new management by cytoreductive surgery and intraperitoneal chemohyperthermia. Lancet Oncol. 2004;5(4):219–28.CrossRefPubMedGoogle Scholar
  15. 15.
    Common Terminology Criteria for Adverse Events (CTCAE) Version 4.0. https://www.evs.nci.nih.gov/ftp1/CTCAE/CTCAE_4.03_2010-06-14.
  16. 16.
    Bristow RE, Tomacruz RS, Armstrong DK, et al. Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis. J Clin Oncol. 2002;20:1248–59.CrossRefPubMedGoogle Scholar
  17. 17.
    Thigpen T. The if and when of surgical debulking for ovarian carcinoma. N Engl J Med. 2004;351:2544–6.CrossRefPubMedGoogle Scholar
  18. 18.
    Amate P, Huchon C, Dessapt AL, et al. Ovarian cancer: sites of recurrence. Int J Gynecol Cancer. 2013;23(9):1590–6.CrossRefPubMedGoogle Scholar
  19. 19.
    Harter P, du Bois A, Hahmann M, et al. Surgery in recurrent ovarian cancer: the arbeitsgemeinschaft gynaekologische onkologie (AGO) DESKTOP OVAR trial. Ann Surg Oncol. 2006;13(12):1702–10.CrossRefPubMedGoogle Scholar
  20. 20.
    Bristow RE, Chi DS. Platinum-based neoadjuvant chemotherapy and interval surgical cytoreduction for advanced ovarian cancer: a meta-analysis. Gynecol Oncol. 2006;103(3):1070–6.CrossRefPubMedGoogle Scholar
  21. 21.
    Prat J. Staging classification for the cancer of the ovary, fallopian tube and peritoneum. Int J Gynaecol Obstet. 2014;124:1–5.CrossRefPubMedGoogle Scholar
  22. 22.
    Harter P, Sehouli J, Lorusso D, et al. LION: lymphadenectomy in ovarian neoplasms-A prospective randomized AGO study group led gynecologic cancer intergroup trial. J Clin Oncol. 2017;35:5500.Google Scholar
  23. 23.
    Baumgartner JM, Tobin L, Heavey SF, et al. Predictors of progression in high-grade appendiceal or colorectal peritoneal carcinomatosis after cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Ann Surg Oncol. 2015;22(5):1716–21.CrossRefPubMedGoogle Scholar
  24. 24.
    El Halabi H, Gushchin V, Francis J, et al. The role of cytoredcutive surgery and heated intraperitoneal chemotherapy (CRS/HIPEC) in patients with high-grade appendiceal carcinoma and extensive peritoneal carcinomatosis. Ann Surg Oncol. 2012;19(1):110–4.CrossRefPubMedGoogle Scholar
  25. 25.
    Miner TJ, Shia J, Jacques DP, et al. Long-term survival following treatment of pseudomyxoma peritonei: an analysis of surgical therapy. Ann Surg. 2005;241:300–8.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Bakrin N, Bereder JM, Decullier E, Classe JM, et al. Peritoneal carcinomatosis treated with cytoreductive surgery and Hyperthermic Intraperitoneal Chemotherapy (HIPEC) for advanced ovarian carcinoma: a French multicentre retrospective cohort study of 566 patients. Eur J Surg Oncol. 2013;39(12):1435–43.CrossRefPubMedGoogle Scholar
  27. 27.
    Lee YY, et al. Prognosis of ovarian clear cell carcinoma compared to other histological subtypes: a meta-analysis. Gynecol Oncol. 2011;122(3):541–7.CrossRefPubMedGoogle Scholar
  28. 28.
    Davis M, Rauh-Hain JA, Andrade C, et al. Comparison of clinical outcomes of patients with clear cell and endometrioid ovarian cancer associated with endometriosis to papillary serous carcinoma of the ovary. Gynecol Oncol. 2014;132:760–6.CrossRefPubMedGoogle Scholar
  29. 29.
    Hayes-Jordan A, Lopez C, Green HL et al. Cytoreductive surgery (CRS) and hyperthermic intraperitoneal chemotherapy (HIPEC) in pediatric ovarian tumors: a novel treatment approach. Pediatr Surg Int. 2016;32(1):71–3.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Pectasides D, Fountzilas G, Aravantinos G, et al. Advanced stage mucinous epithelial ovarian cancer: the Hellenic cooperative oncology group experience. Gynecol Oncol. 2005;97:436–41.CrossRefPubMedGoogle Scholar
  31. 31.
    Schiavone MB, Herzog TJ, Lewin SN, et al. Natural history and outcome of mucinous carcinoma of the ovary. Am J Obstet Gynecol. 2011;205:480.e1–8.Google Scholar
  32. 32.
    Chan JK, Zhang M, Kaleb V, et al. Prognostic factors responsible for survival in sex cord stromal tumor of the ovary: a multivariate analysis. Gynecol Oncol. 2005;96:204–9.CrossRefPubMedGoogle Scholar
  33. 33.
    Seagle BL, Ann P, Butler S, Shahabi S. Ovarian granulosa cell tumor: a National Cancer Database study. Gynecol Oncol. 2017;146(2):285–91.CrossRefPubMedGoogle Scholar
  34. 34.
    Gouy S, Uzan C, Pautier P et al. Results of oxaliplatin-based hyperthermic intraperitoneal chemotherapy in recurrent ovarian granulosa cell tumors. Eur J Obstet Gynecol Reprod Biol. 2013;170(2):464–7.CrossRefPubMedGoogle Scholar
  35. 35.
    Al-Badawi IA, Abu-Zaid A, Azzam A, et al. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for management for recurrent/relapsed ovarian granulosa cell tumor: a single center experience. J Obstet Gynaecol Res. 2014;40(9):2066–75.CrossRefPubMedGoogle Scholar
  36. 36.
    Pashankar F, Hale JP, Dang H, et al. Is adjuvant chemotherapy indicated in ovarian immature teratoma? A combined data analysis from the malignant germ cell tumor international collaborative. Cancer. 2016;122(2):230–7.CrossRefPubMedGoogle Scholar
  37. 37.
    Poujade O, Uzan C, Gouy S, et al. Primary psammocarcinoma of the ovary or peritoneum. Int J Gynecol Cancer. 2009;19(5):844–6.CrossRefPubMedGoogle Scholar
  38. 38.
    WItkowski L, Goudie C, Foulkes WD, McCluggage WG. Small-cell carcinoma of the ovary of hypercalcemic type (malignant rhabdoid tumor of the ovary): a review with recent development on pathogenesis. Surg Pathol Clin. 2016;9:215–26.Google Scholar
  39. 39.
    Chua TC, Moran BJ, Sugarbaker PH, et al. Early and long-term outcome data of patients with pseudomyxoma peritonei from appendiceal origin treated by a strategy of cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. J Clin Oncol. 2012;30(20):2449–56.CrossRefPubMedGoogle Scholar
  40. 40.
    Armstrong DK, Bundy B, Wenzel L, et al. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. N Engl J Med. 2006;354:34–43.CrossRefPubMedGoogle Scholar
  41. 41.
    Walker JL, Brady MF, DiSilvestro PA, et al. A phase III trial of bevacizumab with IV versus IP chemotherapy in ovarian, fallopian tube, and peritoneal carcinoma NCI-supplied agent(s): A GOG/NRG trial (GOG 252). 2016 Society of Gynecologic Oncology Annual Meeting. Late-breaking abstract 6. Presented March 21, 2016.Google Scholar
  42. 42.
    Van Driel, WJ, Koole SN, Sikorska K, et al. Hyperthermic intraperitoneal chemotherapy in ovarian cancer. N Eng J Med. 2018;378:230–40.CrossRefGoogle Scholar
  43. 43.
    Passot G, Vaudoyer D, Villeneuve L, et al. What made hyperthermic intraperitnoeal chemotherapy an effective curative treatment for peritoneal surface malignancy: a 25-year experience with 1125 procedures. J Surg Oncol. 2016;113:796–803.CrossRefPubMedGoogle Scholar

Copyright information

© Society of Surgical Oncology 2018

Authors and Affiliations

  • Frédéric Mercier
    • 1
  • Naoual Bakrin
    • 1
    • 2
  • David L. Bartlett
    • 3
  • Diane Goere
    • 4
  • François Quenet
    • 5
  • Frédéric Dumont
    • 6
  • Bruno Heyd
    • 7
  • Karine Abboud
    • 8
  • Christelle Marolho
    • 9
  • Laurent Villeneuve
    • 2
    • 9
  • Olivier Glehen
    • 1
    • 2
  • the PSOGI Working Group
  • the BIG-RENAPE Working Group
  1. 1.Department of Surgical OncologyCentre Hospitalier Lyon SudPierre-BéniteFrance
  2. 2.EMR 3738, Lyon 1 UniversityLyonFrance
  3. 3.Department of Surgical OncologyUniversity of Pittsburgh School of MedicinePittsburghUSA
  4. 4.Department of Surgical OncologyGustave RoussyVillejuif CedexFrance
  5. 5.Department of SurgeryInstitut Du Cancer de MontpellierMontpellierFrance
  6. 6.Department of Surgical OncologyICO René Gauducheau Cancer CenterSaint-HerblainFrance
  7. 7.Department of Digestive SurgeryMinjoz University HospitalBesançonFrance
  8. 8.Department of General SurgerySt Etienne University HospitalSaint-ÉtienneFrance
  9. 9.Unité de Recherche CliniqueHospices Civils de Lyon, Pôle Information Médicale Evaluation RechercheLyonFrance

Personalised recommendations