What Is the Value of Lymphadenectomy in Early Ovarian Cancer?

  • Sven Mahner
  • Jacobus Pfisterer
  • Ganendra Raj K. Ali Mohan
  • Michael A. Quinn


A sizeable proportion of patients with seemingly early-stage ovarian cancer confined to the ovary will have their disease upstaged by lymphadenectomy, and this has obvious prognostic importance. Tumor grade and histology are important when considering this pattern of spread, but the evidence for a survival benefit for lymphadenectomy is scarce, there has been no uniform agreement on the extent of lymphadenectomy, and long-term follow-up of patients who have undergone systematic lymphadenectomy in this context is lacking including quality of life studies.


Ovarian Cancer Sentinel Node Biopsy Epithelial Ovarian Cancer Surgical Staging Systematic Lymphadenectomy 
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Part I

  1. 1.
    Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2009. CA Cancer J Clin. 2009;59:225–49.PubMedCrossRefGoogle Scholar
  2. 2.
    Trimbos B, Timmers P, Pecorelli S, et al. Surgical staging and treatment of early ovarian cancer: long-term analysis from a randomized trial. J Natl Cancer Inst. 2010;102:982–7.PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    du Bois A, Reuss A, Pujade-Lauraine E, et al. Role of surgical outcome as prognostic factor in advanced epithelial ovarian cancer: a combined exploratory analysis of 3 prospectively randomized phase 3 multicenter trials: by the Arbeitsgemeinschaft Gynaekologische Onkologie Studiengruppe Ovarialkarzinom (AGO-OVAR) and the Groupe d’Investigateurs Nationaux Pour les Etudes des Cancers de l’Ovaire (GINECO). Cancer. 2009;115:1234–44.PubMedCrossRefGoogle Scholar
  4. 4.
    du Bois A, Rochon J, Pfisterer J, et al. Variations in institutional infrastructure, physician specialization and experience, and outcome in ovarian cancer: a systematic review. Gynecol Oncol. 2009;112:422–36.PubMedCrossRefGoogle Scholar
  5. 5.
    Kommoss S, Harter P, Traut A, et al. Compliance to consensus recommendations, surgeon’s experience, and introduction of a quality assurance and management program: influence on therapy of early-stage ovarian carcinoma. Int J Gynecol Cancer. 2009;19:787–93.PubMedCrossRefGoogle Scholar
  6. 6.
    Young RC, Decker DG, Wharton JT, et al. Staging laparotomy in early ovarian cancer. JAMA. 1983;250:3072–6.PubMedCrossRefGoogle Scholar
  7. 7.
    Soper JT, Johnson P, Johnson V, et al. Comprehensive restaging laparotomy in women with apparent early ovarian carcinoma. Obstet Gynecol. 1992;80:949–53.PubMedGoogle Scholar
  8. 8.
    Cass I, Li AJ, Runowicz CD, et al. Pattern of lymph node metastases in clinically unilateral stage I invasive epithelial ovarian carcinomas. Gynecol Oncol. 2001;80:56–61.PubMedCrossRefGoogle Scholar
  9. 9.
    Benedetti-Panici P, Greggi S, Maneschi F, et al. Anatomical and pathological study of retroperitoneal nodes in epithelial ovarian cancer. Gynecol Oncol. 1993;51:150–4.PubMedCrossRefGoogle Scholar
  10. 10.
    Suzuki M, Ohwada M, Yamada T, et al. Lymph node metastasis in stage I epithelial ovarian cancer. Gynecol Oncol. 2000;79:305–8.PubMedCrossRefGoogle Scholar
  11. 11.
    Sakuragi N, Yamada H, Oikawa M, et al. Prognostic significance of lymph node metastasis and clear cell histology in ovarian carcinoma limited to the pelvis (pT1M0 and pT2M0). Gynecol Oncol. 2000;79:251–5.PubMedCrossRefGoogle Scholar
  12. 12.
    Morice P, Joulie F, Camatte S, et al. Lymph node involvement in epithelial ovarian cancer: analysis of 276 pelvic and paraaortic lymphadenectomies and surgical implications. J Am Coll Surg. 2003;197:198–205.PubMedCrossRefGoogle Scholar
  13. 13.
    Negishi H, Takeda M, Fujimoto T, et al. Lymphatic mapping and sentinel node identification as related to the primary sites of lymph node metastasis in early stage ovarian cancer. Gynecol Oncol. 2004;94:161–6.PubMedCrossRefGoogle Scholar
  14. 14.
    Takeshima N, Hirai Y, Umayahara K, et al. Lymph node metastasis in ovarian cancer: difference between serous and non-serous primary tumors. Gynecol Oncol. 2005;99:427–31.PubMedCrossRefGoogle Scholar
  15. 15.
    Maggioni A, Benedetti Panici P, Dell’Anna T, et al. Randomised study of systematic lymphadenectomy in patients with epithelial ovarian cancer macroscopically confined to the pelvis. Br J Cancer. 2006;95:699–704.PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Harter P, Gnauert K, Hils R, et al. Pattern and clinical predictors of lymph node metastases in epithelial ovarian cancer. Int J Gynecol Cancer. 2007;17:1238–44.PubMedCrossRefGoogle Scholar
  17. 17.
    Burghardt E, Girardi F, Lahousen M, et al. Patterns of pelvic and paraaortic lymph node involvement in ovarian cancer. Gynecol Oncol. 1991;40:103–6.PubMedCrossRefGoogle Scholar
  18. 18.
    Baiocchi G, Grosso G, di Re E, et al. Systematic pelvic and paraaortic lymphadenectomy at second-look laparotomy for ovarian cancer. Gynecol Oncol. 1998;69:151–6.PubMedCrossRefGoogle Scholar
  19. 19.
    Desteli GA, Gultekin M, Usubutun A, et al. Lymph node metastasis in grossly apparent clinical stage Ia epithelial ovarian cancer: Hacettepe experience and review of literature. World J Surg Oncol. 2010;8:106.PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Schmeler KM, Tao X, Frumovitz M, et al. Prevalence of lymph node metastasis in primary mucinous carcinoma of the ovary. Obstet Gynecol. 2010;116:269–73.PubMedCrossRefGoogle Scholar
  21. 21.
    Rouzier R, Bergzoll C, Brun JL, et al. The role of lymph node resection in ovarian cancer: analysis of the Surveillance, Epidemiology, and End Results (SEER) database. BJOG. 2010;117:1451–8.PubMedCrossRefGoogle Scholar
  22. 22.
    Nomura H, Tsuda H, Susumu N, et al. Lymph node metastasis in grossly apparent stages I and II epithelial ovarian cancer. Int J Gynecol Cancer. 2010;20:341–5.PubMedCrossRefGoogle Scholar
  23. 23.
    Takano M, Sugiyama T, Yaegashi N, et al. The impact of complete surgical staging upon survival in early-stage ovarian clear cell carcinoma: a multi-institutional retrospective study. Int J Gynecol Cancer. 2009;19:1353–7.PubMedCrossRefGoogle Scholar
  24. 24.
    Fournier M, Stoeckle E, Guyon F, et al. Lymph node involvement in epithelial ovarian cancer: sites and risk factors in a series of 355 patients. Int J Gynecol Cancer. 2009;19:1307–13.PubMedCrossRefGoogle Scholar
  25. 25.
    Hoskins WJ. Epithelial ovarian carcinoma: principles of primary surgery. Gynecol Oncol. 1994;55:S91–6.PubMedCrossRefGoogle Scholar
  26. 26.
    Trimbos JB, Bolis G. Guidelines for surgical staging of ovarian cancer. Obstet Gynecol Surv. 1994;49:814–6.PubMedCrossRefGoogle Scholar
  27. 27.
    Powless CA, Aletti GD, Bakkum-Gamez JN, et al. Risk factors for lymph node metastasis in apparent early-stage epithelial ovarian cancer: implications for surgical staging. Gynecol Oncol. 2011;122:536–40.PubMedCrossRefGoogle Scholar
  28. 28.
    Trimbos JB. Lymphadenectomy in ovarian cancer: standard of care or unnecessary risk. Curr Opin Oncol. 2011;23:507–11.PubMedCrossRefGoogle Scholar
  29. 29.
    du Bois A, Reuss A, Harter P, et al. Potential role of lymphadenectomy in advanced ovarian cancer: a combined exploratory analysis of three prospectively randomized phase III multicenter trials. J Clin Oncol. 2010;28:1733–9.PubMedCrossRefGoogle Scholar
  30. 30.
    Trimbos JB, Vergote I, Bolis G, et al. Impact of adjuvant chemotherapy and surgical staging in early-stage ovarian carcinoma: European Organisation for Research and Treatment of Cancer-Adjuvant ChemoTherapy in Ovarian Neoplasm trial. J Natl Cancer Inst. 2003;95:113–25.PubMedCrossRefGoogle Scholar
  31. 31.
    Zanetta G, Rota S, Chiari S, et al. The accuracy of staging: an important prognostic determinator in stage I ovarian carcinoma. A multivariate analysis. Ann Oncol. 1998;9:1097–101.PubMedCrossRefGoogle Scholar
  32. 32.
    Verleye L, Ottevanger PB, van der Graaf W, et al. EORTC-GCG process quality indicators for ovarian cancer surgery. Eur J Cancer. 2009;45:517–26.PubMedCrossRefGoogle Scholar
  33. 33.
    Timmers PJ, Zwinderman K, Coens C, et al. Lymph node sampling and taking of blind biopsies are important elements of the surgical staging of early ovarian cancer. Int J Gynecol Cancer. 2010;20:1142–7.PubMedCrossRefGoogle Scholar
  34. 34.
    Chan JK, Munro EG, Cheung MK, et al. Association of lymphadenectomy and survival in stage I ovarian cancer patients. Obstet Gynecol. 2007;109:12–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Skirnisdottir I, Sorbe B. Lymph node sampling is of prognostic value in early stage epithelial ovarian carcinoma. Eur J Gynaecol Oncol. 2005;26:181–5.PubMedGoogle Scholar
  36. 36.
    Carnino F, Fuda G, Ciccone G, et al. Significance of lymph node sampling in epithelial carcinoma of the ovary. Gynecol Oncol. 1997;65:467–72.PubMedCrossRefGoogle Scholar
  37. 37.
    Onda T, Yoshikawa H, Yokota H, et al. Assessment of metastases to aortic and pelvic lymph nodes in epithelial ovarian carcinoma. A proposal for essential sites for lymph node biopsy. Cancer. 1996;78:803–8.PubMedCrossRefGoogle Scholar

Part II

  1. 38.
    Calcagno M, Montera R, Cafa EV, Sereni MI, Panici PB, Angioli R, Plotti F, Palaia I. Update on lymphadenectomy in early and advanced ovarian cancer. Curr Opin Obstet Gynecol. 2008;20(1):34–9. Review.PubMedCrossRefGoogle Scholar
  2. 39.
    Rungruang B, Miller A, Richard SD, Hamilton CA, Rodriguez N, Bookman MA, Maxwell GL, Horowitz NS. Should stage IIIC ovarian cancer be further stratified by intraperitoneal vs. retroperitoneal only disease? A Gynecologic Oncology Group study. Gynecol Oncol. 2012;124(1):53–8. Epub 2011 Oct 26.PubMedCrossRefGoogle Scholar
  3. 40.
    Benedetti-Panici P, Maggioni A, Hacker N, Landoni F, Ackermann S, Campagnutta E, et al. Systematic aortic and pelvic lymphadenectomy versus resection of bulky nodes only in optimally debulked advanced ovarian cancer: a randomized clinical trial. J Natl Cancer Inst. 2005;97:560–6.CrossRefGoogle Scholar
  4. 41.
    Scarabelli C, Gallo A, Zarrelli A, Visentin C, Campagnutta E. Systematic pelvic and para-aortic lymphadenectomy during cytoreductive surgery in advanced ovarian cancer: potential benefit on survival. Gynecol Oncol. 1995;56(3):328–37.PubMedCrossRefGoogle Scholar
  5. 42.
    Maggioni A, Benedetti Panici P, Dell’Anna T, Landoni F, Lissoni A, Pellegrino A, et al. Randomised study of systematic lymphadenectomy in patients with epithelial ovarian cancer macroscopically confined to the pelvis. Br J Cancer. 2006;18:699–704.CrossRefGoogle Scholar
  6. 43.
    International Collaborative Ovarian Neoplasm (ICON1) Collaborators. International collaborative ovarian neoplasm trial 1 and adjuvant chemotherapy in ovarian neoplasm trial: two parallel randomized phase III trials of adjuvant chemotherapy in patients with early-stage ovarian carcinoma. J Natl Cancer Inst. 2003;95:105–12.CrossRefGoogle Scholar
  7. 44.
    Kleppe M, Wang T, Van Gorp T, Slangen BF, Kruse AJ, Kruitwagen RF. Lymph node metastasis in stages I and II ovarian cancer: a review. Gynecol Oncol. 2011;123(3):610–4. Epub 2011 Oct 6. Review.PubMedCrossRefGoogle Scholar
  8. 45.
    Satoh T, Hatae M, Watanabe Y, Yaegashi N, Ishiko O, Kodama S, et al. Outcomes of fertility-sparing surgery for stage I epithelial ovarian cancer: a proposal for patient selection. Clin Oncol. 2010;28(10):1727–32. Epub 2010 Mar 1. Erratum in: J Clin Oncol. 2011;29(35):4725.CrossRefGoogle Scholar
  9. 46.
    Uzan C, Morice P, Rey A, et al. Outcomes after combined therapy including surgical resection in patients with epithelial ovarian cancer recurrences exclusively in lymph nodes. Ann Surg Oncol. 2004;11:658–64.PubMedCrossRefGoogle Scholar
  10. 47.
    Benedetti Panici P, Perniola G, Angioli R, et al. Bulky lymph node resection in patients with recurrent epithelial ovarian cancer: impact of surgery. Int J Gynecol Cancer. 2007;17:1245–51.PubMedCrossRefGoogle Scholar
  11. 48.
    Bell J, Brady MF, Young RC, Lage J, Walker JL, Look KY, Rose GS, Spirtos NM, Gynecologic Oncology Group. Randomized phase III trial of three versus six cycles of adjuvant carboplatin and paclitaxel in early stage epithelial ovarian carcinoma: a Gynecologic Oncology Group study. Gynecol Oncol. 2006;102(3):432.PubMedCrossRefGoogle Scholar
  12. 49.
    Chan JK, Tian C, Fleming GF, Monk BJ, Herzog TJ, Kapp DS, Bell J. The potential benefit of 6 vs. 3 cycles of chemotherapy in subsets of women with early-stage high-risk epithelial ovarian cancer: an exploratory analysis of a Gynecologic Oncology Group study. Gynecol Oncol. 2010;116(3):301.PubMedCrossRefGoogle Scholar
  13. 50.
    Young RC, Walton LA, Ellenberg SS, Homesley HD, Wilbanks GD, Decker DG, Miller A, Park R, Major Jr F. Adjuvant therapy in stage I and stage II epithelial ovarian cancer. Results of two prospective randomized trials. N Engl J Med. 1990;322(15):1021.PubMedCrossRefGoogle Scholar
  14. 51.
    Kim HS, Ju W, Jee BC, Kim YB, Park NH, Song YS, Kim SC, Kang SB, Kim JW. Systematic lymphadenectomy for survival in epithelial ovarian cancer: a meta-analysis. Int J Gynecol Cancer. 2010;20(4):520–8.PubMedCrossRefGoogle Scholar
  15. 52.
    Berek JS. Lymph node-positive stage IIIC ovarian cancer: a separate entity? Int J Gynecol Cancer. 2009;19 Suppl 2:S18–20. Review.PubMedCrossRefGoogle Scholar
  16. 53.
    Dizon DS, Restivo A, Lomme M, Charbonneau N, Brard L, Hughes T, Weitzen S, Legare R, Granai CO, Disilvestro P. For women receiving chemotherapy for clinically apparent early ovarian cancer, is there a benefit to surgical staging? Am J Clin Oncol. 2008;31(1):39–42.PubMedCrossRefGoogle Scholar
  17. 54.
    Ayhan A, Celik H, Dursun P. Lymphatic mapping and sentinel node biopsy in gynecological cancers: a critical review of the literature. World J Surg Oncol. 2008;6:53.PubMedCentralPubMedCrossRefGoogle Scholar
  18. 55.
    Nyberg RH, Korkola P, Mäenpää J. Ovarian sentinel node: is it feasible? Int J Gynecol Cancer. 2011;21(3):568–72.PubMedCrossRefGoogle Scholar
  19. 56.
    Colomer AT, Jiménez AM, Bover Barceló MI. Laparoscopic treatment and staging of early ovarian cancer. J Minim Invasive Gynecol. 2008;15(4):414–9. Epub 2008 Jun 6.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London 2014

Authors and Affiliations

  • Sven Mahner
    • 1
  • Jacobus Pfisterer
    • 2
  • Ganendra Raj K. Ali Mohan
    • 3
  • Michael A. Quinn
    • 4
  1. 1.Gynecology and Gynecologic OncologyUniversity Medical Center Hamburg-EppendorfHamburgGermany
  2. 2.Gynecologic Cancer CenterKielGermany
  3. 3.Gynaecology OncologyKing Edward Memorial HospitalPerthAustralia
  4. 4.The University of Melbourne, Royal Women’s HospitalMelbourneAustralia

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