Uterine Cancer pp 207-221 | Cite as

The Role of Lymphadenectomy in Endometrial Cancer: The Mayo Clinic Experience

  • Mariam M. Al Hilli
  • Sean C. Dowdy


While endometrial cancer (EC) is the most common gynecologic malignancy in the USA, it is the second most common gynecologic malignancy after cervical cancer worldwide and has been responsible for an increasing percentage of cancer deaths in recent years [1, 2]. There is poor consensus on the extent of surgery needed to treat patients with EC who have no evidence of extrauterine spread. Total abdominal hysterectomy and bilateral salpingo-oophorectomy has been the cornerstone of surgical treatment, while the addition of lymph node evaluation varies according to surgeon and institutional preferences. Comprehensive surgical staging has been traditionally utilized in only 30–40 % of EC patients in the USA [4]. In comparison, lymphadenectomy is performed infrequently in some European countries in women with stage I EC.


Endometrial Cancer Myometrial Invasion Paraaortic Lymph Node Endometrial Cancer Patient Deep Myometrial Invasion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.CrossRefPubMedGoogle Scholar
  2. 2.
    Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin. 2012;62:10–29.CrossRefPubMedGoogle Scholar
  3. 3.
    Bakkum-Gamez JN, Gonzalez-Bosquet J, Laack NN, Mariani A, Dowdy SC. Current issues in the management of endometrial cancer. Mayo Clin Proc. 2008;83:97–112.CrossRefPubMedGoogle Scholar
  4. 4.
    Chan JK, Kapp DS. Role of complete lymphadenectomy in endometrioid uterine cancer. Lancet Oncol. 2007;8:831–41.CrossRefPubMedGoogle Scholar
  5. 5.
    Kitchener H, Swart AM, Qian Q, Amos C, Parmar MK. Efficacy of systematic pelvic lymphadenectomy in endometrial cancer (MRC ASTEC trial): a randomised study. Lancet. 2009;373:125–36.CrossRefPubMedGoogle Scholar
  6. 6.
    Creutzberg CL, van Putten WL, Koper PC, Lybeert ML, Jobsen JJ, Warlam-Rodenhuis CC, et al. Surgery and postoperative radiotherapy versus surgery alone for patients with stage-1 endometrial carcinoma: multicentre randomised trial. PORTEC study group. Post operative radiation therapy in endometrial carcinoma. Lancet. 2000;355:1404–11.CrossRefPubMedGoogle Scholar
  7. 7.
    Nout RA, Smit VT, Putter H, Jurgenliemk-Schulz IM, Jobsen JJ, Lutgens LC, et al. Vaginal brachytherapy versus pelvic external beam radiotherapy for patients with endometrial cancer of high-intermediate risk (PORTEC-2): an open-label, non-inferiority, randomised trial. Lancet. 2010;375:816–23.CrossRefPubMedGoogle Scholar
  8. 8.
    Creasman WT, Odicino F, Maisonneuve P, Quinn MA, Beller U, Benedet JL, et al. Carcinoma of the corpus uteri. FIGO 26th annual report on the results of treatment in gynecological cancer. Int J Gynaecol Obstet. 2006;95 Suppl 1:S105–43.CrossRefPubMedGoogle Scholar
  9. 9.
    Gray LA. Lymph node excision in the treatment of gynecologic malignancies. Am J Surg. 1964;108:660–3.CrossRefPubMedGoogle Scholar
  10. 10.
    Creasman WT, Odicino F, Maisonneuve P, Beller U, Benedet JL, Heintz AP, et al. Carcinoma of the corpus uteri. J Epidemiol Biostat. 2001;6:47–86.PubMedGoogle Scholar
  11. 11.
    Boronow RC, Morrow CP, Creasman WT, Disaia PJ, Silverberg SG, Miller A, et al. Surgical staging in endometrial cancer: clinical-pathologic findings of a prospective study. Obstet Gynecol. 1984;63:825–32.PubMedGoogle Scholar
  12. 12.
    Kehoe SM, Miller DS. The role of lymphadenectomy in endometrial cancer. Clin Obstet Gynecol. 2011;54:235–44.CrossRefPubMedGoogle Scholar
  13. 13.
    Soliman PT, Frumovitz M, Spannuth W, Greer MJ, Sharma S, Schmeler KM, et al. Lymphadenectomy during endometrial cancer staging: practice patterns among gynecologic oncologists. Gynecol Oncol. 2010;119:291–4.PubMedCentralCrossRefPubMedGoogle Scholar
  14. 14.
    Mariani A, Webb MJ, Keeney GL, Haddock MG, Calori G, Podratz KC. Low-risk corpus cancer: is lymphadenectomy or radiotherapy necessary? Am J Obstet Gynecol. 2000;182:1506–19.CrossRefPubMedGoogle Scholar
  15. 15.
    Mariani A, Dowdy SC, Cliby WA, Gostout BS, Jones MB, Wilson TO, et al. Prospective assessment of lymphatic dissemination in endometrial cancer: a paradigm shift in surgical staging. Gynecol Oncol. 2008;109:11–8.PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    Dowdy SC, Borah BJ, Bakkum-Gamez JN, Weaver AL, McGree ME, Haas LR, et al. Prospective assessment of survival, morbidity, and cost associated with lymphadenectomy in low-risk endometrial cancer. Gynecol Oncol. 2012;127:5–10.CrossRefPubMedGoogle Scholar
  17. 17.
    Dowdy SC, Borah BJ, Bakkum-Gamez JN, Kumar S, Weaver AL, McGree ME, et al. Factors predictive of postoperative morbidity and cost in patients with endometrial cancer. Obstet Gynecol. 2012;120:1419–27.PubMedGoogle Scholar
  18. 18.
    Mariani A, Dowdy SC, Keeney GL, Long HJ, Lesnick TG, Podratz KC. High-risk endometrial cancer subgroups: candidates for target-based adjuvant therapy. Gynecol Oncol. 2004;95:120–6.CrossRefPubMedGoogle Scholar
  19. 19.
    Mariani A, Webb MJ, Keeney GL, Haddock MG, Aletti G, Podratz KC. Stage IIIC endometrioid corpus cancer includes distinct subgroups. Gynecol Oncol. 2002;87:112–7.CrossRefPubMedGoogle Scholar
  20. 20.
    Mariani A, Webb MJ, Keeney GL, Calori G, Podratz KC. Hematogenous dissemination in corpus cancer. Gynecol Oncol. 2001;80:233–8.CrossRefPubMedGoogle Scholar
  21. 21.
    Mariani A, Dowdy SC, Keeney GL, Haddock MG, Lesnick TG, Podratz KC. Predictors of vaginal relapse in stage I endometrial cancer. Gynecol Oncol. 2005;97:820–7.CrossRefPubMedGoogle Scholar
  22. 22.
    Mariani A, Webb MJ, Keeney GL, Aletti G, Podratz KC. Endometrial cancer: predictors of peritoneal failure. Gynecol Oncol. 2003;89:236–42.CrossRefPubMedGoogle Scholar
  23. 23.
    Mariani A, Webb MJ, Keeney GL, Podratz KC. Routes of lymphatic spread: a study of 112 consecutive patients with endometrial cancer. Gynecol Oncol. 2001;81:100–4.CrossRefPubMedGoogle Scholar
  24. 24.
    Mariani A, Webb MJ, Keeney GL, Aletti G, Podratz KC. Predictors of lymphatic failure in endometrial cancer. Gynecol Oncol. 2002;84:437–42.CrossRefPubMedGoogle Scholar
  25. 25.
    Hirahatake K, Hareyama H, Sakuragi N, Nishiya M, Makinoda S, Fujimoto S. A clinical and pathologic study on para-aortic lymph node metastasis in endometrial carcinoma. J Surg Oncol. 1997;65:82–7.CrossRefPubMedGoogle Scholar
  26. 26.
    Lecuru F, Neji K, Robin F, Darles C, de Bievre P, Taurelle R. Lymphatic drainage of the uterus. Preliminary results of an experimental study. J Gynecol Obstet Biol Reprod (Paris). 1997;26:418–23.Google Scholar
  27. 27.
    Burke TW, Levenback C, Tornos C, Morris M, Wharton JT, Gershenson DM. Intraabdominal lymphatic mapping to direct selective pelvic and paraaortic lymphadenectomy in women with high-risk endometrial cancer: results of a pilot study. Gynecol Oncol. 1996;62:169–73.CrossRefPubMedGoogle Scholar
  28. 28.
    Morrow CP, Bundy BN, Kurman RJ, Creasman WT, Heller P, Homesley HD, et al. Relationship between surgical pathological risk-factors and outcome in clinical stage-I and stage-Ii carcinoma of the endometrium – a Gynecologic Oncology Group-study. Gynecol Oncol. 1991;40:55–65.CrossRefPubMedGoogle Scholar
  29. 29.
    Mariani A, Keeney GL, Aletti G, Webb MJ, Haddock MG, Podratz KC. Endometrial carcinoma: paraaortic dissemination. Gynecol Oncol. 2004;92:833–8.CrossRefPubMedGoogle Scholar
  30. 30.
    Todo Y, Suzuki Y, Azuma M, Hatanaka Y, Konno Y, Watari H, et al. Ultrastaging of para-aortic lymph nodes in stage IIIC1 endometrial cancer: a preliminary report. Gynecol Oncol. 2012;127:532–7.CrossRefPubMedGoogle Scholar
  31. 31.
    Todo Y, Okamoto K, Hayashi M, Minobe S, Nomura E, Hareyama H, et al. A validation study of a scoring system to estimate the risk of lymph node metastasis for patients with endometrial cancer for tailoring the indication of lymphadenectomy. Gynecol Oncol. 2007;104:623–8.CrossRefPubMedGoogle Scholar
  32. 32.
    Chi DS, Barakat RR, Palayekar MJ, Levine DA, Sonoda Y, Alektiar K, et al. The incidence of pelvic lymph node metastasis by FIGO staging for patients with adequately surgically staged endometrial adenocarcinoma of endometrioid histology. Int J Gynecol Cancer. 2008;18:269–73.CrossRefPubMedGoogle Scholar
  33. 33.
    Creasman WT, Morrow CP, Bundy BN, Homesley HD, Graham JE, Heller PB. Surgical pathologic spread patterns of endometrial cancer. A Gynecologic Oncology Group study. Cancer. 1987;60:2035–41.CrossRefPubMedGoogle Scholar
  34. 34.
    Schink JC, Rademaker AW, Miller DS, Lurain JR. Tumor size in endometrial cancer. Cancer. 1991;67:2791–4.CrossRefPubMedGoogle Scholar
  35. 35.
    Alhilli MM, Podratz KC, Dowdy SC, Bakkum-Gamez JN, Weaver AL, McGree ME, et al. Preoperative biopsy and intraoperative tumor diameter predict lymph node dissemination in endometrial cancer. Gynecol Oncol. 2013;128(2):294–9. doi:  10.1016/j.ygyno.2012.10.009. Epub 2012/10/17.
  36. 36.
    Kumar S, Medeiros F, Dowdy SC, Keeney GL, Bakkum-Gamez JN, Podratz KC, et al. A prospective assessment of the reliability of frozen section to direct intraoperative decision making in endometrial cancer. Gynecol Oncol. 2012;127:525–31.CrossRefPubMedGoogle Scholar
  37. 37.
    Chan JK, Cheung MK, Huh WK, Osann K, Husain A, Teng NN, et al. Therapeutic role of lymph node resection in endometrioid corpus cancer: a study of 12,333 patients. Cancer. 2006;107:1823–30.CrossRefPubMedGoogle Scholar
  38. 38.
    Abu-Rustum NR, Iasonos A, Zhou Q, Oke E, Soslow RA, Alektiar KM, et al. Is there a therapeutic impact to regional lymphadenectomy in the surgical treatment of endometrial carcinoma? Am J Obstet Gynecol. 2008;198(4):457.e1-5; discussion 457.e5-6. doi:  10.1016/j.ajog.2008.01.010.
  39. 39.
    Lutman CV, Havrilesky LJ, Cragun JM, Secord AA, Calingaert B, Berchuck A, et al. Pelvic lymph node count is an important prognostic variable for FIGO stage I and II endometrial carcinoma with high-risk histology. Gynecol Oncol. 2006;102:92–7.CrossRefPubMedGoogle Scholar
  40. 40.
    Fujimoto T, Tanaka T. Evaluation of the efficacy of systematic pelvic lymphadenectomy in endometrial cancer. Future Oncol. 2009;5:459–63.CrossRefPubMedGoogle Scholar
  41. 41.
    Fujimoto T, Nanjyo H, Nakamura A, Yokoyama Y, Takano T, Shoji T, et al. Para-aortic lymphadenectomy may improve disease-related survival in patients with multipositive pelvic lymph node stage IIIc endometrial cancer. Gynecol Oncol. 2007;107:253–9.CrossRefPubMedGoogle Scholar
  42. 42.
    Bakkum-Gamez JN, Mariani A, Dowdy SC, Weaver AL, McGree ME, Cliby WA, et al. The impact of surgical guidelines and periodic quality assessment on the staging of endometrial cancer. Gynecol Oncol. 2011;123:58–64.CrossRefPubMedGoogle Scholar
  43. 43.
    Chan JK, Urban R, Cheung MK, Shin JY, Husain A, Teng NN, et al. Lymphadenectomy in endometrioid uterine cancer staging – how many lymph nodes are enough? A study of 11,443 patients. Cancer. 2007;109:2454–60.CrossRefPubMedGoogle Scholar
  44. 44.
    Todo Y, Kato H, Kaneuchi M, Watari H, Takeda M, Sakuragi N. Survival effect of para-aortic lymphadenectomy in endometrial cancer (SEPAL study): a retrospective cohort analysis. Lancet. 2010;375:1165–72.CrossRefPubMedGoogle Scholar
  45. 45.
    Mariani A, El-Nashar SA, Dowdy SC. Lymphadenectomy in endometrial cancer: which is the right question? Int J Gynecol Cancer. 2010;20:S52–4.CrossRefPubMedGoogle Scholar
  46. 46.
    Creutzberg CL, van Putten WL, Warlam-Rodenhuis CC, van den Bergh AC, de Winter KA, Koper PC, et al. Outcome of high-risk stage IC, grade 3, compared with stage I endometrial carcinoma patients: the postoperative radiation therapy in endometrial carcinoma trial. J Clin Oncol. 2004;22:1234–41.CrossRefPubMedGoogle Scholar
  47. 47.
    Keys HM, Roberts JA, Brunetto VL, Zaino RJ, Spirtos NM, Bloss JD, et al. A phase III trial of surgery with or without adjunctive external pelvic radiation therapy in intermediate risk endometrial adenocarcinoma: a Gynecologic Oncology Group study (vol 92, pg 744, 2004). Gynecol Oncol. 2004;94:241–2.CrossRefGoogle Scholar
  48. 48.
    Horowitz NS, Peters 3rd WA, Smith MR, Drescher CW, Atwood M, Mate TP. Adjuvant high dose rate vaginal brachytherapy as treatment of stage I and II endometrial carcinoma. Obstet Gynecol. 2002;99:235–40.CrossRefPubMedGoogle Scholar
  49. 49.
    Straughn Jr JM, Huh WK, Kelly FJ, Leath 3rd CA, Kleinberg MJ, Hyde Jr J, et al. Conservative management of stage I endometrial carcinoma after surgical staging. Gynecol Oncol. 2002;84:194–200.CrossRefPubMedGoogle Scholar
  50. 50.
    Powell MA. Lymph node dissection in endometrial cancer treatment – to do or not to do, that remains the question. Gynecol Oncol. 2012;127:1–2.CrossRefPubMedGoogle Scholar
  51. 51.
    Boll D, Verhoeven RH, van der Aa MA, Lybeert ML, Coebergh JW, Janssen-Heijnen ML. Adherence to national guidelines for treatment and outcome of endometrial cancer stage I in relation to co-morbidity in southern Netherlands 1995–2008. Eur J Cancer. 2011;47:1504–10.CrossRefPubMedGoogle Scholar
  52. 52.
    Truong PT, Kader HA, Lacy B, Lesperance M, MacNeil MV, Berthelet E, et al. The effects of age and comorbidity on treatment and outcomes in women with endometrial cancer. Am J Clin Oncol. 2005;28:157–64.CrossRefPubMedGoogle Scholar
  53. 53.
    Benedetti Panici P, Basile S, Maneschi F, Alberto Lissoni A, Signorelli M, Scambia G, et al. Systematic pelvic lymphadenectomy vs. no lymphadenectomy in early-stage endometrial carcinoma: randomized clinical trial. J Natl Cancer Inst. 2008;100:1707–16.CrossRefPubMedGoogle Scholar
  54. 54.
    Strasberg SM, Linehan DC, Hawkins WG. The accordion severity grading system of surgical complications. Ann Surg. 2009;250:177–86.CrossRefPubMedGoogle Scholar
  55. 55.
    Walker JL, Piedmonte MR, Spirtos NM, Eisenkop SM, Schlaerth JB, Mannel RS, et al. Laparoscopy compared with laparotomy for comprehensive surgical staging of uterine cancer: Gynecologic Oncology Group study LAP2. J Clin Oncol. 2009;27:5331–6.PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Mariani A, Webb MJ, Galli L, Podratz KC. Potential therapeutic role of para-aortic lymphadenectomy in node-positive endometrial cancer. Gynecol Oncol. 2000;76:348–56.CrossRefPubMedGoogle Scholar
  57. 57.
    Podratz KC, Mariani A, Webb MJ. Staging and therapeutic value of lymphadenectomy in endometrial cancer. Gynecol Oncol. 1998;70:163–4.CrossRefPubMedGoogle Scholar
  58. 58.
    Kilgore LC, Partridge EE, Alvarez RD, Austin JM, Shingleton HM, Noojin 3rd F, et al. Adenocarcinoma of the endometrium: survival comparisons of patients with and without pelvic node sampling. Gynecol Oncol. 1995;56:29–33.CrossRefPubMedGoogle Scholar
  59. 59.
    May K, Bryant A, Dickinson HO, Kehoe S, Morrison J. Lymphadenectomy for the management of endometrial cancer. Cochrane Database Syst Rev. 2010:CD007585.Google Scholar
  60. 60.
    Chuang L, Burke TW, Tornos C, Marino BD, Mitchell MF, Tortolero-Luna G, et al. Staging laparotomy for endometrial carcinoma: assessment of retroperitoneal lymph nodes. Gynecol Oncol. 1995;58:189–93.CrossRefPubMedGoogle Scholar
  61. 61.
    Havrilesky LJ, Cragun JM, Calingaert B, Synan I, Secord AA, Soper JT, et al. Resection of lymph node metastases influences survival in stage IIIC endometrial cancer. Gynecol Oncol. 2005;99:689–95.CrossRefPubMedGoogle Scholar
  62. 62.
    Todo Y, Kato H, Minobe S, Okamoto K, Suzuki Y, Konno Y, et al. A validation study of the new revised FIGO staging system to estimate prognosis for patients with stage IIIC endometrial cancer. Gynecol Oncol. 2011;121:126–30.CrossRefPubMedGoogle Scholar
  63. 63.
    Kumar S, Mariani A, Bakkum-Gamez JN, Weaver AL, McGree ME, Keeney GL, et al. Risk factors that mitigate the role of paraaortic lymphadenectomy in uterine endometrioid cancer. Gynecol Oncol. 2013;130:441–5.CrossRefPubMedGoogle Scholar
  64. 64.
    AlHilli MM, Mariani A. The role of para-aortic lymphadenectomy in endometrial cancer. Int J Clin Oncol. 2013;18:193–9.CrossRefPubMedGoogle Scholar
  65. 65.
    Case AS, Rocconi RP, Straughn Jr JM, Conner M, Novak L, Wang W, et al. A prospective blinded evaluation of the accuracy of frozen section for the surgical management of endometrial cancer. Obstet Gynecol. 2006;108:1375–9.CrossRefPubMedGoogle Scholar
  66. 66.
    Frumovitz M, Slomovitz BM, Singh DK, Broaddus RR, Abrams J, Sun CC, et al. Frozen section analyses as predictors of lymphatic spread in patients with early-stage uterine cancer. J Am Coll Surg. 2004;199:388–93.CrossRefPubMedGoogle Scholar
  67. 67.
    Kucera E, Kainz C, Reinthaller A, Sliutz G, Leodolter S, Kucera H, et al. Accuracy of intraoperative frozen-section diagnosis in stage I endometrial adenocarcinoma. Gynecol Obstet Invest. 2000;49:62–6.CrossRefPubMedGoogle Scholar
  68. 68.
    Sanjuan A, Cobo T, Pahisa J, Escaramis G, Ordi J, Ayuso JR, et al. Preoperative and intraoperative assessment of myometrial invasion and histologic grade in endometrial cancer: role of magnetic resonance imaging and frozen section. Int J Gynecol Cancer. 2006;16:385–90.CrossRefPubMedGoogle Scholar
  69. 69.
    Frei KA, Kinkel K, Bonel HM, Lu Y, Zaloudek C, Hricak H. Prediction of deep myometrial invasion in patients with endometrial cancer: clinical utility of contrast-enhanced MR imaging-a meta-analysis and Bayesian analysis. Radiology. 2000;216:444–9.CrossRefPubMedGoogle Scholar
  70. 70.
    Pakkal MV, Rudralingam V, McCluggage WG, Kelly BE. MR staging in carcinoma of the endometrium and carcinoma of the cervix. Ulster Med J. 2004;73:20–4.PubMedCentralPubMedGoogle Scholar
  71. 71.
    Chung HH, Kim JW, Park NH, Song YS, Kang SB, Lee HP. Use of preoperative serum CA-125 levels for prediction of lymph node metastasis and prognosis in endometrial cancer. Acta Obstet Gyn Scan. 2006;85:1501–5.CrossRefGoogle Scholar
  72. 72.
    Powell JL, Hill KA, Shiro BC, Diehl SJ, Gajewski WH. Preoperative serum CA-125 levels in treating endometrial cancer. J Reprod Med. 2005;50:585–90.PubMedGoogle Scholar
  73. 73.
    Kalogera E, Scholler N, Powless C, Weaver A, Drapkin R, Li J, et al. Correlation of serum HE4 with tumor size and myometrial invasion in endometrial cancer. Gynecol Oncol. 2012;124:270–5.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer India 2015

Authors and Affiliations

  1. 1.Division of Gynecologic SurgeryMayo ClinicRochesterUSA

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