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Journal of Cancer Research and Clinical Oncology

, Volume 145, Issue 1, pp 213–221 | Cite as

Surgical staging in endometrial cancer

  • Maria Luisa GasparriEmail author
  • Donatella Caserta
  • Pierluigi Benedetti Panici
  • Andrea Papadia
  • Michael D. Mueller
Review – Clinical Oncology
  • 230 Downloads

Abstract

In several malignancies, it has been demonstrated that the lymph nodal status is the most important pathologic factor affecting prognosis and giving the indication to further adjuvant treatment. The surgical assessment of the lymph nodal status in endometrial cancer is debated since 30 years. Recently, the sentinel lymph node mapping is rapidly gaining clinical acceptance in endometrial cancer. The adoption of Indocyanine Green as a safe and user friendly tracer for sentinel lymph node mapping increased the speed to which this procedure is getting applied in clinical practice. As a consequence of this rapid growth, several fundamental questions have been raised and are still debatable. In this manuscript, we discuss the importance of a known pathological lymph nodal status, the technique of the sentinel lymph node mapping with the reported false negative rates and detection rates according to the different tracers adopted, and the clinical scenarios in which a sentinel lymph node mapping could be employed.

Keywords

Endometrial cancer Laparoscopy Sentinel lymph node mapping Indocyanine green Fluorescence 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare to have no conflict of interest.

References

  1. ASTEC Study Group, Kitchener H, Swart AM et al (2009) Efficacy of systematic pelvic lymphadenectomy in endometrial cancer (MRC ASTEC trial): a randomised study. Lancet 373:125–136CrossRefGoogle Scholar
  2. Ballester M, Dubernard G, Lécuru F et al (2011) Detection rate and diagnostic accuracy of sentinel-node biopsy in early stage endometrial cancer: a prospective multicentre study (SENTI-ENDO). Lancet Oncol 12:469–476CrossRefGoogle Scholar
  3. Barlin JN, Khoury-Collado F, Kim CH et al (2012) The importance of applying a sentinel lymph node mapping algorithm in endometrial cancer staging: beyond removal of blue nodes. Gynecol Oncol 125:531–535CrossRefGoogle Scholar
  4. Bodurtha Smith AJ, Fader AN, Tanner EJ (2017) Sentinel lymph node assessment in endometrial cancer: a systematic review and meta analysis. Am J Obstet Gynecol 216:459–476CrossRefGoogle Scholar
  5. Bogani G, Dowdy SC, Cliby WA et al (2014) Role of pelvic and para-aortic lymphadenectomy in endometrial cancer: current evidence. J Obstet Gynaecol Res 40:301–311CrossRefGoogle Scholar
  6. Buda A, Papadia A, Zapardiel I et al (2016) From conventional radiotracer Tc-99(m) with blue dye to indocyanine green fluorescence: a comparison of methods towards optimization of sentinel lymph node mapping in early stage cervical cancer for a laparoscopic approach. Ann Surg Oncol 23:2959–2965CrossRefGoogle Scholar
  7. Buda A, Papadia A, Di Martino G et al (2018a) Real-time fluorescent sentinel lymph node mapping with indocyanine green in women with previous conization undergoing laparoscopic surgery for early invasive cervical cancer: comparison with radiotracer ± blue dye. J Minim Invasive Gynecol 25:455–460CrossRefGoogle Scholar
  8. Buda A, Gasparri ML, Puppo A et al (2018b) Lymph node evaluation in high-risk early stage endometrial cancer: a multi-institutional retrospective analysis comparing the sentinel lymph node (SLN) algorithm and SLN with selective lymphadenectomy. Gynecol Oncol.  https://doi.org/10.1016/j.ygyno.2018.06.003 Google Scholar
  9. Cabanas RM (1977) An approach for the treatment of penile carcinoma. Cancer 39:456–466CrossRefGoogle Scholar
  10. Chagpar AB, Scoggins CR, Martin RC et al (2007) Are three sentinel nodes sufficient? Arch Surg 142:456–460CrossRefGoogle Scholar
  11. Colombo N, Creutzberg C, Amant F et al (2016) ESMO-ESGO-ESTRO Consensus Conference on Endometrial Cancer: diagnosis, treatment and follow-up. Ann Oncol 27:16–41CrossRefGoogle Scholar
  12. Creasman W (2009) Revised FIGO staging for carcinoma of the endometrium. Int J Gynaecol Obstet 105:109CrossRefGoogle Scholar
  13. Creasman WT, Morrow CP, Bundy BN et al (1987) Surgical pathologic spread patterns of endometrial cancer. A Gynecologic Oncology Group Study. Cancer 60:2035–2041CrossRefGoogle Scholar
  14. Di Martino G, Crivellaro C, De Ponti E et al (2017) Indocyanine green versus radiotracer with or without blue dye for sentinel lymph node mapping in Stage > IB1 cervical cancer (> 2 cm). J Minim Invasive Gynecol 24:954–959CrossRefGoogle Scholar
  15. Ditto A, Martinelli F, Bogani G et al (2015) Sentinel node mapping using hysteroscopic injection of indocyanine green and laparoscopic Near-Infrared fluorescence imaging in endometrial cancer staging. J Minim Invasive Gynecol 22:132–133CrossRefGoogle Scholar
  16. Ehrisman J, Secord AA, Berchuck A et al (2016) Performance of sentinel lymph node biopsy in high-risk endometrial cancer. Gynecol Oncol Rep 17:69–71CrossRefGoogle Scholar
  17. Eriksson AG, Ducie J, Ali N et al (2016) Comparison of a sentinel lymph node and a selective lymphadenectomy algorithm in patients with endometrioid endometrial carcinoma and limited myometrial invasion. Gynecol Oncol 140:394–399CrossRefGoogle Scholar
  18. Eriksson AG, Beavis A, Soslow RA et al (2017) A comparison of the detection of sentinel lymph nodes using indocyanine green and near-infrared fluorescence imaging versus blue dye during robotic surgery in uterine cancer. Int J Gynecol Cancer 27:743–747CrossRefGoogle Scholar
  19. FIGO stages (1989) 1988 revision. Gynecol Oncol 35:125–127CrossRefGoogle Scholar
  20. Frumovitz M, Plante M, Lee PS, Sandadi S, Lilja JF, Escobar PF, Gien LT, Urbauer DL, Abu-Rustum NR (2018) Near-infrared fluorescence for detection of sentinel lymph nodes in women with cervical and uterine cancers (FILM): a randomised, phase 3, multicentre, non-inferiority trial. Lancet Oncol 19(10):1394–1403CrossRefGoogle Scholar
  21. Gasparri ML, Ruscito I, Bolla D et al (2017) The efficacy of fibrin sealant patches in reducing the incidence of lymphatic morbidity after radical lymphadenectomy: a meta-analysis. Int J Gynecol Cancer 27:1283–1292CrossRefGoogle Scholar
  22. Goyal A, Newcombe RG, Chhabra A et al (2006) Factors affecting failed localization and false negative rates of sentinel node biopsy in breast cancer-results of the ALMANAC validation phase. Breast Cancer Res Treat 99:203–208CrossRefGoogle Scholar
  23. Greene FL, Page DL, Irvin D et al (2003) AJCC cancer staging manual, 6th edn. Springer-Verlag, New York, 223Y240Google Scholar
  24. Holloway RW, Bravo RA, Rakowski JA et al (2012) Detection of sentinel lymph nodes in patients with endometrial cancer undergoing robotic-assisted staging: a comparison of colorimetric and fluorescence imaging. Gynecol Oncol 126:25–29CrossRefGoogle Scholar
  25. Holloway RW, Ahmad S, Kendrick JE et al (2017) A prospective cohort study comparing colorimetric and fluorescent imaging for sentinel lymph node mapping in endometrial cancer. Ann Surg Oncol 24:1972–1979CrossRefGoogle Scholar
  26. How J, Gotlieb WH, Press JZ et al (2015) Comparing indocyanine green, technetium, and blue dye for sentinel lymph node mapping in endometrial cancer. Gynecol Oncol 137:436–442CrossRefGoogle Scholar
  27. Imboden S, Papadia A, Nauwerk M et al (2015) A comparison of radiocolloid and indocyanine green fluorescence imaging, sentinel lymph node mapping in patients with cervical cancer undergoing laparoscopic surgery. Ann Surg Oncol 22:4198–4203CrossRefGoogle Scholar
  28. Kumar S, Medeiros F, Dowdy SC et al (2012) A prospective assessment of the reliability of frozen section to direct intraoperative decision making in endometrial cancer. Gynecol Oncol 127:525–531CrossRefGoogle Scholar
  29. Kumar S, Podratz KC, Bakkum-Gamez JN et al (2014) Prospective assessment of the prevalence of pelvic, para-aortic and high para-aortic lymph node metastasis in endometrial cancer. Gynecol Oncol 132:38–43CrossRefGoogle Scholar
  30. Laufer J, Scasso S, Papadia A et al (2013) Association between tumor diameter and lymphovascular space invasion among women with early-stage endometrial cancer. Int J Gynaecol Obstet 123:142–145CrossRefGoogle Scholar
  31. Lin H, Ding Z, Kota VG et al (2017) Sentinel lymph node mapping in endometrial cancer: a systematic review and meta-analysis. Oncotarget 8:46601–46610Google Scholar
  32. Maggino T, Romagnolo C, Zola P et al (1995) An analysis of approaches to the treatment of endometrial cancer in western Europe: a CTF study. Eur J Cancer 31A:1993–1997CrossRefGoogle Scholar
  33. Maggino T, Romagnolo C, Landoni F et al (1998) An analysis of approaches to the management of endometrial cancer in North America: a CTF study. Gynecol Oncol 68:274–279CrossRefGoogle Scholar
  34. Martin RC, Edwards MJ, Wong SL et al (2000) Practical guidelines for optimal gamma probe detection of sentinel lymph nodes in breast cancer: results of a multiinstitutional study. Surgery 128:139–144CrossRefGoogle Scholar
  35. McCarter MD, Yeung H, Fey J et al (2001) The breast cancer patient with multiple sentinel nodes: when to stop? J Am Coll Surg 192:692–697CrossRefGoogle Scholar
  36. McMasters KM, Wong SL, Chao C et al (2001) Defining the optimal surgeon experience for breast cancer sentinel lymph node biopsy: a model for implementation of new surgical techniques. Ann Surg 234:292–300CrossRefGoogle Scholar
  37. Morotti M, Menada MV, Moioli M et al (2012) Frozen section pathology at time of hysterectomy accurately predicts endometrial cancer in patients with preoperative diagnosis of atypical endometrial hyperplasia. Gynecol Oncol 125:536–540CrossRefGoogle Scholar
  38. Morton DL, Thompson JF, Cochran AJ et al (2006) Sentinel-node biopsy or nodal observation in melanoma. N Engl J Med 355:1307–1317CrossRefGoogle Scholar
  39. Naoura I, Canlorbe G, Bendifallah S et al (2015) Relevance of sentinel lymph node procedure for patients with high-risk endometrial cancer. Gynecol Oncol 136:60–64CrossRefGoogle Scholar
  40. NCCN Clinical Practice Guidelines in Oncology (2018) Uterine neoplasms. Version 1.2018. http://www.nccn.org/professionals/physician_gls/pdf/uterine.pdf
  41. Ouldamer L, Bendifallah S, Body G et al (2017) Call for surgical nodal staging in women with ESMO/ESGO/ESTRO high-intermediate risk endometrial cancer: a multicentre cohort analysis from the FRANCOGYN Study Group. Ann Surg Oncol 24:1660–1666CrossRefGoogle Scholar
  42. Panici PB, Basile S, Maneschi F et al (2008) Systematic pelvic lymphadenectomy vs no lymphadenectomy in early-stage endometrial carcinoma: randomized clinical trial. J Natl Cancer Inst 100:1707–1716 CrossRefGoogle Scholar
  43. Papadia A, Azioni G, Brusaca B et al (2009) Frozen section underestimates the need for surgical staging in endometrial cancer patients. Int J Gynecol Cancer 19:1570–1573CrossRefGoogle Scholar
  44. Papadia A, Imboden S, Siegenthaler FA et al (2016a) Laparoscopic indocyanine green sentinel lymph node mapping in endometrial cancer. Ann Surg Oncol 23:2206–2211CrossRefGoogle Scholar
  45. Papadia A, Imboden S, Gasparri ML et al (2016b) Endometrial and cervical cancer patients with multiple sentinel lymph nodes at laparoscopic ICG mapping: how many are enough? J Cancer Res Clin Oncol 142:1831–1836CrossRefGoogle Scholar
  46. Papadia A, Gasparri ML, Buda A et al (2017a) Sentinel lymph node mapping in endometrial cancer: comparison of fluorescence dye with traditional radiocolloid and blue. J Cancer Res Clin Oncol 143:2039–2048CrossRefGoogle Scholar
  47. Papadia A, Gasparri ML, Mueller MD (2017b) Are allergic reactions to indocyanine green really that uncommon? A single institution experience. Obstet Gynecol Rep 1:1–2CrossRefGoogle Scholar
  48. Papadia A, Gasparri ML, Mueller MD (2017c) Is it time to consider the sentinel lymph node mapping the new standard in endometrial cancer? Transl Cancer Res 6:S547–S552CrossRefGoogle Scholar
  49. Papadia A, Zapardiel I, Bussi B, Ghezzi F, Ceccaroni M, De Ponti E, Elisei F, Imboden S, de la Noval BD, Gasparri ML, Di Martino G, De Santiago J, Mueller M, Vecchione F, Dell’Orto F, Buda A (2017d) Sentinel lymph node mapping in patients with stage I endometrial carcinoma: a focus on bilateral mapping identification by comparing radiotracer Tc99m with blue dye versus indocyanine green fluorescent dye. J Cancer Res Clin Oncol 143(3):475–480CrossRefGoogle Scholar
  50. Papadia A, Gasparri ML, Siegenthaler F et al (2017e) FIGO stage IIIC endometrial cancer identification among patients with complex atypical hyperplasia, grade 1 and 2 endometrioid endometrial cancer: laparoscopic indocyanine green sentinel lymph node mapping versus frozen section of the uterus, why get around the problem? J Cancer Res Clin Oncol 143:491–497CrossRefGoogle Scholar
  51. Papadia A, Buda A, Gasparri ML et al (2018a) The impact of different doses of indocyanine green on the sentinel lymph node mapping in early stage endometrial cancer. J Cancer Res Clin Oncol 144:2187–2191CrossRefGoogle Scholar
  52. Papadia A, Gasparri ML, Radan AP et al (2018b) Retrospective validation of the laparoscopic ICG SLN mapping in patients with grade 3 endometrial cancer. J Cancer Res Clin Oncol 144:1385–1393CrossRefGoogle Scholar
  53. Persson J, Geppert B, Lönnerfors C et al (2017) Description of a reproducible anatomically based surgical algorithm for detection of pelvic sentinel lymph nodes in endometrial cancer. Gynecol Oncol 147:120–125CrossRefGoogle Scholar
  54. Richards P, Tucker WD, Srivastava SC (1982) Technetium-99m: an historical perspective. Int J Appl Radiat Isotopes 33:793–799CrossRefGoogle Scholar
  55. Rossi EC, Kowalski LD, Scalici J et al (2017) A comparison of sentinel lymph node biopsy to lymphadenectomy for endometrial cancer staging (FIRES trial): a multicentre, prospective, cohort study. Lancet Oncol 18:384–392CrossRefGoogle Scholar
  56. Ruscito I, Gasparri ML, Braicu EI et al (2016) Sentinel node mapping in cervical and endometrial cancer: indocyanine green versus other conventional dyes—a metaanalysis. Ann Surg Oncol 23:3749–3756CrossRefGoogle Scholar
  57. Sala P, Morotti M, Menada MV et al (2014) Intraoperative frozen section risk assessment accurately tailors the surgical staging in patients affected by early-stage endometrial cancer: the application of 2 different risk algorithms. Int J Gynecol Cancer 24:1021–1026CrossRefGoogle Scholar
  58. Segrè E, Seaborg GT (1938) Nuclear isomerism in element 43. Phys Rev 54:772CrossRefGoogle Scholar
  59. Sharma C, Deutsch I, Lewin SN et al (2011) Lymphadenectomy influences the utilization of adjuvant radiation treatment for endometrial cancer. Am J Obstet Gynecol 205:e1–e9CrossRefGoogle Scholar
  60. Simpkins F, Papadia A, Kunos C et al (2013) Patterns of recurrence in stage I endometrioid endometrial adenocarcinoma with lymphovascular space invasion. Int J Gynecol Cancer 23:98–104CrossRefGoogle Scholar
  61. Sinno AK, Fader AN, Roche KL et al (2014) A comparison of colorimetric versus fluorometric sentinel lymph node mapping during robotic surgery for endometrial cancer. Gynecol Oncol 134:281–286CrossRefGoogle Scholar
  62. Sinno AK, Peijnenburg E, Fader AN et al (2016) Reducing overtreatment: A comparison of lymph node assessment strategies for endometrial cancer. Gynecol Oncol 143:281–286CrossRefGoogle Scholar
  63. Soliman PT, Westin SN, Dioun S et al (2017) A prospective validation study of sentinel lymph node mapping for high-risk endometrial cancer. Gynecol Oncol 146:234–239CrossRefGoogle Scholar
  64. Tanner EJ, Sinno AK, Stone RL et al (2015) Factors associated with successful bilateral sentinel lymph node mapping in endometrial cancer. Gynecol Oncol 138:542–547CrossRefGoogle Scholar
  65. Touhami O, Grégoire J, Renaud MC et al (2017) Performance of sentinel lymph node (SLN) mapping in high-risk endometrial cancer. Gynecol Oncol 147:549–555CrossRefGoogle Scholar
  66. Vaidya JS, Dewar JA, Brown DC et al (2005) A mathematical model for the effect of a false-negative sentinel node biopsy on breast cancer mortality: a tool for everyday use. Breast Cancer Res 7:225–227CrossRefGoogle Scholar
  67. Van der Zee AG, Oonk MH, De Hullu JA et al (2008) Sentinel node dissection is safe in the treatment of early-stage vulvar cancer. J Clin Oncol 26:884–889CrossRefGoogle Scholar
  68. Veronesi U, Paganelli G, Viale G (2003) A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 349:546–553CrossRefGoogle Scholar
  69. Wilke LG, McCall LM, Posther KE, Whitworth PW, Reintgen DS et al (2006) Surgical complications associated with sentinel lymph node biopsy: results from a prospective international cooperative group trial. Ann Surg Oncol 13:491–500CrossRefGoogle Scholar
  70. Woznick A, Franco M, Bendick P et al (2006) Sentinel lymph node dissection for breast cancer: how many nodes are enough and which technique is optimal? Am J Surg 191:330–333CrossRefGoogle Scholar
  71. Xiong L, Gazyakan E, Yang W et al (2014) Indocyanine green fluorescence- guided sentinel node biopsy: a meta-analysis on detection rate and diagnostic performance. Eur J Surg Oncol 40:843–849CrossRefGoogle Scholar
  72. Zakaria S, Degnim AC, Kleer CG et al (2007) Sentinel lymph node biopsy for breast cancer: how many lymph nodes are enough? J Surg Oncol 96:554–559CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Obstetrics and GynecologyUniversity Hospital of Bern and University of BernBernSwitzerland
  2. 2.Surgical and Medical Department of Translational MedicineSapienza University of RomeRomeItaly
  3. 3.Department of Gynecological-Obstetrical Sciences and Urological SciencesSapienza University of RomeRomeItaly

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