Status of Sentinel Lymph Node Biopsy in Endometrial Cancer

Abstract

The role of lymphadenectomy in surgical staging remains one of the biggest controversies in the management of endometrial cancer. The concept of sentinel lymph node biopsy in endometrial cancer has been evaluated for a number of years, with promising sensitivity rates and negative predictive values. The possibility of adequate staging while avoiding systematic lymphadenectomy leads to a significant reduction in the rate of peri- and postoperative morbidity. Nevertheless, the status of sentinel lymph node biopsy in endometrial cancer has not yet been fully elucidated and is variously assessed internationally. According to current European guidelines and recommendations, sentinel lymph node biopsy in endometrial cancer should be performed only in the context of clinical studies. In this review article, the developments of the past decade are explored concisely. In addition, current data regarding the technical aspects, accuracy and prognostic relevance of sentinel lymph node biopsy are explained and evaluated critically.

Key words

endometrial cancer - sentinel lymph node - sentinel mapping - ultrastaging

Publikationsverlauf

Eingereicht: 27. Juli 2020

Angenommen nach Revision: 01. März 2021

Artikel online veröffentlicht:
20. Mai 2021

• References/Literatur

• 1 Accessed December 29, 2020 at: https://www.krebsdaten.de/Krebs/DE/Content/Publikationen/Krebs_in_Deutschland/kid_2019/kid_2019_c54_c55_gebaermutterkoerper.pdf?__blob=publicationFile
• 2 Ballester M, Dubernard G, Lecuru F. et al. Detection rate and diagnostic accuracy of sentinel-node biopsy in early stage endometrial cancer: A prospective multicentre study (SENTI-ENDO). Lancet Oncol 2011; 12: 469-476
• 3 Abu-Rustum NR, Zhou Q, Iasonos A. et al. The revised 2009 FIGO staging system for endometrial cancer: should the 1988 FIGO stages IA and IB be altered?. Int J Gynecol Cancer 2011; 21: 511-516
• 4 Holloway RW, Abu-Rustum NR, Backes FJ. et al. Sentinel Lymph Node Mapping and Staging in Endometrial Cancer: A Society of Gynecologic Oncology Literature Review with Consensus Recommendations. Gynecol Oncol 2017; 146: 405-415
• 5 Emons G, Steiner E, Vordermark D. et al. Interdisciplinary Diagnosis, Therapy and Follow-up of Patients with Endometrial Cancer. Guideline (S3-Level, AWMF Registry Nummer 032/034-OL, April 2018) – Part 1 with Recommendations on the Epidemiology, Screening, Diagnosis and Hereditary Factors of Endometrial Cancer. Geburtshilfe Frauenheilkd 2018; 78: 949-971
• 6 Emons G, Steiner E, Vordermark D. et al. Interdisciplinary Diagnosis, Therapy and Follow-up of Patients with Endometrial Cancer. Guideline (S3-Level, AWMF Registry Number 032/034-OL, April 2018) – Part 2 with Recommendations on the Therapy and Follow-up of Endometrial Cancer, Palliative Care, Psycho-oncological/Psychosocial Care/Rehabilitation/Patient Information and Healthcare Facilities. Geburtshilfe Frauenheilkd 2018; 78: 1089-1109
• 7 Accessed January 05, 2021 at: https://www.awmf.org/uploads/tx_szleitlinien/032-034OLl_S3_Endometriumkarzinom-Diagnostik-Therpie-Nachsorge_2018-04.pdf
• 8 Koh WJ, Abu-Rustum NR, Bean S. et al. Uterine Neoplasms, Version 1.2018, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw 2018; 16: 170-199
• 9 Casarin J, Multinu F, Abu-Rustum N. et al. Factors influencing the adoption of the sentinel lymph node technique for endometrial cancer staging: an international survey of gynecologic oncologists. Int J Gynecol Cancer 2019; 29: 60-67
• 10 Colombo N, Creutzberg C, Amant F. et al. ESMO-ESGO-ESTRO Endometrial Consensus Conference Working Group. Ann Oncol 2016; 27: 16-41
• 11 Rossi EC. Current state of sentinel lymph nodes for women with endometrial cancer. Int J Gynecol Cancer 2019; 29: 613-621
• 12 Sueoka K, Umayahara K, Abe A. et al. Prognosis for endometrial cancer patients treated with systematic pelvic and para-aortic lymphadenectomy followed by platinum-based chemotherapy. Int J Gynecol Cancer 2015; 25: 81-86
• 13 Randall ME, Filiaci VL, Muss H. et al. Randomized phase III trial of whole-abdominal irradiation versus doxorubicin and cisplatin chemotherapy in advanced endometrial carcinoma: a Gynecologic Oncology Group Study. J Clin Oncol 2006; 24: 36-44
• 14 Benedetti Panici P, Basile S, Maneschi F. et al. Systematic pelvic lymphadenectomy vs. no lymphadenectomy in early-stage endometrial carcinoma: Randomized clinical trial. J Natl Cancer Inst 2008; 100: 1707-1716
• 15 Kitchener H, Swart AM, Qian Q. et al. Efficacy of systematic pelvic lymphadenectomy in endometrial cancer (MRC ASTEC trial): A randomised study. Lancet 2009; 373: 125-136
• 16 Eltabbakh GH, Piver MS, Hempling RE. et al. Excellent long-term survival and absence of vaginal recurrences in 332 patients with low-risk stage I endometrial adenocarcinoma treated with hysterectomy and vaginal brachytherapy without formal staging lymph node sampling: report of a prospective trial. Int J Radiat Oncol Biol Phys 1997; 38: 373-380
• 17 Mariani A, Webb MJ, Keeney GL. et al. Low-risk corpus cancer: is lymphadenectomy or radiotherapy necessary?. Am J Obstet Gynecol 2000; 182: 1506-1519
• 18 Dowdy SC, Borah BJ, Bakkum-Gamez JN. et al. Prospective assessment of survival, morbidity, and cost associated with lymphadenectomy in low-risk endometrial cancer. Gynecol Oncol 2012; 127: 5-10
• 19 Bendifallah S, Koskas M, Ballester M. et al. The survival impact of systematic lymphadenectomy in endometrial cancer with the use of propensity score matching analysis. Am J Obstet Gynecol 2012; 206: 500.e1-500.e11
• 20 Todo Y, Kato H, Kaneuchi M. et al. Survival effect of para-aortic lymphadenectomy in endometrial cancer (SEPAL study): a retrospective cohort analysis. Lancet 2010; 375: 1165-1172
• 21 Kuroda K, Yamamoto Y, Yanagisawa M. et al. Risk factors and a prediction model for lower limb lymphedema following lymphadenectomy in gynecologic cancer: a hospital-based retrospective cohort study. BMC Womens Health 2017; 17: 50
• 22 Polan RM, Rossi EC, Barber EL. Extent of lymphadenectomy and postoperative major complications among women with endometrial cancer treated with minimally invasive surgery. Am J Obstet Gynecol 2019; 220: 263.e1-263.e8
• 23 Cabanas RM. An approach for the treatment of penile carcinoma. Cancer 1977; 39: 456-466
• 24 Zivanovic O, Khoury-Collado F, Abu-Rustum NR. et al. Sentinel lymph node biopsy in the management of vulvar carcinoma, cervical cancer, and endometrial cancer. Oncologist 2009; 14: 695-705
• 25 Sahbai S, Fiz F, Taran F. et al. Influence of 99m-Tc-Nanocolloid Activity Concentration on Sentinel Lymph Node Detection in Endometrial Cancer: A Quantitative SPECT/CT Study. Diagnostics (Basel) 2020; 10: 700
• 26 Perrone AM, Casadio P, Formelli G. et al. Cervical and hysteroscopic injection for identification of sentinel lymph node in endometrial cancer. Gynecol Oncol 2008; 111: 62-67
• 27 Robova H, Charvat M, Strnad P. et al. Lymphatic mapping in endometrial cancer: Comparison of hysteroscopic and subserosal injection and the distribution of sentinel lymph nodes. Int J Gynecol Cancer 2009; 19: 391-394
• 28 Mücke J, Klapdor R, Schneider M. et al. Isthmocervical labelling and SPECT/CT for optimized sentinel detection in endometrial cancer: Technique, experience and results. Gynecol Oncol 2014; 134: 287-292
• 29 Burke TW, Levenback C, Tornos C. et al. 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: 169-173
• 30 Holub Z, Kliment L, Lukác J. et al. Laparoscopically-assisted intraoperative lymphatic mapping in endometrial cancer: preliminary results. Eur J Gynaecol Oncol 2001; 22: 118-121
• 31 Echt ML, Finan MA, Hoffman MS. et al. Detection of sentinel lymph nodes with lymphazurin in cervical, uterine, and vulvar malignancies. South Med J 1999; 92: 204-208
• 32 Altgassen C, Pagenstecher J, Hornung D. et al. A new approach to label sentinel nodes in endometrial cancer. Gynecol Oncol 2007; 105: 457-461
• 33 Li B, Li XG, Wu LY. et al. A pilot study of sentinel lymph nodes identification in patients with endometrial cancer. Bull Cancer 2007; 94: E1-E4
• 34 Niikura H, Kaiho-Sakuma M, Tokunaga H. et al. Tracer injection sites and combinations for sentinel lymph node detection in patients with endometrial cancer. Gynecol Oncol 2013; 131: 299-303
• 35 Sawicki S, Lass P, Wydra D. Sentinel Lymph Node Biopsy in Endometrial Cancer–Comparison of 2 Detection Methods. Int J Gynecol Cancer 2015; 25: 1044-1050
• 36 Sahbai S, Taran FA, Fiz F. et al. Pericervical Injection of 99 mTc-Nanocolloid Is Superior to Peritumoral Injection for Sentinel Lymph Node Detection of Endometrial Cancer in SPECT/CT. Clin Nucl Med 2016; 41: 927-932
• 37 Zuo J, Wu LY, Cheng M. et al. Comparison Study of Laparoscopic Sentinel Lymph Node Mapping in Endometrial Carcinoma Using Carbon Nanoparticles and Lymphatic Pathway Verification. J Minim Invasive Gynecol 2019; 26: 1125-1132
• 38 Abu-Rustum NR, Khoury-Collado F, Pandit-Taskar N. et al. Sentinel lymph node mapping for grade 1 endometrial cancer: is it the answer to the surgical staging dilemma?. Gynecol Oncol 2009; 113: 163-163
• 39 Abu-Rustum NR, Gomez JD, Alektiar KM. et al. The incidence of isolated paraaortic nodal metastasis in surgically staged endometrial cancer patients with negative pelvic lymph nodes. Gynecol Oncol 2009; 115: 236-238
• 40 Accessed January 07, 2021 at: https://www.fda.gov/media/124115/download
• 41 Frumovitz M, Plante M, Lee PS. et al. 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 2018; 19: 1394-1403
• 42 Kessous R, How J, Abitbol J. et al. Triple tracer (blue dye, indocyanine green, and Tc99) compared to double tracer (indocyanine green and Tc99) for sentinel lymph node detection in endometrial cancer: a prospective study with random assignment. Int J Gynecol Cancer 2019; 29: 1121-1125
• 43 Cabrera S, Bebia V, Franco-Camps S. et al. Technetium-99 m-indocyanine green versus technetium-99 m-methylene blue for sentinel lymph node biopsy in early-stage endometrial cancer. Int J Gynecol Cancer 2020; 30: 311-317
• 44 Thomaier L, Jager L, Stone R. et al. Risk of empty lymph node packets in sentinel lymph node mapping for endometrial cancer using indocyanine green. Int J Gynecol Cancer 2019; 29: 513-517
• 45 Holloway RW, Bravo RA, Rakowski JA. et al. Detection of sentinel lymph nodes in patients with endometrial cancer undergoing robotic-assisted staging: a comparison of colorimetric and fluorescence imaging. Gynecol Oncol 2012; 126: 25-29
• 46 Sinno AK, Fader AN, Roche KL. et al. A comparison of colorimetric versus fluorometric sentinel lymph node mapping during robotic surgery for endometrial cancer. Gynecol Oncol 2014; 134: 281-286
• 47 How J, Gotlieb WH, Press JZ. et al. Comparing indocyanine green, technetium, and blue dye for sentinel lymph node mapping in endometrial cancer. Gynecol Oncol 2015; 137: 436-442
• 48 Buda A, Crivellaro C, Elisei F. et al. Impact of Indocyanine Green for Sentinel Lymph Node Mapping in Early Stage Endometrial and Cervical Cancer: Comparison with Conventional Radiotracer (99m)Tc and/or Blue Dye. Ann Surg Oncol 2016; 23: 2183-2191
• 49 Papadia A, Zapardiel I, Bussi B. et al. Sentinel lymph node mapping in patients with stage I endometrial carcinoma: a focus on bilateral mapping identification by comparing radiotracer Tc99 ^m with blue dye versus indocyanine green fluorescent dye. J Cancer Res Clin Oncol 2017; 143: 475-480
• 50 Eriksson AG, Beavis A, Soslow RA. et al. 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 2017; 27: 743-747
• 51 Holloway RW, Ahmad S, Kendrick JE. et al. A prospective cohort study comparing colorimetric and fluorescent imaging for sentinel lymph node mapping in endometrial cancer. Ann Surg Oncol 2017; 24: 1972-1979
• 52 Rozenholc A, Samouelian V, Warkus T. et al. Green versus blue: Randomized controlled trial comparing indocyanine green with methylene blue for sentinel lymph node detection in endometrial cancer. Gynecol Oncol 2019; 153: 500-504
• 53 Backes FJ, Cohen D, Salani R. et al. Prospective clinical trial of robotic sentinel lymph node assessment with isosulfane blue (ISB) and indocyanine green (ICG) in endometrial cancer and the impact of ultrastaging (NCT01818739). Gynecol Oncol 2019; 153: 496-499
• 54 Schreuder HW, Oei G, Maas M. et al. Implementation of simulation in surgical practice: minimally invasive surgery has taken the lead: the Dutch experience. Med Teach 2011; 33: 105-115
• 55 Khoury-Collado F, St Clair C, Abu-Rustum NR. Sentinel Lymph Node Mapping in Endometrial Cancer: An Update. Oncologist 2016; 21: 461-466
• 56 Casarin J, Multinu F, Tortorella L. et al. Sentinel lymph node biopsy for robotic-assisted endometrial cancer staging: further improvement of perioperative outcomes. Int J Gynecol Cancer 2020; 30: 41-47
• 57 Persson J, Salehi S, Bollino M. et al. Pelvic Sentinel lymph node detection in high-risk Endometrial Cancer (SHREC-trial)-the final step towards a paradigm shift in surgical staging. Eur J Cancer 2019; 116: 77-85
• 58 Rossi EC, Kowalski LD, Scalici J. et al. A comparison of sentinel lymph node biopsy to lymphadenectomy for endometrial cancer staging (FIRES trial): A multicentre, prospective, cohort study. Lancet Oncol 2017; 18: 384-392
• 59 Bodurtha Smith AJ, Fader AN, Tanner EJ. Sentinel lymph node assessment in endometrial cancer: a systematic review and meta-analysis. Am J Obstet Gynecol 2017; 216: 459-476
• 60 Simmons RM. Review of sentinel lymph node credentialing: how many cases are enough?. J Am Coll Surg 2001; 193: 206-209
• 61 Khoury-Collado F, Glaser GE, Zivanovic O. et al. Improving sentinel lymph node detection rates in endometrial cancer: how many cases are needed?. Gynecol Oncol 2009; 115: 453-455
• 62 How J, Boldeanu I, Lau S. et al. Unexpected locations of sentinel lymph nodes in endometrial cancer. Gynecol Oncol 2017; 147: 18-23
• 63 Altay A, Toptas T, Dogan S. et al. Analysis of Metastatic Regional Lymph Node Locations and Predictors of Para-aortic Lymph Node Involvement in Endometrial Cancer Patients at Risk for Lymphatic Dissemination. Int J Gynecol Cancer 2015; 25: 657-664
• 64 Salehi S, Avall-Lundqvist E, Legerstam B. et al. Robot-assisted laparoscopy versus laparotomy for infrarenal paraaortic lymphadenectomy in women with high-risk endometrial cancer: a randomised controlled trial. Eur J Cancer 2017; 79: 81-89
• 65 Soliman PT, Westin SN, Dioun S. et al. A prospective validation study of sentinel lymph node mapping for high-risk endometrial cancer. Gynecol Oncol 2017; 146: 234-239
• 66 Touhami O, Grégoire J, Renaud MC. et al. Performance of sentinel lymph node (SLN) mapping in high-risk endometrial cancer. Gynecol Oncol 2017; 147: 549-553
• 67 Ducie JA, Eriksson AGZ, Ali N. et al. Comparison of a sentinel lymph node mapping algorithm and comprehensive lymphadenectomy in the detection of stage IIIC endometrial carcinoma at higher risk for nodal disease. Gynecol Oncol 2017; 147: 541-548
• 68 Delpech Y, Cortez A, Coutant C. et al. The sentinel node concept in endometrial cancer: histopathologic validation by serial section and immunohistochemistry. Ann Oncol 2007; 18: 1799-1803
• 69 Holloway RW, Gupta S, Stavitzski NM. et al. Sentinel lymph node mapping with staging lymphadenectomy for patients with endometrial cancer increases the detection of metastasis. Gynecol Oncol 2016; 141: 206-210
• 70 Raimond E, Ballester M, Hudry D. et al. Impact of sentinel lymph node biopsy on the therapeutic management of early-stage endometrial cancer: Results of a retrospective multicenter study. Gynecol Oncol 2014; 133: 506-511
• 71 Bogani G, Mariani A, Paolini B. et al. Low-volume disease in endometrial cancer: The role of micrometastasis and isolated tumor cells. Gynecol Oncol 2019; 153: 670-675
• 72 Kim CH, Soslow RA, Park KJ. et al. Pathologic ultrastaging improves micrometastasis detection in sentinel lymph nodes during endometrial cancer staging. Int J Gynecol Cancer 2013; 23: 964-970
• 73 St Clair CM, Eriksson AG, Ducie JA. et al. Low-Volume Lymph Node Metastasis Discovered During Sentinel Lymph Node Mapping for Endometrial Carcinoma. Ann Surg Oncol 2016; 23: 1653-1659
• 74 Plante M, Stanleigh J, Renaud MC. et al. Isolated tumor cells identified by sentinel lymph node mapping in endometrial cancer: Does adjuvant treatment matter?. Gynecol Oncol 2017; 146: 240-246
• 75 Buda A, Di Martino G, Restaino S. et al. The impact on survival of two different staging strategies in apparent early stage endometrial cancer comparing sentinel lymph nodes mapping algorithm and selective lymphadenectomy: An Italian retrospective analysis of two reference centers. Gynecol Oncol 2017; 147: 528-534
• 76 Schiavone MB, Zivanovic O, Zhou Q. et al. Survival of patients with uterine carcinosarcoma undergoing sentinel lymph node mapping. Ann Surg Oncol 2016; 23: 196-202
• 77 Darai E, Dubernard G, Bats AS. et al. Sentinel node biopsy for the management of early stage endometrial cancer: Long-term results of the SENTI-ENDO study. Gynecol Oncol 2015; 136: 54-59
• 78 Bogani G, Murgia F, Ditto F. et al. Sentinel node mapping vs. lymphadenectomy in endometrial cancer: A systematic review and meta-analysis. Gynecol Oncol 2019; 153: 676-683
• 79 Zahl Eriksson AG, Ducie J, Ali N. et al. Comparison of a sentinel lymph node and a selective lymphadenectomy algorithm in patients with endometrioid endometrial carcinoma and limited myometrial invasion. Gynecol Oncol 2016; 140: 394-399
• 80 Schlappe BA, Weaver AL, Ducie JA. et al. Multicenter study comparing oncologic outcomes between two nodal assessment methods in patients with deeply invasive endometrioid endometrial carcinoma: A sentinel lymph node algorithm versus a comprehensive pelvic and paraaortic lymphadenectomy. Gynecol Oncol 2018; 151: 235-242
• 81 Schlappe BA, Weaver AL, McGree ME. et al. Multicenter study comparing oncologic outcomes after lymph node assessment via a sentinel lymph node algorithm versus comprehensive pelvic and paraaortic lymphadenectomy in patients with serous and clear cell endometrial carcinoma. Gynecol Oncol 2020; 156: 62-69
• 82 Multinu F, Ducie JA, Eriksson AGZ. et al. Role of lymphadenectomy in endometrial cancer with nonbulky lymph node metastasis: Comparison of comprehensive surgical staging and sentinel lymph node algorithm. Gynecol Oncol 2019; 155: 177-185