The current evidence for the use of minimally-invasive surgery in endometrial cancer

The aim of the present study is to review the current available data regarding the use of minimally-invasive surgery in endometrial cancer patients and investigate the feasibility and safety of it for cancer control. We also reviewed the current understanding of sentinel lymph node mapping and the use of robotic surgery in endometrial cancer. Studies have consistently demonstrated better short-term outcomes of minimally-invasive surgery in endometrial cancer compared to laparotomy such as less blood loss, shorter hospital stay, and fewer wound complications. Large randomized clinical trials and meta-analyses also suggest the feasibility and safety of minimally-invasive surgery in terms of oncologic outcomes especially in patients with early stage disease. Although evidence for advanced stage disease and patients with high risk for recurrence are still lacking, the current available data seem to support the use of minimally-invasive surgery for those patient groups as well. A large body of literature supports the role of sentinel lymph node mapping in endometrial cancer with a high sensitivity and a low false negative rate, as well as a favorable negative predictive value. Studies also show that robotic surgery is a safe and effective alternative to conventional laparoscopic surgery for endometrial cancer staging but further long-term data are required. Further prospective studies with long-term follow-up are warranted to evaluate the feasibility and safety of minimally-invasive surgery especially in patients with advanced stage disease and high risk for recurrence. However, the current available data support the use of minimally-invasive surgery in all patient groups of endometrial cancer.

Endometrial cancer; Minimally-invasive surgery; Laparoscopy; Laparotomy; Gynecology

[1] Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians. 2018; 68: 394-424.

[2] Creasman W, Odicino F, Maisonneuve P, Quinn M, Beller U, Benedet J, et al. Carcinoma of the corpus uteri. International Journal of Gynecology & Obstetrics. 2006; 95: S105-S143.

[3] Lu Q, Liu H, Liu C, Wang S, Li S, Guo S, et al. Comparison of laparoscopy and laparotomy for management of endometrial carcinoma: a prospective randomized study with 11-year experience. Journal of Cancer Research and Clinical Oncology. 2013; 139: 1853-1859.

[4] Obermair A, Janda M, Baker J, Kondalsamy-Chennakesavan S, Brand A, Hogg R, et al. Improved surgical safety after laparoscopic compared to open surgery for apparent early stage endometrial cancer: results from a randomised controlled trial. European Journal of Cancer. 2012; 48: 1147-1153.

[5] He H, Zeng D, Ou H, Tang Y, Li J, Zhong H. Laparoscopic treatment of endometrial cancer: systematic review. Journal of Minimally Invasive Gynecology. 2013; 20: 413-423.

[6] 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. Journal of Clinical Oncology. 2009; 27: 5331-5336.

[7] Frumovitz M, dos Reis R, Sun CC, Milam MR, Bevers MW, Brown J, et al. Comparison of total laparoscopic and abdominal radical hysterectomy for patients with early-stage cervical cancer. Obstetrics & Gynecology. 2007; 110: 96-102.

[8] Casarin J, Multinu F, Ubl DS, Dowdy SC, Cliby WA, Glaser GE, et al. Adoption of minimally invasive surgery and decrease in surgical morbidity for endometrial cancer treatment in the United States. Obstetrics & Gynecology. 2018; 131: 304-311.

[9] Malur S, Possover M, Michels W, Schneider A. Laparoscopicassisted vaginal versus abdominal surgery in patients with endometrial cancera prospective randomized trial. Gynecologic Oncology. 2001; 80: 239-244.

[10] Janda M, Gebski V, Davies LC, Forder P, Brand A, Hogg R, et al. Effect of total laparoscopic hysterectomy vs total abdominal hysterectomy on diseasefree survival among women with stage I endometrial cancer. Journal of the American Medical Association. 2017; 317: 1224-1233.

[11] Walker JL, Piedmonte MR, Spirtos NM, Eisenkop SM, Schlaerth JB, Mannel RS, et al. Recurrence and survival after random assignment to laparoscopy versus laparotomy for comprehensive surgical staging of uterine cancer: gynecologic oncology group LAP2 study. Journal of Clinical Oncology. 2012; 30: 695-700.

[12] Malzoni M, Tinelli R, Cosentino F, Perone C, Rasile M, Iuzzolino D, et al. Total laparoscopic hysterectomy versus abdominal hysterectomy with lymphadenectomy for early-stage endometrial cancer: a prospective randomized study. Gynecologic Oncology. 2009; 112: 126-133.

[13] Mourits MJ, Bijen CB, Arts HJ, ter Brugge HG, van der Sijde R, Paulsen L, et al. Safety of laparoscopy versus laparotomy in earlystage endometrial cancer: a randomised trial. The Lancet Oncology. 2010; 11: 763-771.

[14] Galaal K, Donkers H, Bryant A, Lopes AD. Laparoscopy versus laparotomy for the management of early stage endometrial cancer. Cochrane Database of Systematic Reviews. 2018; 10: CD006655.

[15] Smorgick N, Patzkowsky KE, Hoffman MR, Advincula AP, Song AH, As-Sanie S. The increasing use of robot-assisted approach for hysterectomy results in decreasing rates of abdominal hysterectomy and traditional laparoscopic hysterectomy. Archives of Gynecology and Obstetrics. 2014; 289: 101-105.

[16] Scalici J, Laughlin BB, Finan MA, Wang B, Rocconi RP. The trend towards minimally invasive surgery (MIS) for endometrial cancer: an ACSNSQIP evaluation of surgical outcomes. Gynecologic Oncology. 2015; 136: 512-515.

[17] Fader AN, Boruta D, Olawaiye AB, Gehrig PA. Uterine papillary serous carcinoma: epidemiology, pathogenesis and management. Current Opinion in Obstetrics and Gynecology. 2010; 22: 21-29.

[18] Boruta DM, Gehrig PA, Fader AN, Olawaiye AB. Management of women with uterine papillary serous cancer: a Society of Gynecologic Oncology (SGO) review. Gynecologic Oncology. 2009; 115: 142- 153.

[19] Moore KN, Nickles Fader A. Uterine papillary serous carcinoma. Clinical Obstetrics and Gynecology. 2011; 54: 278-291.

[20] Fader AN, Java J, Tenney M, Ricci S, Gunderson CC, Temkin SM, et al. Impact of histology and surgical approach on survival among women with earlystage, highgrade uterine cancer: an NRG Oncology/Gynecologic Oncology Group ancillary analysis. Gynecologic Oncology. 2016; 143: 460-465.

[21] Fader AN, Seamon LG, Escobar PF, Frasure HE, Havrilesky LA, Zanotti KM, et al. Minimally invasive surgery versus laparotomy in women with high grade endometrial cancer: a multisite study performed at high volume cancer centers. Gynecologic Oncology. 2012; 126: 180-185.

[22] Monterossi G, Ghezzi F, Vizza E, Zannoni GF, Uccella S, Corrado G, et al. Minimally invasive approach in type II endometrial cancer: is it wise and safe? Journal of Minimally Invasive Gynecology. 2017; 24: 438-445.

[23] Koskas M, Jozwiak M, Fournier M, Vergote I, Trum H, Lok C, et al. Longterm oncological safety of minimally invasive surgery in highrisk endometrial cancer. European Journal of Cancer. 2016; 65: 185-191.

[24] Vardar MA, Gulec UK, Guzel AB, Gumurdulu D, Khatib G, Seydaoglu G. Laparoscopic surgery for low, intermediate and high-risk endometrial cancer. Journal of Gynecologic Oncology. 2019; 30: e24.

[25] Papadia A, Garbade A, Gasparri ML, Wang J, Radan AP, Mueller MD. Minimally invasive surgery does not impair overall survival in stage IIIC endometrial cancer patients. Archives of Gynecology and Obstetrics. 2020; 301: 585-590.

[26] Kupryjanczyk J, Thor AD, Beauchamp R, Poremba C, Scully RE, Yandell DW. Ovarian, peritoneal, and endometrial serous carcinoma: clonal origin of multifocal disease. Modern Pathology. 1996; 9: 166-173.

[27] Sagae S, Susumu N, Viswanathan AN, Aoki D, Backes FJ, Provencher DM, et al. Gynecologic Cancer InterGroup (GCIG) consensus review for uterine serous carcinoma. International Journal of Gynecologic Cancer. 2014; 24: S83-S89.

[28] Favero G, Anton C, Le X, Silva e Silva A, Dogan NU, Pfiffer T, et al. Oncologic safety of laparoscopy in the surgical treatment of type II endometrial cancer. International Journal of Gynecologic Cancer. 2016; 26: 1673-1678.

[29] Scaletta G, Dinoi G, Capozzi V, Cianci S, Pelligra S, Ergasti R, et al. Comparison of minimally invasive surgery with laparotomic approach in the treatment of high risk endometrial cancer: a systematic review. European Journal of Surgical Oncology. 2020; 46: 782- 788.

[30] Colombo N, Creutzberg C, Amant F, Bosse T, González-Martín A, Ledermann J, et al. ESMO-ESGO-ESTRO consensus conference on endometrial cancer. International Journal of Gynecological Cancer. 2016; 26: 2-30.

[31] Herron DM, Marohn M. A consensus document on robotic surgery. Surgical Endoscopy. 2008; 22: 313-325.

[32] Administration USFaD. Caution when using robotically-assisted surgical devices in women’s health including mastectomy and other cancer-related surgeries: fda safety communication. 2019; Available at: https://www.fda.gov/medical-devices/safety-com munications/caution-when-using-robotically-assisted-surgica l- devices-womens-health-including-mastectomy-and.

[33] Song J, Le T, Hopkins L, Fung-Kee-Fung M, Lupe K, Gaudet M, et al. A comparison of disease recurrence between robotic versus laparotomy approach in patients with intermediate-risk endometrial cancer. International Journal of Gynecologic Cancer. 2020; 30: 160-166.

[34] Xie W, Cao D, Yang J, Shen K, Zhao L. Robot-assisted surgery versus conventional laparoscopic surgery for endometrial cancer: a systematic review and meta-analysis. Journal of Cancer Research and Clinical Oncology. 2016; 142: 2173-2183.

[35] Park DA, Lee DH, Kim SW, Lee SH. Comparative safety and effectiveness of robot-assisted laparoscopic hysterectomy versus conventional laparoscopy and laparotomy for endometrial cancer: a systematic review and meta-analysis. European Journal of Surgical Oncology. 2016; 42: 1303-1314.

[36] Chen S, Li Z, Huang R, Xue H. Robot-assisted versus conventional laparoscopic surgery for endometrial cancer staging: a meta-analysis. Taiwanese Journal of Obstetrics and Gynecology. 2016; 55: 488-494.

[37] Chiou H, Chiu L, Chen C, Yen Y, Chang C, Liu W. Comparing robotic surgery with laparoscopy and laparotomy for endometrial cancer management: a cohort study. International Journal of Surgery. 2015; 13: 17-22.

[38] Gueli Alletti S, Perrone E, Cianci S, Rossitto C, Monterossi G, Bernardini F, et al. 3 mm Senhance robotic hysterectomy: a step towards future perspectives. Journal of Robotic Surgery. 2018; 12: 575-577.

[39] Cianci S, Rosati A, Rumolo V, Gueli Alletti S, Gallotta V, Turco LC, et al. Robotic single-port platform in general, urologic, and gynecologic surgeries: a systematic review of the literature and meta-analysis. World Journal of Surgery. 2019; 43: 2401-2419.

[40] Lim PC, Kang E, Park DH. Learning curve and surgical outcome for robotic-assisted hysterectomy with lymphadenectomy: case-matched controlled comparison with laparoscopy and laparotomy for treatment of endometrial cancer. Journal of Minimally Invasive Gynecology. 2010; 17: 739-748.

[41] Fader AN, Arriba LN, Frasure HE, von Gruenigen VE. Endometrial cancer and obesity: epidemiology, biomarkers, prevention and survivorship. Gynecologic Oncology. 2009; 114: 121-127.

[42] Lau S, Vaknin Z, Ramana-Kumar AV, Halliday D, Franco EL, Gotlieb WH. Outcomes and cost comparisons after introducing a robotics program for endometrial cancer surgery. Obstetrics & Gynecology. 2012; 119: 717-724.

[43] Bell MC, Torgerson J, Seshadri-Kreaden U, Suttle AW, Hunt S. Comparison of outcomes and cost for endometrial cancer staging via traditional laparotomy, standard laparoscopy and robotic techniques. Gynecologic Oncology. 2008; 111: 407-411.

[44] Herling SF, Palle C, Møller AM, Thomsen T, Sørensen J. Cost-analysis of robotic-assisted laparoscopic hysterectomy versus total abdominal hysterectomy for women with endometrial cancer and atypical complex hyperplasia. Acta Obstetricia et Gynecologica Scandinavica. 2016; 95: 299-308.

[45] Leitao MM, Bartashnik A, Wagner I, Lee SJ, Caroline A, Hoskins WJ, et al. Cost-effectiveness analysis of robotically assisted laparoscopy for newly diagnosed uterine cancers. Obstetrics & Gynecology. 2014; 123: 1031-1037.

[46] Salehi S, Åvall-Lundqvist E, Legerstam B, Carlson JW, Falconer H. Robot-assisted laparoscopy versus laparotomy for infrarenal paraaortic lymphadenectomy in women with high-risk endometrial cancer: a randomised controlled trial. European Journal of Cancer. 2017; 79: 81-89.

[47] Reynisson P, Persson J. Hospital costs for robot-assisted laparoscopic radical hysterectomy and pelvic lymphadenectomy. Gynecologic Oncology. 2013; 130: 95-99.

[48] Laursen KR, Hyldgård VB, Jensen PT, Søgaard R. Health care cost consequences of using robot technology for hysterectomy: a register-based study of consecutive patients during 2006-2013. Journal of Robotic Surgery. 2018; 12: 283-294.

[49] Chan JK, Gardner AB, Taylor K, Thompson CA, Blansit K, Yu X, et al. Robotic versus laparoscopic versus open surgery in morbidly obese endometrial cancer patients-a comparative analysis of total charges and complication rates. Gynecologic Oncology. 2015; 139: 300- 305.

[50] Leitao MM, Narain WR, Boccamazzo D, Sioulas V, Cassella D, Ducie JA, et al. Impact of robotic platforms on surgical approach and costs in the management of morbidly obese patients with newly diagnosed uterine cancer. Annals of Surgical Oncology. 2016; 23: 2192-2198.

[51] Wright JD, Ananth CV, Tergas AI, Herzog TJ, Burke WM, Lewin SN, et al. An economic analysis of robotically assisted hysterectomy. Obstetrics & Gynecology. 2014; 123: 1038-1048.

[52] Borgfeldt C, Kalapotharakos G, Asciutto KC, Löfgren M, Högberg T. A population-based registry study evaluating surgery in newly diagnosed uterine cancer. Acta Obstetricia et Gynecologica Scan-dinavica. 2016; 95: 901-911.

[53] Corrado G, Cutillo G, Pomati G, Mancini E, Sperduti I, Patrizi L, et al. Surgical and oncological outcome of robotic surgery compared to laparoscopic and abdominal surgery in the management of endometrial cancer. European Journal of Surgical Oncology. 2015; 41: 1074-1081.

[54] Herling SF, Møller AM, Palle C, Thomsen T. Health-related quality of life after robotic-assisted laparoscopic hysterectomy for women with endometrial cancera prospective cohort study. Gynecologic Oncology. 2016; 140: 107-113.

[55] Corrado G, Chiantera V, Fanfani F, Cutillo G, Lucidi A, Mancini E, et al. Robotic hysterectomy in severely obese patients with endometrial cancer: a multicenter study. Journal of Minimally Invasive Gynecology. 2016; 23: 94-100.

[56] Ballester M, Dubernard G, Lécuru F, Heitz D, Mathevet P, Marret H, et al. Detection rate and diagnostic accuracy of sentinelnode biopsy in early stage endometrial cancer: a prospective multicentre study (SENTI-ENDO). The Lancet Oncology. 2011; 12: 469-476.

[57] Rossi EC, Kowalski LD, Scalici J, Cantrell L, Schuler K, Hanna RK, et al. A comparison of sentinel lymph node biopsy to lymphadenectomy for endometrial cancer staging (FIRES trial): a multicentre, prospective, cohort study. The Lancet Oncology. 2017; 18: 384-392.

[58] Bodurtha Smith AJ, Fader AN, Tanner EJ. Sentinel lymph node assessment in endometrial cancer: a systematic review and meta-analysis. American Journal of Obstetrics and Gynecology. 2017; 216: 459-476.e10.

[59] Daraï E, Dubernard G, Bats A, Heitz D, Mathevet P, Marret H, et al. Sentinel node biopsy for the management of early stage endometrial cancer: long-term results of the SENTIENDO study. Gynecologic Oncology. 2015; 136: 54-59.

[60] Rossi EC, Ivanova A, Boggess JF. Robotically assisted fluorescence-guided lymph node mapping with ICG for gynecologic malignancies: a feasibility study. Gynecologic Oncology. 2012; 124: 78-82.

[61] Chaowawanit W, Campbell V, Wilson E, Chetty N, Perrin L, Jagasia N, et al. Comparison between laparoscopic and robotic surgery for sentinel lymph node mapping in endometrial cancer using indocyanine green and near infrared fluorescence imaging. Journal of Obstetrics and Gynaecology. 2020; 1-5.

[62] Moukarzel LA, Sinno AK, Fader AN, Tanner EJ. Comparing singlesite and multiport robotic hysterectomy with sentinel lymph node mapping for endometrial cancer: surgical outcomes and cost analysis. Journal of Minimally Invasive Gynecology. 2017; 24: 977-983.

[63] Holloway RW, Ahmad S, Kendrick JE, Bigsby GE, Brudie LA, Ghurani GB, et al. A prospective cohort study comparing colorimetric and fluorescent imaging for sentinel lymph node mapping in endometrial cancer. Annals of Surgical Oncology. 2017; 24: 1972-1979.

[64] Ehrisman J, Secord AA, Berchuck A, Lee PS, Di Santo N, Lopez Acevedo M, et al. Performance of sentinel lymph node biopsy in high-risk endometrial cancer. Gynecologic Oncology Reports. 2016; 17: 69-71.

[65] Naoura I, Canlorbe G, Bendifallah S, Ballester M, Daraï E. Relevance of sentinel lymph node procedure for patients with high-risk endometrial cancer. Gynecologic Oncology. 2015; 136: 60-64.

[66] Soliman PT, Westin SN, Dioun S, Sun CC, Euscher E, Munsell MF, et al. A prospective validation study of sentinel lymph node mapping for high-risk endometrial cancer. Gynecologic Oncology. 2017; 146: 234-239.

[67] Touhami O, Grégoire J, Renaud M, Sebastianelli A, Plante M. Performance of sentinel lymph node (SLN) mapping in high-risk endometrial cancer. Gynecologic Oncology. 2017; 147: 549-553.

[68] Bogani G, Murgia F, Ditto A, Raspagliesi F. Sentinel node mapping vs. lymphadenectomy in endometrial cancer: a systematic review and meta-analysis. Gynecologic Oncology. 2019; 153: 676-683.

[69] Gasparri ML, Caserta D, Benedetti Panici P, Papadia A, Mueller MD. Surgical staging in endometrial cancer. Journal of Cancer Research and Clinical Oncology. 2019; 145: 213-221.

[70] Plante M, Stanleigh J, Renaud MC, Sebastianelli A, Grondin K, Gregoire J. Isolated tumor cells identified by sentinel lymph node mapping in endometrial cancer: does adjuvant treatment matter?Gynecologic Oncology. 2017; 146: 240-246.

[71] Peiretti M, Candotti G, Buda A, Zapardiel I, Fanni D, Proto A, et al. Feasibility of handassisted laparoscopic sentinel node biopsy in open endometrial cancer surgery. Minimally Invasive Therapy & Allied Technologies. 2020; 29: 299-303.

[72] Buda A, Dell’Anna T, Vecchione F, Verri D, Di Martino G, Milani R. Nearinfrared sentinel lymph node mapping with indocyanine green using the VITOM II ICG exoscope for open surgery for gynecologic malignancies. Journal of Minimally Invasive Gynecology. 2016; 23: 628-632.

[73] Zuo J, Wu LY, Cheng M, Bai P, Lei CZ, Li N, et al. Comparison study of laparoscopic sentinel lymph node mapping in endometrial carcinoma using carbon nanoparticles and lymphatic pathway verification. Journal of Minimally Invasive Gynecology. 2019; 26: 1125-1132.

[74] Lin H, Ding Z, Kota VG, Zhang X, Zhou J. Sentinel lymph node mapping in endometrial cancer: a systematic review and metaanalysis. Oncotarget. 2017; 8: 46601-46610.

[75] Papadia A, Gasparri ML, Buda A, Mueller MD. Sentinel lymph node mapping in endometrial cancer: comparison of fluorescence dye with traditional radiocolloid and blue. Journal of Cancer Research and Clinical Oncology. 2017; 143: 2039-2048.

[76] Carter J, Huang H, Chase DM, Walker JL, Cella D, Wenzel L. Sexual function of patients with endometrial cancer enrolled in the gynecologic oncology group LAP2 study. International Journal of Gynecological Cancer. 2012; 22: 1624-1633.

[77] Ferguson SE, Panzarella T, Lau S, Gien LT, Samouëlian V, Giede C, et al. Prospective cohort study comparing quality of life and sexual health outcomes between women undergoing robotic, laparoscopic and open surgery for endometrial cancer. Gynecologic Oncology. 2018; 149: 476-483.