Fertility-Sparing Treatment for Early-Stage Cervical Cancer ≥ 2 cm: A Problem with a Thousand Nuances—A Systematic Review of Oncological Outcomes (original) (raw)

Abstract

Background. Fertility-sparing treatments (FSTs) have played a crucial role in the management of early-stage cervical cancer (ECC). The guidelines have recognized various approaches, depending on the tumor stage and other risk factors such as histotype and lymphovascular positivity. Much more debate has centered around the boundary within which these treatments should be considered. Indeed, these are methods to be reserved for ECC, but tumor size may represent the most significant limitation. In particular, there is no consensus on the strategy to be adopted in the case of ECC C 2 cm. Therefore, this systematic review was to collect the literature evidence regarding the management of these patients. Methods. Following the recommendations in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement, we systematically searched the Pubmed and Scopus databases was conducted in April 2022, from the date of the first publication. We made no limitation on the country. We included all studies containing data on disease-free survival, overall survival, recurrence rate (RR), or complete response rate (CRR) to chemotherapy. Results. Twenty-six studies fulfilled the inclusion criteria, and 691 patients were analyzed regarding FST. Surgerybased FST showed an RR of between 0 and 42.9%, which drops to 12.9% after excluding the vaginal or minimally invasive approaches. Furthermore, papers regarding FST based on the neoadjuvant chemotherapy (NACT) approach showed a CRR of between 21.4 and 84.5%, and an RR of between 0 and 22.2% Conclusion. This paper focused on the significant heterogeneity present in the clinical management of FST of ECC C 2 cm. Nevertheless, from an oncological point of view, approaches limited to the minimally invasive or vaginal techniques showed the highest RR. Vice versa, the lack of standardization of NACT schemes and the wealth of confounders to be attributed to the histological features of the tumor make it difficult, if not impossible, to set a standard of treatment. Although the incidence of cervical cancer has shown a downward trend in recent decades, in Western countries the age of first pregnancy has shown an opposite trend, raising its threshold. 1,2 This has resulted in a possible overlapping, making it increasingly common for patients to be diagnosed with early-stage cervical carcinoma (ECC) who have not yet completed their reproductive expectations. Therefore, fertility-sparing treatments (FSTs) have played a crucial role in patient management. The guidelines recognize various approaches, 3,4 depending on the tumor stage and other risk factors such as histotype and lymphovascular positivity. 5 Much more debate has centered around the boundary within which these treatments should be

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (64)

  1. Falcaro M, Castan ˜on A, Ndlela B, Checchi M, Soldan K, Lopez- Bernal J, Elliss-Brookes L, Sasieni P. The effects of the national HPV vaccination programme in England, UK, on cervical cancer and grade 3 cervical intraepithelial neoplasia incidence: a register- based observational study. Lancet. 2021;398(10316):2084-92. h ttps://doi.org/10.1016/S0140-6736(21)02178-4.
  2. du Fosse ´NA, van der Hoorn MP, van Lith JMM, le Cessie S, Lashley EELO. Advanced paternal age is associated with an increased risk of spontaneous miscarriage: a systematic review and meta-analysis. Hum Reprod Update. 2020;26(5):650-69. h ttps://doi.org/10.1093/humupd/dmaa010.
  3. Cibula D, Po ¨tter R, Chiva L, Planchamp F, Avall-Lundqvist E, Cibula D, Raspollini M. The European Society of Gynaecological Oncology/ European Society for Radiotherapy and Oncology/European Society of Pathology guidelines for the management of patients with cervical cancer. Int J Gynecol Cancer. 2018;28(4):641-55. https://doi.org/10\. 1097/IGC.0000000000001216.
  4. Cervical Cancer, Version 3.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Cancer Netw. 2019;17(1):64-84. https://doi.org/10.6004/jnccn.2019.0001.
  5. Bentivegna E, Gouy S, Maulard A, Chargari C, Leary A, Morice P. Oncological outcomes after fertility-sparing surgery for cer- vical cancer: a systematic review. Lancet Oncol. 2016;17(6): e240-53. https://doi.org/10.1016/S1470-2045(16)30032-8.
  6. Delgado G, Bundy B, Zaino R, Sevin BU, Creasman WT, Major F. Prospective surgical-pathological study of disease-free interval in patients with stage IB squamous cell carcinoma of the cervix: a Gynecologic Oncology Group study. Gynecol Oncol. 1990;38: 352-7.
  7. Covens A, Rosen B, Murphy J, et al. How important is removal of the parametrium at surgery for carcinoma of the cervix? Gynecol Oncol. 2002;84:145-9.
  8. Ramirez PT, Frumovitz M, Pareja R, et al. Minimally invasive versus abdominal radical hysterectomy for cervical cancer. N Engl J Med. 2018;379:1895-904.
  9. Moher D. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264. https://doi.org/10.7326/0003-4819-151-4-200908 180-00135.
  10. Kansagara D, O'Neil M, Nugent S, Freeman M, Low A, Kondo K, Elven C, Zakher B, Motu'apuaka M, Paynter R, et al. [Table], Quality Assessment Criteria for Observational Studies, Based on the Newcastle-Ottawa Scale. (2017) https://www.ncbi.nlm.nih.g ov/books/NBK476448/table/appc.t4/. Accessed 16 Aug 2021.
  11. Cao DY, Yang JX, Wu XH, Chen YL, Li L, Liu KJ, Cui MH, Xie X, Wu YM, Kong BH, Zhu GH, Xiang Y, Lang JH, Shen K, China Gynecologic Oncology Group. Comparisons of vaginal and abdominal radical trachelectomy for early-stage cervical cancer: preliminary results of a multi-center research in China. Br J Cancer. 2013;109(11):2778-82. https://doi.org/10.1038/bjc.20 13.656.
  12. de Vincenzo R, Ricci C, Fanfani F, Gui B, Gallotta V, Fagotti A, Ferrandina G, Scambia G. Neoadjuvant chemotherapy followed by conization in stage IB2-IIA1 cervical cancer larger than 2 cm: a pilot study. Fertil Steril. 2021;115(1):148-56. https://doi.org/ 10.1016/j.fertnstert.2020.07.006.
  13. Deng X, Zhang Y, Li D, Zhang X, Guo H, Wang F, Sheng X. Abdominal radical trachelectomy guided by sentinel lymph node biopsy for stage IB1 cervical cancer with tumors C2 cm. Onco- target. 2017;8(2):3422-9. https://doi.org/10.18632/oncotarget. 13788.
  14. Guo J, Zhang Y, Chen X, Sun L, Chen K, Sheng X. Surgical and oncologic outcomes of radical abdominal trachelectomy versus hysterectomy for stage IA2-IB1 cervical cancer. J Minim Invasive Gynecol. 2019;26(3):484-91. https://doi.org/10.1016/j.jmig.2018\. 06.006.
  15. Kim JH, Park JY, Kim DY, Kim YM, Kim YT, Nam JH. Fer- tility-sparing laparoscopic radical trachelectomy for young women with early stage cervical cancer. BJOG. 2010;117(3):340-7. https://doi.org/10.1111/j.1471-0528.2009.02 446.x.
  16. Lanowska M, Mangler M, Speiser D, Bockholdt C, Schneider A, Ko ¨hler C, Vasiljeva J, Al-Hakeem M, Vercellino GF. Radical vaginal trachelectomy after laparoscopic staging and neoadjuvant chemotherapy in women with early-stage cervical cancer over 2 cm: oncologic, fertility, and neonatal outcome in a series of 20 patients. Int J Gynecol Cancer. 2014;24(3):586-93. https://doi. org/10.1097/IGC.0000000000000080.
  17. Li J, Li Z, Wang H, Zang R, Zhou Y, Ju X, Ke G, Wu X. Radical abdominal trachelectomy for cervical malignancies: surgical, oncological and fertility outcomes in 62 patients. Gynecol Oncol. 2011;121(3):565-70. https://doi.org/10.1016/j.ygyno.2011.01.
  18. Li X, Li J, Jiang Z, Xia L, Ju X, Chen X, Wu X. Oncological results and recurrent risk factors following abdominal radical trachelectomy: an updated series of 333 patients. BJOG. 2019;126(9):1169-74. https://doi.org/10.1111/1471-0528.15621.
  19. Lintner B, Saso S, Tarnai L, Novak Z, Palfalvi L, Del Priore G, Smith JR, Ungar L. Use of abdominal radical trachelectomy to treat cervical cancer greater than 2 cm in diameter. Int J Gynecol Cancer. 2013;23(6):1065-70. https://doi.org/10.1097/IGC.0b013 e318295fb41.
  20. Lu Q, Zhang Y, Wang S, Guo S, Guo H, Zhang Z, Liu C. Neoadjuvant intra-arterial chemotherapy followed by total laparoscopic radical trachelectomy in stage IB1 cervical cancer. Fertil Steril. 2014;101(3):812-7. https://doi.org/10.1016/j.fertnst ert.2013.12.001.
  21. Marchiole P, Tigaud JD, Costantini S, Mammoliti S, Buenerd A, Moran E, Mathevet P. Neoadjuvant chemotherapy and vaginal radical trachelectomy for fertility-sparing treatment in women affected by cervical cancer (FIGO stage IB-IIA1). Gynecol Oncol. 2011;122(3):484-90. https://doi.org/10.1016/j.ygyno.201 1.05.010.
  22. Marchiole `P, Ferraioli D, Moran E, Mammoliti S, Tigaud JD, Beurrier F, Chopin N, Mathevet P. NACT and laparoscopic-as- sisted radical vaginal trachelectomy in young patients with large (2-5 cm) high risk cervical cancers: safety and obstetrical out- come. Surg Oncol. 2018;27(2):236-44. https://doi.org/10.1016/j. suronc.2018.04.006.
  23. Okugawa K, Yahata H, Sonoda K, Ohgami T, Yasunaga M, Kaneki E, Kato K. Safety evaluation of abdominal trachelectomy in patients with cervical tumors C2 cm: a single-institution, ret- rospective analysis. J Gynecol Oncol. 2020;31(4):e41. https://doi. org/10.3802/jgo.2020.31.e41.
  24. Pahisa J, Alonso I, Torne ´A. Vaginal approaches to fertility- sparing surgery in invasive cervical cancer. Gynecol Oncol. 2008;110(3 Suppl 2):S29-32. https://doi.org/10.1016/j.ygyno.20 08.05.005.
  25. Park JY, Joo WD, Chang SJ, Kim DY, Kim JH, Kim YM, Kim YT, Nam JH. Long-term outcomes after fertility-sparing laparo- scopic radical trachelectomy in young women with early-stage cervical cancer: an Asan Gynecologic Cancer Group (AGCG) study. J Surg Oncol. 2014;110(3):252-7. https://doi.org/10.1002/ jso.23631.
  26. Plante M, Gregoire J, Renaud MC, Roy M. The vaginal radical trachelectomy: an update of a series of 125 cases and 106 preg- nancies. Gynecol Oncol. 2011;121(2):290-7. https://doi.org/10\. 1016/j.ygyno.2010.12.345.
  27. Rendo ´n GJ, Lopez Blanco A, Aragona A, Saadi JM, Di Guilmi J, Arab Eblen C, Heredia Mun ˜oz F, Pareja R. Oncological and obstetrical outcomes after neo-adjuvant chemotherapy followed by fertility-sparing surgery in patients with cervical cancer C2 cm. Int J Gynecol Cancer. 2021;31(3):462-7. https://doi.org/10\. 1136/ijgc-2020-002076.
  28. Robova H, Halaska MJ, Pluta M, Skapa P, Matecha J, Lisy J, Rob L. Oncological and pregnancy outcomes after high-dose density neoadjuvant chemotherapy and fertility-sparing surgery in cer- vical cancer. Gynecol Oncol. 2014;135(2):213-6. https://doi.org/ 10.1016/j.ygyno.2014.08.021.
  29. Salihi R, Leunen K, Van Limbergen E, Moerman P, Neven P, Vergote I. Neoadjuvant chemotherapy followed by large cone resection as fertility-sparing therapy in stage IB cervical cancer. Gynecol Oncol. 2015;139(3):447-51. https://doi.org/10.1016/j.yg yno.2015.05.043.
  30. Slama J, Cerny A, Dusek L, Fischerova D, Zikan M, Kocian R, Germanova A, Cibula D. Results of less radical fertility-sparing procedures with omitted parametrectomy for cervical cancer: 5years of experience. Gynecol Oncol. 2016;142(3):401-4. http s://doi.org/10.1016/j.ygyno.2016.07.008.
  31. Tesfai FM, Kroep JR, Gaarenstroom K, De Kroon C, Van Loenhout R, Smit V, Trimbos B, Nout RA, van Poelgeest MIE, Beltman JJ. Fertility-sparing surgery of cervical cancer C2 cm (International Federation of Gynecology and Obstetrics 2009 stage IB1-IIA) after neoadjuvant chemotherapy. Int J Gynecol Cancer. 2020;30(1):115-21. https://doi.org/10.1136/ijgc-2019- 000647.
  32. Testa R, Ramirez PT, Ferreyra H, Saadi J, Franco G, Goldsman M, Perrotta M. Abdominal radical trachelectomy: a safe and feasible option for fertility preservation in developing countries. J Low Genit Tract Dis. 2013;17(4):378-84. https://doi.org/10.1097/ LGT.0b013e31827cce89.
  33. Unga ´r L, Pa ´lfalvi L, Hogg R, Siklo ´s P, Boyle DC, Del Priore G, Smith JR. Abdominal radical trachelectomy: a fertility-preserving option for women with early cervical cancer. BJOG. 2005;112(3):366-9. https://doi.org/10.1111/j.1471-0528.2004.00 421.x.
  34. Vercellino GF, Piek JM, Schneider A, Ko ¨hler C, Mangler M, Speiser D, Chiantera V. Laparoscopic lymph node dissection should be performed before fertility preserving treatment of patients with cervical cancer. Gynecol Oncol. 2012;126(3):325-9. https://doi.org/10.1016/j.ygyno.2012.05.033.
  35. Wethington SL, Sonoda Y, Park KJ, Alektiar KM, Tew WP, Chi DS, Leitao MM Jr, Jewell EL, Barakat RR, Abu-Rustum NR. Expanding the indications for radical trachelectomy: a report on 29 patients with stage IB1 tumors measuring 2 to 4 centimeters. Fertility-Sparing Treatment for Early-Stage Cervical… Int J Gynecol Cancer. 2013;23(6):1092-8. https://doi.org/10.10 97/IGC.0b013e318296034e.
  36. Zusterzeel PLM, Aarts JWM, Pol FJM, Ottevanger PB, van Ham MAPC. Neoadjuvant chemotherapy followed by vaginal radical trachelectomy as fertility-preserving treatment for patients with FIGO 2018 stage 1B2 cervical cancer. Oncologist. 2020;25(7):e1051-9. https://doi.org/10.1634/theoncologist.2020- 0063.
  37. Cibula D, McCluggage WG. Sentinel lymph node (SLN) concept in cervical cancer: Current limitations and unanswered questions. Gynecol Oncol. 2019;152(1):202-7. https://doi.org/10.1016/j.yg yno.2018.10.007.
  38. Cibula D, Zikan M, Slama J, Fischerova D, Kocian R, Ger- manova A, Burgetova A, Dusek L, Dundr P, Gregova M, Nemejcova K. Risk of micrometastases in non-sentinel pelvic lymph nodes in cervical cancer. Gynecol Oncol. 2016;143(1):83-6. https://doi.org/10.1016/j.ygyno.2016.07.101.
  39. Lv X, Chen L, Yu H, Zhang X, Yan D. Intra-operative frozen section analysis of common iliac lymph nodes in patients with stage IB1 and IIA1 cervical cancer. Arch Gynecol Obstet. 2012;285(3):811-6. https://doi.org/10.1007/s00404-011-2038-z.
  40. Dı ´az-Feijoo B, Franco S, Torne ´A, Benito V, Herna ´ndez A, Lago V, Rovira R, Acosta U ´, Agustı ´N, Gil-Moreno A, SEGO Spain- GOG Group. Implications of extraperitoneal paraaortic lym- phadenectomy to the left renal vein in locally advanced cervical cancer. A Spanish multicenter study. Gynecol Oncol. 2020;158(2):287-93. https://doi.org/10.1016/j.ygyno.2020.05.
  41. Fanfani F, Monterossi G, Di Meo ML, La Fera E, Dell'Orto F, Gioe `A, Lamanna M, Ferrari D, De Ponti E, Perego P, Restaino S, Carlo R, Zannoni GF, Landoni F, Scambia G, Buda A. Standard ultra-staging compared to one-step nucleic acid amplification for the detection of sentinel lymph node metastasis in endometrial cancer patients: a retrospective cohort comparison. Int J Gynecol Cancer. 2020;30:372-7.
  42. Restaino S, Ronsini C, Finelli A, Perrone E, Scambia G, Fanfani F. Role of blue dye for sentinel lymph node detection in early endometrial cancer. Gynecol Surg. 2017;14(1):23. https://doi.org/ 10.1186/s10397-017-1026-0.
  43. Chen C, Duan H, Zhang W, Zhao H, Wang L, Kang S, Lin L, Zhao W, Ni Y, Li D, Chen J, Fan H, Chen X, Bin X, Lang J, Liu P. Comparison of survival outcomes with or without Para-aortic lymphadenectomy in surgical patients with stage IB1-IIA2 cer- vical cancer in China from 2004 to 2016. BMC Cancer. 2021;21(1):1091. https://doi.org/10.1186/s12885-021-08797-2.
  44. Tsuruga T, Fujimoto A, Kawana K, Mori M, Hasumi Y, Kino N, Tomio K, Miura S, Tanikawa M, Sone K, Miyamoto Y, Ikeda Y, Kojima S, Adachi K, Nagasaka K, Matsumoto Y, Arimoto T, Oda K, Nakagawa S, Horie K, Yasugi T, Yokota H, Osuga Y, Fujii T. Radical hysterectomy with or without para-aortic lymphadenec- tomy for patients with stage IB2, IIA2, and IIB cervical cancer: outcomes for a series of 308 patients. Int J Clin Oncol. 2016;21(2):359-66. https://doi.org/10.1007/s10147-015-0907-3.
  45. Yan DD, Tang Q, Tu YQ, Chen JH, Lv XJ. A comprehensive analysis of the factors of positive pelvic lymph nodes on survival of cervical cancer patients with 2018 FIGO stage IIIC1p. Cancer Manag Res. 2019;11:4223-30. https://doi.org/10.2147/CMAR. S204154.
  46. Salvo G, Odetto D, Saez Perrotta MC, Noll F, Perrotta M, Pareja R, Wernicke A, Ramirez PT. Measurement of tumor size in early cervical cancer: an ever-evolving paradigm. Int J Gynecol Can- cer. 2020;30(8):1215-23. https://doi.org/10.1136/ijgc-2020- 001436.
  47. Zyla RE, Gien LT, Vicus D, Olkhov-Mitsel E, Mirkovic J, Nofech-Mozes S, Djordjevic B, Parra-Herran C. The prognostic role of horizontal and circumferential tumor extent in cervical cancer: Implications for the 2019 FIGO staging system. Gynecol Oncol. 2020;158(2):266-72. https://doi.org/10.1016/j.ygyno.202 0.05.016.
  48. Stolnicu S, Hoang L, Almadani N, De Brot L, Bovolim G, Baiocchi G, Brito MJ, Karpathiou G, Ieni A, Fernandez EG, Kyiokawa T, Dundr P, Parra-Herran C, Le ´rias S, Felix A, Roma A, Pesci A, Oliva E, Soslow RA, Abu-Rustum NR, Park KJ. Horizontal tumor extent (HZTE) has limited prognostic signifi- cance in 2018 FIGO stage I endocervical adenocarcinoma (ECA): a retrospective study of 416 cases. J Cancer Res Clin Oncol. 2022;148(3):577-86. https://doi.org/10.1007/s00432-021-03850- w.
  49. Bhatla N, Berek JS, Cuello Fredes M, Denny LA, Grenman S, Karunaratne K, Kehoe ST, Konishi I, Olawaiye AB, Prat J, Sankaranarayanan R, Brierley J, Mutch D, Querleu D, Cibula D, Quinn M, Botha H, Sigurd L, Rice L, Ryu HS, Ngan H, Ma ¨enpa ¨a J, Andrijono A, Purwoto G, Maheshwari A, Bafna UD, Plante M, Natarajan J. Revised FIGO staging for carcinoma of the cervix uteri. Int J Gynaecol Obstet. 2019;145(1):129-35. https://doi.org/ 10.1002/ijgo.12749.
  50. Di Donato V, Caruso G, Sassu CM, Santangelo G, Bogani G, Plotti F, Sorbi F, Perniola G, Palaia I, Terrin G, Angioli R, Benedetti Panici P, Muzii L. Fertility-sparing surgery for women with stage I cervical cancer of 4 cm or larger: a systematic review. J Gynecol Oncol. 2021;32(6):e83. https://doi.org/10.380 2/jgo.2021.32.e83.
  51. Ditto A, Martinelli F, Bogani G, Fischetti M, Di Donato V, Lorusso D, Raspagliesi F. Fertility-sparing surgery in early-stage cervical cancer patients: oncologic and reproductive outcomes. Int J Gynecol Cancer. 2015;25(3):493-7. https://doi.org/10.1097/ IGC.0000000000000371.
  52. Lin J, Albers AE, Qin J, Kaufmann AM. Prognostic significance of overexpressed p16INK4a in patients with cervical cancer: a meta-analysis. PLoS ONE. 2014;9(9):e106384. https://doi.org/10\. 1371/journal.pone.0106384.
  53. Allam M, Feely C, Millan D, Nevin J, Davis J, Siddiqui N. Depth of cervical stromal invasion as a prognostic factor after radical surgery for early stage cervical cancer. Gynecol Oncol. 2004;93(3):637-41. https://doi.org/10.1016/j.ygyno.2004.02.029.
  54. Sedlis A, Bundy BN, Rotman MZ, Lentz SS, Muderspach LI, Zaino RJ. A randomized trial of pelvic radiation therapy versus no further therapy in selected patients with stage IB carcinoma of the cervix after radical hysterectomy and pelvic lymphadenec- tomy: a Gynecologic Oncology Group Study. Gynecol Oncol. 1999;73(2):177-83. https://doi.org/10.1006/gyno.1999.5387.
  55. Cong Q, Song Y, Wang Q, Zhang H, Gao S, Du M, Xie F, Dong J, Feng H, Diao W, Zhu C, Sui L. A large retrospective study of 12714 cases of LEEP conization focusing on cervical cancer that colposcopy-directed biopsy failed to detect. Biomed Res Int. 2018;2018:5138232. https://doi.org/10.1155/2018/5138232.
  56. Delgado G, Bundy B, Zaino R, Sevin BU, Creasman WT, Major F. Prospective surgical-pathological study of disease-free interval in patients with stage IB squamous cell carcinoma of the cervix: a Gynecologic Oncology Group study. Gynecol Oncol. 1990;38(3):352-7. https://doi.org/10.1016/0090-8258(90)90072- s.
  57. Morice P, Piovesan P, Rey A, Atallah D, Haie-Meder C, Pautier P, Sideris L, Pomel C, Duvillard P, Castaigne D. Prognostic value of lymphovascular space invasion determined with hematoxylin- eosin staining in early stage cervical carcinoma: results of a multivariate analysis. Ann Oncol. 2003;14(10):1511-7. https://d oi.org/10.1093/annonc/mdg412.
  58. Ronsini C, Anchora LP, Restaino S, Fedele C, Arciuolo D, Teodorico E, Bizzarri N, Zannoni GF, Ferrandina G, Scambia G, Fanfani F. The role of semiquantitative evaluation of lympho- vascular space invasion in early stage cervical cancer patients.
  59. Gynecol Oncol. 2021;162(2):299-307. https://doi.org/10.1016/j. ygyno.2021.06.002.
  60. Bizzarri N, Pedone Anchora L, Kucukmetin A, Ratnavelu N, Korompelis P, Carbone V, Fedele C, Bruno M, Vizzielli G, Gallotta V, De Vincenzo R, Chiantera V, Fagotti A, Fanfani F, Ferrandina G, Scambia G. Protective role of conization before radical hysterectomy in early-stage cervical cancer: a propensity- score matching study. Ann Surg Oncol. 2021;28(7):3585-94. h ttps://doi.org/10.1245/s10434-021-09695-4.
  61. Ronsini C, Ko ¨hler C, De Franciscis P, La Verde M, Mosca L, Solazzo MC, Colacurci N. Laparo-assisted vaginal radical hys- terectomy as a safe option for Minimal Invasive Surgery in early stage cervical cancer: a systematic review and meta-analysis.
  62. Gynecol Oncol. 2022. https://doi.org/10.1016/j.ygyno.2022.04\. 010.
  63. Bogani G, Ghezzi F, Chiva L, Gisone B, Pinelli C, Dell'Acqua A, Casarin J, Ditto A, Raspagliesi F. Patterns of recurrence after laparoscopic versus open abdominal radical hysterectomy in patients with cervical cancer: a propensity-matched analysis. Int J Gynecol Cancer. 2020;30(7):987-92. https://doi.org/10.1136/ijg c-2020-001381.
  64. Legge F, Restaino S, Leone L, Carone V, Ronsini C, Di Fiore GLM, Pasciuto T, Pelligra S, Ciccarone F, Scambia G, Fanfani F. Clinical outcome of recurrent endometrial cancer: analysis of post-relapse survival by pattern of recurrence and secondary treatment. Int J Gynecol Cancer. 2020;30(2):193-200. https://doi. org/10.1136/ijgc-2019-000822.