Short-term and Long-term Outcomes in Patients with Early-stage Cervical Cancer, Comparing Clinical and Adjuvant Therapy between Laparoscopic and Open Radical Hysterectomy: A Systematic Review and Meta-analysis
DOI:
https://doi.org/10.3889/oamjms.2023.11688Keywords:
cervical cancer, minimally invasive surgery, outcomes, survivalAbstract
BACKGROUND: Cervical cancer represents one of the most common gynecological malignancies worldwide and the standard treatment has been radical abdominal hysterectomy (RAH). Recent surgical developments can be done through minimally invasive surgery (MIS) using laparoscopic radical hysterectomy (LRH), but the data regarding LRH are still conflicting.
AIM: Therefore, we undertook a systematic review and meta-analysis comparing the short-term and long-term outcomes of laparoscopic versus RAH in women with early-stage cervical cancer.
METHODS: A systematic search was performed within PubMed, Cochrane, Science Direct, and Google Scholar databases to research the outcome of LRH versus RAH in early-stage cervical cancer. Two reviewers independently reviewed titles, abstracts, and full article text to identify studies meeting inclusion and exclusion criteria. If there any discrepancies, it will be resolved by discussion. The Newcastle–Ottawa scale (NOS) was used to assess the risk of bias of non-randomized studies in this analysis. We used Review Manager 5.4 to calculate the result of 95% CI for the outcomes, odds ratio (OR), and mean differences (MD). The endpoints of interest are short-term, during operation, early post-operation, and long-term outcomes.
RESULT: The initial search identified 3.030 citations after a comprehensive review of the final 35 observational studies included, involving 6.919 early-stage cervical cancer patients. Pooled analysis showed that LRH had better intraoperative outcomes, estimated blood loss (EBL) significantly lower LRH (MD = 145.88 [95% CI: 132.84–158.92; p < 0.0001; I2 = 94%]), lesser intraoperative urinary tract injury (OR = 0.91), and vascular injury (OR = 0.76) but was not significant, number of pelvic lymph nodes resected tended to be higher in RAH with MD = 3.63 (95% CI: 3.10–4.15; p < 0.0001; I2 = 95%), shorter bowel recovery time post-operative (MD = 0.05 [95% CI: 0.34–0.66; p < 0.001]). Uniquely, the duration of surgery was not significantly different but still shorter in LRH with MD = 0.73. Long-term outcome was not significantly different for LRH from survival (OR = 1.17) and recurrence (OR = 0.83). LRH had shorter length of stay post-operative (MD = 13.23 [95% CI: 12.98–13.47; p < 0.001; I2 = 100%]) and tend to use significantly fewer adjunctive chemotherapy treatments (OR = 1.84 [95% CI: 1.38–2.45; p < 0.001; I2 = 73%]), the same was seen in radiotherapy treatment (OR = 1.27 [95% CI: 1.03–1.58; p = 0.03; I2 = 68%]).
DISCUSSION: The result demonstrated that for the long-term outcome, there was no significant difference between the two techniques. In general, LRH is considered to be associated with better recovery, smaller scar, and faster back to normal life than ARH. Some comparative studies have reported that survival outcome and perioperative complications after LRH are comparable to those after ARH. However, some study found that MIS was associated with a higher risk of death than open surgery for patients with tumor size ≥2 cm (HR 1.66, 95% CI: 1.19–2.30) and had significantly worse progression-free survival than those in the open surgery group with tumor size >2 cm and ≤4 cm (p = 0.044). This may be because of the use of uterine manipulator or because the difference approaches in handling the vaginal margin. Thus, avoiding tumor spillage and diminishing tumor handling during MIS may be beneficial. A Korean study demonstrated that LRH was associated with a lower total cost of care within 6-month postoperatively than RAH. It appeared that using laparoscopic approach was the least expensive approach from a societal perspective followed by robotic and then abdominal hysterectomy.
CONCLUSION: This systematic review and meta-analysis of observational studies found that among patients who underwent radical hysterectomy for early-stage cervical cancer, LRH had a better outcome in intraoperative, faster post-operative recovery time, and less need for adjunctive therapy.
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Zhao Y, Hang B, Xiong GW, Zhang XW. Laparoscopic radical hysterectomy in early stage cervical cancer: A systematic review and meta-analysis. J Laparoendosc Adv Surg Tech. 2017;27(11):1132-44. https://doi.org/10.1089/lap.2017.0022 PMid:28300465 DOI: https://doi.org/10.1089/lap.2017.0022
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 lymphadenectomy: A Gynecologic Oncology Group Study. Gynecol Oncol. 1999;73(2):177-83. https://doi.org/10.1006/gyno.1999.5387 PMid:10329031 DOI: https://doi.org/10.1006/gyno.1999.5387
Cohen PA, Jhingran A, Oaknin A, Denny L. Cervical cancer. Lancet. 2019;393(10167):169-82. https://doi.org/10.1016/S0140-6736(18)32470-X PMid:30638582 DOI: https://doi.org/10.1016/S0140-6736(18)32470-X
Landoni F, Maneo A, Zapardiel I, Zanagnolo V, Mangioni C. Class I versus class III radical hysterectomy in stage IB1- IIA cervical cancer. A prospective randomized study. Eur J Surg Oncol. 2012;38(3):203-9. https://doi.org/10.1016/j.ejso.2011.12.017 PMid:22244909 DOI: https://doi.org/10.1016/j.ejso.2011.12.017
Raspagliesi F, Bogani G. Radical surgery for cervical cancer. Lancet Oncol. 2019;20(9):1198-9. https://doi.org/10.1016/ S1470-2045(19)30409-7 PMid:31383546 DOI: https://doi.org/10.1016/S1470-2045(19)30409-7
Bhatla N, Aoki D, Sharma DN, Sankaranarayanan R. Cancer of the cervix uteri: 2021 update. Int J Gynaecol Obstet. 2021;155(Suppl 1):28-44. https://doi.org/10.1002/ijgo.13865 PMid:34669203 DOI: https://doi.org/10.1002/ijgo.13865
Cibula D, Pötter R, Planchamp F, Avall-Lundqvist E, Fischerova D, Haie-Meder C, et al. 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 PMid:29688967 DOI: https://doi.org/10.1097/IGC.0000000000001216
National Comprehensive Cancer Network. NCCN Clinical Practice Guidelines in Oncology: Cervical Cancer (Version I. 2018); National Comprehensive Cancer Network: Plymouth Meeting, PA, USA; 2017.
Peters WA 3rd, Liu PY, Barrett RJ 2nd, Stock RJ, Monk BJ, Berek JS, et al. Concurrent chemotherapy and pelvic radiation therapy compared with pelvic radiation therapy alone as adjuvant therapy after radical surgery in high-risk early-stage cancer of the cervix. J Clin Oncol. 2000;18(8):1606-13. https://doi.org/10.1200/JCO.2000.18.8.1606 PMid:10764420 DOI: https://doi.org/10.1200/JCO.2000.18.8.1606
Toptas T, Simsek T. Total laparoscopic versus open radical hysterectomy in stage IA2-IB1 cervical cancer: Disease recurrence and survival comparison. J Laparoendosc Adv Surg Tech A. 2014;24(6):373-8. https://doi.org/10.1089/lap.2013.0514 PMid:24742012 DOI: https://doi.org/10.1089/lap.2013.0514
Wang W, Chu HJ, Shang CL, Gong X, Liu TY, Zhao YH, et al. Long- term oncological outcomes after laparoscopic versus abdominal radical hysterectomy in stage IA2 to IIA2 cervical cancer: A matched cohort study. Int J Gynecol Cancer. 2016;26(7):1264-73. https://doi.org/10.1097/IGC.0000000000000749 PMid:27643649 DOI: https://doi.org/10.1097/IGC.0000000000000749
Wang YZ, Deng L, Xu HC, Zhang Y, Liang ZQ. Laparoscopy versus laparotomy for the management of early stage cervical cancer. BMC Cancer. 2015;15:928. https://doi.org/10.1186/s12885-015-1818-4 PMid:26596955 DOI: https://doi.org/10.1186/s12885-015-1818-4
Zhu T, Chen X, Zhu J, Chen Y, Yu A, Chen L, et al. Surgical and pathological outcomes of laparoscopic versus abdominal radical hysterectomy with pelvic lymphadenectomy and/or para-aortic lymph node sampling for bulky early-stage cervical cancer. Int J Gynecol Cancer. 2017;27(6):1222-7. https://doi.org/10.1097/IGC.0000000000000716 PMid:28640767 DOI: https://doi.org/10.1097/IGC.0000000000000716
Li X, Li J, Wen H, Ju X, Chen X, Xia L, et al. The survival rate and surgical morbidity of abdominal radical trachelectomy versus abdominal radical hysterectomy for stage IB1 cervical cancer. Ann Surg Oncol. 2016;23(9):2953-8. https://doi.org/10.1245/s10434-016-5216-1 PMid:27044448 DOI: https://doi.org/10.1245/s10434-016-5216-1
Lee CL, Huang KG, Jain S, Lee PS, Soong YK. Comparison of laparoscopic and conventional surgery in the treatment of early cervical cancer. J Am Assoc Gynecol Laparosc. 2002;9(4):481-7. https://doi.org/10.1016/s1074-3804(05)60523-3 PMid:12386360 DOI: https://doi.org/10.1016/S1074-3804(05)60523-3
Li G, Yan X, Shang H, Wang G, Chen L, Han Y. A comparison of laparoscopic radical hysterectomy and pelvic lymphadenectomy and laparotomy in the treatment of Ib-IIa cervical cancer. Gynecol Oncol. 2007;105(1):176-80. https://doi.org/10.1016/j.ygyno.2006.11.011 PMid:17197013 DOI: https://doi.org/10.1016/j.ygyno.2006.11.011
Lee EJ, Kang H, Kim DH. A comparative study of laparoscopic radical hysterectomy with radical abdominal hysterectomy for early-stage cervical cancer: A long-term follow-up study. Eur J Obstet Gynecol Reprod Biol. 2011;156(1):83-6. https://doi.org/10.1016/j.ejogrb.2010.12.016 PMid:21269754 DOI: https://doi.org/10.1016/j.ejogrb.2010.12.016
Park JY, Kim DY, Kim JH, Kim YM, Kim YT, Nam JH. Laparoscopic versus open radical hysterectomy for elderly patients with early- stage cervical cancer. Am J Obstet Gynecol. 2012;207(3):195. e1-8. https://doi.org/10.1016/j.ajog.2012.06.081 PMid:22939724 DOI: https://doi.org/10.1016/j.ajog.2012.06.081
Park JY, Kim DY, Kim JH, Kim YM, Kim YT, Nam HJ. Laparoscopic compared with open radical hysterectomy in obese women with early-stage cervical cancer. Obstet Gynecol. 2012;119(6):1201-9. https://doi.org/10.1097/AOG.0b013e318256ccc5 PMid:22617585 DOI: https://doi.org/10.1097/AOG.0b013e318256ccc5
Nam JH, Park JY, Kim DY, Kim JH, Kim YM, Kim YT. Laparoscopic versus open radical hysterectomy in early-stage cervical cancer: Long-term survival outcomes in a matched cohort study. Ann Oncol. 2012;23(4):903-11. https://doi.org/10.1093/annonc/mdr360 PMid:21841155 DOI: https://doi.org/10.1093/annonc/mdr360
Chen CH, Chiu LH, Chang CW, Yen YK, Huang YH, Liu WM. Comparing robotic surgery with conventional laparoscopy and laparotomy for cervical cancer management. Int J Gynecol Cancer. 2014;24(6):1105-11. https://doi.org/10.1097/IGC.0000000000000160 PMid:24927245 DOI: https://doi.org/10.1097/IGC.0000000000000160
Xiao M, Zhang Z. Total laparoscopic versus laparotomic radical hysterectomy and lymphadenectomy in cervical cancer: An observational study of 13-year experience. Medicine (Baltimore). 2015;94(30):e1264. https://doi.org/10.1097/MD.0000000000001264 PMid:26222868 DOI: https://doi.org/10.1097/MD.0000000000001264
Zhang S, Ma L, Meng QW, Zhou D, Moyiding T. Comparison of laparoscopic-assisted radical vaginal hysterectomy and abdominal radical hysterectomy in patients with early stage cervical cancer: A retrospective study. Medicine (Baltimore). 2017;96(36):e8005. https://doi.org/10.1097/MD.0000000000008005 PMid:28885364 DOI: https://doi.org/10.1097/MD.0000000000008005
Guo J, Yang L, Cai J, Xu L, Min J, Shen Y, et al. Laparoscopic procedure compared with open radical hysterectomy with pelvic lymphadenectomy in early cervical cancer: A retrospective study. Onco Targets Ther. 2018;11:5903-8. https://doi.org/10.2147/OTT.S156064 PMid:30271174 DOI: https://doi.org/10.2147/OTT.S156064
Kwon BS, Roh HJ, Lee S, Yang J, Song YJ, Lee SH, et al. Comparison of long-term survival of total abdominal radical hysterectomy and laparoscopy-assisted radical vaginal hysterectomy in patients with early cervical cancer: Korean multicenter, retrospective analysis. Gynecol Oncol. 2020;159(3):642-8. https://doi.org/10.1016/j.ygyno.2020.09.035 PMid:33041070 DOI: https://doi.org/10.1016/j.ygyno.2020.09.035
Chen IN, Wang IT, Mu HY, Qiu JT, Liu WM, Chang CW, et al. Comparison of survival outcomes between minimally invasive surgery and open radical hysterectomy in early-stage cervical cancer. Cancers (Basel). 2022;14(9):2117. https://doi.org/10.3390/cancers14092117 PMid:35565246 DOI: https://doi.org/10.3390/cancers14092117
Lim TY, Lin KK, Wong WL, Aggarwal IM, Yam PK. Surgical and oncological outcome of total laparoscopic radical hysterectomy versus radical abdominal hysterectomy in early cervical cancer in Singapore. Gynecol Minim Invasive Ther. 2019;8(2):53-8. https://doi.org/10.4103/GMIT.GMIT_43_18 PMid:31143623 DOI: https://doi.org/10.4103/GMIT.GMIT_43_18
Kim SI, Lee J, Hong J, Lee SJ, Park DC, Yoon JH. Comparison of abdominal and minimally invasive radical hysterectomy in patients with early stage cervical cancer. Int J Med Sci. 2021;18(5):1312-7. https://doi.org/10.7150/ijms.55017 PMid:33526992 DOI: https://doi.org/10.7150/ijms.55017
Qin M, Siyi L, Huang HF, Li Y, Gu Y, Wang W, et al. A comparison of laparoscopies and laparotomies for radical hysterectomy in stage IA1-IB1 cervical cancer patients: A single team with 18 years of experience. Front Oncol. 2020;10:1738. https://doi.org/10.3389/fonc.2020.01738 PMid:32984056 DOI: https://doi.org/10.3389/fonc.2020.01738
Kong TW, Chang SJ, Lee J, Paek J, Ryu HS. Comparison of laparoscopic versus abdominal radical hysterectomy for FIGO stage IB and IIA cervical cancer with tumor diameter of 3 cm or greater. Int J Gynecol Cancer. 2014;24(2):280-8. https://doi.org/10.1097/IGC.0000000000000052 PMid:24407571 DOI: https://doi.org/10.1097/IGC.0000000000000052
Abu-Rustum NR, Gemignani ML, Moore K, Sonoda Y, Venkatraman E, Brown C, et al. Total laparoscopic radical hysterectomy with pelvic lymphadenectomy using the argon- beam coagulator: Pilot data and comparison to laparotomy. Gynecol Oncol. 2003;91(2):402-9. https://doi.org/10.1016/s0090-8258(03)00518-3 PMid:14599873 DOI: https://doi.org/10.1016/S0090-8258(03)00518-3
Ghezzi F, Cromi A, Ciravolo G, Volpi E, Uccella S, Rampinelli F, et al. Surgicopathologic outcome of laparoscopic versus open radical hysterectomy. Gynecol Oncol. 2007;106(3):502-6. https://doi.org/10.1016/j.ygyno.2007.04.027 PMid:17553554 DOI: https://doi.org/10.1016/j.ygyno.2007.04.027
Malzoni M, Tinelli R, Cosentino F, Fusco A, Malzoni C. Total laparoscopic radical hysterectomy versus abdominal radical hysterectomy with lymphadenectomy in patients with early cervical cancer: Our experience. Ann Surg Oncol. 2009;16(5):1316-23. https://doi.org/10.1245/s10434-009-0342-7 PMid:19224286 DOI: https://doi.org/10.1245/s10434-009-0342-7
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. Obstet Gynecol. 2007;110(1):96-102. https://doi.org/10.1097/01.AOG.0000268798.75353.04 PMid:17601902 DOI: https://doi.org/10.1097/01.AOG.0000268798.75353.04
Estape R, Lambrou N, Diaz R, Estape R, Dunkin N, Rivera A. A case matched analysis of robotic radical hysterectomy with lymphadenectomy compared with laparoscopy and laparotomy. Gynecol Oncol. 2009;113(3):357-61. https://doi.org/10.1016/j.ygyno.2009.03.009 PMid:19345987 DOI: https://doi.org/10.1016/j.ygyno.2009.03.009
Soliman PT, Frumovitz M, Sun CC, Dos Reis R, Schmeler KM, Nick AM, et al. Radical hysterectomy: A comparison of surgical approaches after adoption of robotic surgery in gynecologic oncology. Gynecol Oncol. 2011;123(2):333-6. https://doi.org/10.1016/j.ygyno.2011.08.001 PMid:21872911 DOI: https://doi.org/10.1016/j.ygyno.2011.08.001
Bogani G, Cromi A, Uccella S, Serati M, Casarin J, Pinelli C, et al. Laparoscopic versus open abdominal management of cervical cancer: Long-term results from a propensity-matched analysis. J Minim Invasive Gynecol. 2014;21(5):857-62. https://doi.org/10.1016/j.jmig.2014.03.018 PMid:24699300 DOI: https://doi.org/10.1016/j.jmig.2014.03.018
Taylor SE, McBee WC Jr., Richard SD, Edwards RP. Radical hysterectomy for early stage cervical cancer: Laparoscopy versus laparotomy. JSLS. 2011;15(2):213-7. https://doi.org/10.4293/108680811X13022985132218 PMid:21902978 DOI: https://doi.org/10.4293/108680811X13022985132218
Sert MB, Abeler V. Robot-assisted laparoscopic radical hysterectomy: comparison with total laparoscopic hysterectomy and abdominal radical hysterectomy; one surgeon’s experience at the Norwegian Radium Hospital. Gynecol Oncol. 2011;121(3):600-4. https://doi.org/10.1016/j.ygyno.2011.02.002 PMid:21353294 DOI: https://doi.org/10.1016/j.ygyno.2011.02.002
Ditto A, Martinelli F, Bogani G, Gasparri ML, Di Donato V, Zanaboni F, et al. Implementation of laparoscopic approach for Type B radical hysterectomy: A comparison with open surgical operations. Eur J Surg Oncol. 2015;41(1):34-9. https://doi.org/10.1016/j.ejso.2014.10.058 PMid:25468458 DOI: https://doi.org/10.1016/j.ejso.2014.10.058
Laterza RM, Uccella S, Casarin J, Morosi C, Serati M, Koelbl H, et al. Recurrence of early stage cervical cancer after laparoscopic versus open radical surgery. Int J Gynecol Cancer. 2016;26(3):547-52. https://doi.org/10.1097/IGC.0000000000000627 PMid:26807638 DOI: https://doi.org/10.1097/IGC.0000000000000627
Anagnostopoulos A, Mitra S, Decruze B, Macdonald R, Kirwan J. Safety and cost considerations during the introduction period of laparoscopic radical hysterectomy. Obstet Gynecol Int. 2017;2017:2103763. https://doi.org/10.1155/2017/2103763 PMid:28167964 DOI: https://doi.org/10.1155/2017/2103763
Gil-Moreno A, Carbonell-Socias M, Salicru S, Centeno- Mediavilla C, Franco-Camps S, Colas E, et al. Radical hysterectomy: Efficacy and safety in the dawn of minimally invasive techniques. J Minim Invasive Gynecol. 2019;26(3):492-500. https://doi.org/10.1016/j.jmig.2018.06.007 PMid:29908339 DOI: https://doi.org/10.1016/j.jmig.2018.06.007
Mendivil AA, Rettenmaier MA, Abaid LN, Brown JV 3rd, Micha JP, Lopez KL, et al. Survival rate comparisons amongst cervical cancer patients treated with an open, robotic-assisted or laparoscopic radical hysterectomy: A five year experience. Surg Oncol. 2016;25(1):66-71. https://doi.org/10.1016/j.suronc.2015.09.004 PMid:26409687 DOI: https://doi.org/10.1016/j.suronc.2015.09.004
Corrado G, Vizza E, Legge F, Anchora LP, Sperduti I, Fagotti A, et al. Comparison of different surgical approaches for stage IB1 cervical cancer patients: A multi-institution study and a review of the literature. Int J Gynecol Cancer. 2018;28(5):1020-8. https://doi.org/10.1097/IGC.0000000000001254 PMid:29727351 DOI: https://doi.org/10.1097/IGC.0000000000001254
Zaccarini F, Santy A, Dabi Y, Lavoue V, Carcopino X, Bendifallah S, et al. Comparison of survival outcomes between laparoscopic and abdominal radical hysterectomy for early-stage cervical cancer: A French multicentric study. J Gynecol Obstet Hum Reprod. 2021;50(2):102046. https://doi.org/10.1016/j.jogoh.2020.102046 PMid:33340751 DOI: https://doi.org/10.1016/j.jogoh.2020.102046
Wenzel HH, Smolders RG, Beltman JJ, Lambrechts S, Trum HW, Yigit R, et al. Survival of patients with early-stage cervical cancer after abdominal or laparoscopic radical hysterectomy: A nationwide cohort study and literature review. Eur J Cancer. 2020;133:14-21. https://doi.org/10.1016/j.ejca.2020.04.006 PMid:32422504 DOI: https://doi.org/10.1016/j.ejca.2020.04.006
Sert BM, Kristensen GB, Kleppe A, Dorum A. Long-term oncological outcomes and recurrence patterns in early- stage cervical cancer treated with minimally invasive versus abdominal radical hysterectomy: The Norwegian Radium Hospital experience. Gynecol Oncol. 2021;162(2):284-91. https://doi.org/10.1016/j.ygyno.2021.05.028 PMid:34083029 DOI: https://doi.org/10.1016/j.ygyno.2021.05.028
Ramirez PT, Frumovitz M, Pareja R, Lopez A, Vieira M, Ribeiro R, et al. Minimally invasive versus abdominal radical hysterectomy for cervical cancer. N Engl J Med. 2018;379(20):1895-904. https://doi.org/10.1056/NEJMoa1806395 PMid:30380365 DOI: https://doi.org/10.1056/NEJMoa1806395
Koh WJ, Greer BE, Abu-Rustum NR, Apte SM, Campos SM, Cho KR, et al. Cervical cancer, version 2.2015. J Natl Compr Canc Netw. 2015;13(4):395-404; quiz 404. https://doi.org/10.6004/jnccn.2015.0055 PMid:25870376 DOI: https://doi.org/10.6004/jnccn.2015.0055
Barnett JC, Judd JP, Wu JM, Scales CD Jr., Myers ER, Havrilesky LJ. Cost comparison among robotic, laparoscopic, and open hysterectomy for endometrial cancer. Obstet Gynecol. 2010;116(3):685-93. https://doi.org/10.1097/AOG.0b013e3181ee6e4d PMid:20733453 DOI: https://doi.org/10.1097/AOG.0b013e3181ee6e4d
Melamed A, Margul DJ, Chen L, Keating NL, Del Carmen MG, Yang J, et al. Survival after minimally invasive radical hysterectomy for early-stage cervical cancer. N Engl J Med. 2018;379(20):1905-14. https://doi.org/10.1056/NEJMoa1804923 PMid:30379613 DOI: https://doi.org/10.1056/NEJMoa1804923
Kim SI, Cho JH, Seol A, Kim YI, Lee M, Kim HS, et al. Comparison of survival outcomes between minimally invasive surgery and conventional open surgery for radical hysterectomy as primary treatment in patients with stage IB1-IIA2 cervical cancer. Gynecol Oncol. 2019;153(1):3-12. https://doi.org/10.1016/j.ygyno.2019.01.008 PMid:30642625 DOI: https://doi.org/10.1016/j.ygyno.2019.01.008
Cusimano MC, Baxter NN, Gien LT, Moineddin R, Liu N, Dossa F, et al. Impact of surgical approach on oncologic outcomes in women undergoing radical hysterectomy for cervical cancer. Am J Obstet Gynecol. 2019;221(6):619.e1-24. https://doi.org/10.1016/j.ajog.2019.07.009 PMid:31288006 DOI: https://doi.org/10.1016/j.ajog.2019.07.009
Chen X, Zhao N, Ye P, Chen J, Nan X, Zhao H, et al. Comparison of laparoscopic and open radical hysterectomy in cervical cancer patients with tumor size ≤2 cm. Int J Gynecol Cancer. 2020;30(5):564-71. https://doi.org/10.1136/ijgc-2019-000994 PMid:32276941 DOI: https://doi.org/10.1136/ijgc-2019-000994
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