Open Access, Peer-reviewed
pISSN 2005-0380   eISSN 2005-0399
    J Gynecol Oncol. 2024;35:e60. Forthcoming. English.
    Published online Feb 23, 2024.
    https://doi.org/10.3802/jgo.2024.35.e60
    © 2024. Asian Society of Gynecologic Oncology, Korean Society of Gynecologic Oncology, and Japan Society of Gynecologic Oncology
    Original Article

    Comparison of outcomes of laparotomic and minimally invasive radical hysterectomy in women with early-stage cervical cancer

    Shu-Han Chang,1,2,* Kuan-Gen Huang,1,2,3,* Lan-Yan Yang,4 Yu-Bin Pan,5 Chyong-Huey Lai,1,2,3 and Hung-Hsueh Chou1,2,6
      • 1Department of Obstetrics and Gynecology, Chang Gung Memorial Hospital, Linkou Branch and Chang Gung University, Taoyuan, Taiwan.
      • 2Gynecologic Cancer Research Center, Chang Gung Memorial Hospital, Linkou Branch, Taoyuan, Taiwan.
      • 3College of Medicine, Chang Gung University, Taoyuan, Taiwan.
      • 4Division of Clinical Trial, Department of Medical Research, Taichung Veterans General Hospital, Taichung, Taiwan.
      • 5Clinical Trial Center, Linkou Chang Gung Memorial Hospital, Taoyuan, Taiwan.
      • 6School of Medicine, National Tsing Hua University, Hsinchu, Taiwan.
    • Correspondence to Hung-Hsueh Chou. Department of Obstetrics and Gynecology, Chang Gung Memorial Hospital, Linkou Branch, 5 Fu-Shin Street, Kueishan, Taoyuan 333, Taiwan. Email: ma2012@cgmh.org.tw

      *Shu-Han Chang and Kuan-Gen Huang contribute equally to this study.
    Received August 22, 2023; Revised January 03, 2024; Accepted February 11, 2024.

    This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Abstract

    Objective

    This study compared the outcomes of laparotomic radical hysterectomy (LRH) and minimally invasive radical hysterectomy (MISRH) in patients with early-stage cervical cancer.

    Methods

    The clinical data of patients with early-stage cervical cancer who underwent LRH or MISRH (laparoscopic/robotic) at Chang Gung Memorial Hospital, Linkou Branch, from 2002 to 2017 were retrospectively reviewed. The surgical safety (operation time, blood loss, blood transfusion rate, length of postoperative stay, and perioperative complications), overall survival (OS), disease-free survival (DFS), and recurrence pattern were analyzed. Propensity score matching (PSM) at a 3:1 ratio was performed to balance prognostic variables.

    Results

    Of the 760 patients (entire cohort), 614 underwent LRH and 146 underwent MISRH. After PSM, 394 and 140 patients were included in the LRH and MISRH groups, respectively. The 5-year OS rate was significantly lower in the MISRH group than in the LRH group (85.6% vs. 93.2%, p=0.043), and the 5-year DFS rate (p=0.21) did not differ significantly. After PSM, the 5-year OS rates did not differ significantly between the MISRH and LRH groups (87.1% vs. 92.1%, p=0.393). The MISRH group had a significantly shorter operation time (p<0.001), lower intraoperative blood loss (p<0.001), lower blood transfusion rate (p<0.001), and shorter postoperative stay (p<0.001) but a significantly higher rate of intraoperative bladder injury (p<0.001) than the LRH group.

    Conclusion

    After PSM, MISRH is associated with nonsignificantly lower OS but a significantly higher risk of intraoperative urological complications than LRH.

    Synopsis

    In patients with early-stage cervical cancer, overall survival rate was significantly worse in minimally invasive radical hysterectomy (MISRH) group than laparotomic group. After propensity score matching, the difference was not significant. MISRH group is associated with a significantly higher rate of intra-operative bladder injury.

    Graphical Abstract

    Keywords
    Cervical Cancer; Hysterectomy; Laparoscopy; Laparotomy; Minimally Invasive Surgical Procedures

    INTRODUCTION

    Cervical cancer is the third most common cancer and the fourth leading cause of death among women worldwide [1]. Radical hysterectomy (RH) with pelvic lymphadenectomy remains the standard surgical treatment for early-stage cervical cancer, with a high 5-year survival rate.

    Traditionally, RH was performed using laparotomy; however, this approach is associated with high rates of perioperative and long-term complications [2, 3, 4]. With advancements in surgical techniques over the past 2 decades, minimally invasive surgery (MIS) has become the preferred method for gynecological operations, including RH for early-stage cervical cancer [5]. Minimally invasive RH (MISRH) can be performed using a laparoscopic or robotic approach. A series of studies have shown that MISRH is associated with fewer perioperative complications than laparotomic RH (LRH), including lower operative pain, lower blood loss, lower rate of blood transfusion, shorter hospital stay, shorter duration of bladder catheterization, quicker return to normal bowel activity, and faster recovery [6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17].

    However, in 2018, the Laparoscopic Approach to Cervical Cancer (LACC) trial [18], a phase III prospective, multicenter, randomized controlled trial (RCT), provided unexpected results. Compared with open surgery, MISRH was associated with significantly lower disease-free survival (DFS) and overall survival (OS) at 3 years postoperatively. Several retrospective studies comparing the outcomes of MISRH and LRH were also published after the LACC trial. For instance, a study involving 2,461 patients with stage IA2 or IB1 cervical cancer from the National Cancer Database revealed a higher mortality rate in the MISRH group than in the LRH group (9.1% vs. 5.3%, p=0.002) [19]. Chen et al. [20] reported a significantly worse 5-year DFS rate for stage IB1 cervical cancer patients with tumor sizes ≤2 cm in the MISRH group (MISRH group, 90.4% vs. LRH group, 97.7%; p=0.02). Moreover, Margul et al. [21] found that in women with ≥2 cm, stage IB1 cervical tumors, MISRH was associated with a significantly lower 5-year OS rate than LRH (MISRH, 81.3% vs. LRH, 90.8%; p<0.001). However, a recent multicenter retrospective study in the United States revealed that the 3-year OS rates were not significantly different between the MISRH and LRH groups (95.8% vs. 96.0%, p=0.8) [22].

    This study compared the outcomes of patients with early-stage cervical cancer who underwent MISRH and LRH at a tertiary institutional hospital in Taiwan.

    MATERIALS AND METHODS

    1. Patients and study design

    This retrospective study recruited patients with early-stage cervical cancer who underwent RH through laparotomy, laparoscopy, or robotic surgery at Chang Gung Memorial Hospital (CGMH), Linkou Branch, from 2002 to 2017. The study protocol was reviewed and approved by the Institutional Review Board of CGMH (IRB201800803B0), and the study was conducted in accordance with the Declaration of Helsinki. Patients who underwent laparoscopic RH and robotic RH were included in the MISRH group, and the outcomes of patients in the MISRH and LRH groups were compared. The primary endpoints were the OS and DFS rates. The secondary endpoints were the safety of surgery, including operation time, estimated blood loss, blood transfusion rate (from the intraoperative period till postoperative day 7), length of postoperative stay, perioperative complications, and recurrence rate.

    Postoperative radiotherapy/chemoradiotherapy was recommended for high-risk patients: positive pelvic nodes, positive surgical margin or full thickness cervical stromal invasion, or positive parametrium [23]. Patients were identified from the Taiwan Cancer Registry Center, CGMH, and their clinical data were obtained from electronic medical records and medical charts. The survival status of the patients was confirmed using the Taiwan Human Mortality Database.

    Patients were eligible if they had histologically proven cervical cancer of stage IB–IIA according to the staging system of the International Federation of Gynecology and Obstetrics (2018) and had undergone type II or III RH (Piver classification). The exclusion criteria were a history of abdominal or pelvic radiotherapy before the operation, prior diagnosis of other malignancies within 5 years, or recurrence. Patients in the 2 groups were matched through propensity score matching (PSM) to reduce bias in the outcome estimates [24]. To reduce the impact of censoring data on survival estimates, the outcomes of patients lost to follow-up were obtained from the Taiwan Human Mortality Database and Taiwan Cancer Registry Center.

    2. Statistical analysis

    Descriptive statistics were used to summarize cohort characteristics; mean and standard deviation values are reported for continuous variables, and frequencies and percentages are reported for categorical variables. For between-group comparisons, continuous variables were compared using an independent t-test, whereas categorical variables were compared using the Pearson χ2 test or Fisher’s exact test, as appropriate. The Kaplan-Meier method was used to construct the OS and DFS curves, and the differences between groups were compared using a log-rank test. Cox regression analysis was performed to identify the independent predictors of OS and DFS. PSM was performed to compare the effects of LRH and MISRH. The LRH and MISRH groups were matched at a 3:1 ratio by using multiple logistic regression. Six matching variables (age, grade, depth of stromal invasion, pelvic lymph node (LN), parametrial invasion, and stage) were used to balance the potential confounding factors in baseline characteristics. Power analysis was performed to evaluate the type II error resulting from the limitation of the sample size. All analyses were performed using SAS version 9.4 (SAS Institute Inc., Cary, NC, USA). Statistical significance was set at a 2-tailed p-value of <0.05.

    RESULTS

    This study included a total of 760 patients (entire cohort). Of these, 614 patients (80.8%) underwent LRH, and 146 (19.2%) underwent MISRH. In the MISRH group, 139 patients underwent laparoscopic RH, and 7 underwent robotic RH. The median follow-up time was 164.2 months in the LRH group and 131.4 months in the MISRH group. The baseline clinical and pathological characteristics are presented in Table 1. Age (p=0.009), parametrial extension (13% vs. 4.1%, p<0.001), and adenocarcinoma distribution (64.4% vs. 54.4%, p=0.029) significantly differed between the MISRH and LRH groups. After PSM, no differences were noted in the 6 matching variables. The distributions of propensity scores between the groups before and after matching are shown in Supplementary Fig. S1. Compared with the LRH group, the MISRH group had a shorter mean operation time (339.2±83 vs. 281.6±72.2 minutes, p<0.001), lower blood loss (928±707.4 vs. 359.9±329.5 mL, p<0.001), and shorter length of postoperative hospital stay (9.2±3.7 vs. 7.9±3.4 days, p<0.001). The differences in these surgical variables remained significant after PSM.

    Table 1
    Baseline clinical and pathological characteristics

    Table 2 provides a summary of the surgery-related complications based on the Clavien-Dindo classification. The percentage of patients with intraoperative blood loss >1,500 mL was significantly higher in the LRH group than in the MISRH group (p<0.001). By contrast, the MISRH group had a higher incidence of bladder injury (8.2% vs. 0.3%, p<0.001) and ureteral injury (2.7% vs. 0.5%, p=0.029). After PSM, the percentage of patients with intraoperative blood loss >1,500 mL remained significantly higher in the LRH group than in the MISRH group (p<0.001). Moreover, the MISRH group had a significantly higher incidence of bladder injury (p<0.001) and a nonsignificantly higher incidence of ureteral injury (p=0.081) than the LRH group. No statistically significant difference was noted between the 2 groups in terms of colonic injury, obturator nerve or main vessel injury, wound infection/dehiscence, and leg thrombosis before and after PSM. The blood transfusion rate was significantly higher in the LRH group than in the MISRH group (PSM: 56.5% vs. 19.9%, p<0.001, and after PSM: 55.1% vs. 20%, p<0.001, respectively).

    Table 2
    Surgery related complications

    The recurrence rates and failure patterns are shown in Table 3. The distant failure rate was higher in the MISRH cohort than in the LRH cohort, although the result was nonsignificant (11% vs. 6.8%, p=0.092). However, this difference was not evident (p=0.324) after PSM.

    Table 3
    Failure patterns

    In multivariate Cox regression analyses for OS, age (hazard ratio [HR]=1.031, 95% confidence interval [CI]=1.009–1.057, p=0.004), pelvic LN metastasis (HR=2.174, 95% CI=1.246–3.973, p=0.006), parametrial invasion (HR=1.936, 95% CI=1.026–3.654, p=0.041), and tumor histology (squamous cell carcinoma [SCC] vs. non-SCC: HR=0.624, 95% CI=0.400–0.974, p=0.038) were found to be significant predictors. After PSM, age and tumor histology remained significant predictors, whereas pelvic LN metastasis, parametrial invasion, and length of postoperative stay became nonsignificant (Table 4). For DFS, cervical stromal invasion and tumor histology were significant predictors (HR=2.293, 95% CI=1.105–4.757, p=0.026 and HR=0.445, 95% CI=0.247–0.802, p=0.007, respectively) (Supplementary Table S1). Stromal invasion was associated with poor outcomes, whereas SCC was associated with more favorable outcomes. PSM was performed for age, pelvic LN metastasis, parametrial invasion, and tumor histology. After PSM, 394 and 140 patients were included in the LRH and MISRH groups, respectively, in which these significant variables were well balanced (Table 1).

    Table 4
    Multivariate analysis of prognostic variables in the cohort for overall survival

    The OS and DFS curves of the entire cohort are shown in Fig. 1. The 5-year OS rate was significantly lower in the MISRH group than in the LRH group (85.6% vs. 93.2%, p=0.043). The 5-year DFS rate was 86.0% in the MISRH group and 90.0% in the LRH group (p=0.21). After PSM, the 5-year OS rate was lower in the MISRH group than in the LRH group, although nonsignificant (87.1% vs. 92.1%, p=0.393) (Fig. 2). After PSM, the 5-year OS rates of the MISRH and LRH groups and of the subgroups of patients with tumor sizes <2 cm (93.8% vs. 95.7%, p=0.948), 2–4 cm (83.7% vs. 89.2%, p=0.568), and >4 cm (77.3% vs. 87.2%, p=0.484) are presented in Supplementary Fig. S2.

    Fig. 1
    OS (A) and DFS (B) rates between the 2 surgical methods in the entire cohort.
    DFS, disease-free survival; LRH, laparotomic radical hysterectomy; MISRH, minimally invasive radical hysterectomy; OP, operation; OS, overall survival.

    Fig. 2
    OS (A) and DFS (B) rates between the 2 surgical methods in the propensity score–matched cohort.
    DFS, disease-free survival; LRH, laparotomic radical hysterectomy; MISRH, minimally invasive radical hysterectomy; OP, operation; OS, overall survival.

    After PSM, no significant difference was noted in the 5-year DFS rates between the MISRH and LRH groups (86.9% vs. 89.1%, p=0.529) (Fig. 2B) and in the subgroups of patients with tumor sizes <2 cm (95.2% vs. 95.2%, p=0.842), 2–4 cm (87.5% vs. 85.5%, p=0.836), and >4 cm (63.6% vs. 74.3%, p=0.286) (Supplementary Fig. S3). Given the limitation of the sample size in each subgroup after PSM, the power achieved was only 28% for patients with tumor sizes >4 cm and only 55% for the whole propensity score–matched cohort.

    DISCUSSION

    Despite the availability of human papillomavirus vaccination and screening strategies, cervical cancer remains the fourth most common cancer in women globally, with approximately 604,000 new cases and 342,000 deaths being reported in 2020 according to the statistics of the World Health Organization. With an increasing number of patients with early-stage cervical cancer undergoing MISRH in the past 2 decades, the survival outcomes of MISRH compared with LRH has attracted increasing research attention.

    Previous studies comparing the outcomes of different surgical methods have reported varying results. Several meta-analyses have proven that MISRH is safe and results in fewer perioperative complications and faster recovery than open surgery [8, 23, 24, 25, 26, 27]. The SUCCOR study, an international European cohort observational study, concluded that MISRH increased the risks of relapse and death in patients with cervical cancer compared with open surgery [28]. Moreover, in a retrospective cohort study, Cusimano et al. [29] demonstrated that MISRH was associated with increased rates of death and recurrence in patients with stage IB cervical cancer. In a meta-analysis, Wang et al. [30] showed that MISRH was associated with poorer survival outcomes than open surgery. In a retrospective study, Chen et al. [31] reported that traditional LRH had a lower recurrence rate than laparoscopic surgery in patients with tumor size <2 cm.

    This retrospective study compared the long-term survival outcomes of patients with early-stage cervical cancer who underwent MISRH and those who underwent LRH. Before PSM, the 5-year OS rate in the MISRH group was lower than that in the LRH group (p=0.043). After PSM, although the 5-year OS rate was lower and the 5-year DFS rate was approximately 10% lower in patients who underwent MISRH and had tumor size >4 cm, no significant difference was noted in the 5-year OS and 5-year DFS rates between the MISRH and LRH groups and between subgroups of patients with tumor sizes <2 cm, 2–4 cm, and >4 cm. Similar results have been reported in other studies [8, 27]. Nam et al. [32] compared 263 pairs of patients with early-stage cervical cancer who underwent MISRH and LRH and found no difference in survival outcomes between the 2 groups. Moreover, in a matched cohort study, Wang et al. [7] compared 203 pairs of patients who underwent MISRH and LRH, and the results revealed similar 5-year DFS and OS rates in the 2 groups.

    Similar to previous findings [33, 34, 35], in this study, we found that the recurrence rates did not differ significantly between the MISRH and LRH groups. However, a slight nonsignificant increase was noted in the MISRH group for both local and distant sites, which may be attributed to the following reasons: First, the use of a uterine manipulator in MIS may increase the risk of tumor spillage. Second, the use of insufflation gas (carbon dioxide) may cause the abdominal metastasis of tumor cells, as mentioned in other studies [36, 37]. Kong et al. [38] compared disease recurrence rates and noted a higher recurrence rate in the intracorporeal colpotomy group than in the vaginal colpotomy group (16% vs. 5%). The robotic-assisted approach to cervical cancer trial (NCT03719547), an open-label RCT launched in 2019 that aims to enroll 768 subjects [39], will provide valuable evidence for the surgical management of early-stage cervical cancer.

    Our study revealed a shorter operation time, lower blood loss, lower blood transfusion rate, and shorter postoperative hospital stay in the MISRH group; these results are similar to those of other studies [6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16]. The proportion with bladder injury was higher in the MISRH group (7.1% vs. 0.3%, p<0.001) before and after PSM. Moreover, the incidence of ureteral injury was higher in the MISRH group; however, it did not reach statistical significance (2.9% vs. 0.8%, p=0.082) after PSM. The bladder injury rate was significantly higher in the MISRH group than in the LRH group in our study (p<0.001). Similarly, in a meta-analysis of urological complications, the odds ratio was significantly higher (1.97, 95% CI=1.23–3.13) in the MISRH group than in the LRH group [40].

    The strength of this study includes that first, we performed PSM at a 3:1 ratio (LRH:MISRH) to correct the imbalance of characteristics of the 2 groups. Second, a large case number was included and analyzed in a single medical center with well-trained and experienced surgeons. Besides, our results were consistent with those studies previously published. Our retrospective study has some limitations. First, some data were too old to be retrieved from either electronic records or medical charts. Second, the sample size of patients with tumor size >4 cm was relatively small in the MISRH group (n=22, 16.2%) and LRH group (n=39, 9.9%). Finally, power analysis showed only 55% power in the whole propensity score–matched cohort (type II error=0.45).

    In our study on patients with early-stage cervical cancer, MISRH was associated with shorter operation time, lower intraoperative blood loss, lower blood transfusion rate, and shorter postoperative hospital stay but a higher rate of intraoperative bladder injury/perforation than LRH. After PSM, MISRH is associated with non-significantly lower OS, similar 5-year DFS and recurrence rates.

    SUPPLEMENTARY MATERIALS

    Supplementary Table S1

    Multivariate analysis of prognostic variables in the cohort for disease-free survival

    Click here to view.(32K, xls)

    Supplementary Fig. S1

    Propensity score distribution before and after matching.

    Click here to view.(331K, ppt)

    Supplementary Fig. S2

    OS among surgical method in tumor size <2 cm (A), 2–4 cm (B), and >4 cm (C) in propensity score matching cohort.

    Click here to view.(209K, ppt)

    Supplementary Fig. S3

    DFS among surgical method in tumor size <2 cm (A), 2–4 cm (B), and >4 cm (C) in propensity score matching cohort.

    Click here to view.(216K, ppt)

    Notes

    Funding:This study was supported by grants from the Chang Gung Medical Foundation, Taiwan (CORPG3J0421 and CMRPG3K1501-2), National Science and Technology Council (NMRPG3J0551), and Ministry of Health and Welfare, Taiwan (MOHW112-TDU-B-212-144005).

    Conflict of Interest:No potential conflict of interest relevant to this article was reported.

    Author Contributions:

    • Conceptualization: C.

    • Data curation: C.

    • Formal analysis: Y.

    • Writing - original draft: C.

    • Writing - review & editing: C.

    ACKNOWLEDGEMENTS

    The authors thank all the members of the Cancer Center, Chang Gung Memorial Hospital, for their invaluable help.

    References

      1. Arbyn M, Weiderpass E, Bruni L, de Sanjosé S, Saraiya M, Ferlay J, et al. Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis. Lancet Glob Health 2020;8:e191–e203.
      1. Averette HE, Nguyen HN, Donato DM, Penalver MA, Sevin BU, Estape R, et al. Radical hysterectomy for invasive cervical cancer. A 25-year prospective experience with the Miami technique. Cancer 1993;71:1422–1437.
      1. Landoni F, Maneo A, Colombo A, Placa F, Milani R, Perego P, et al. Randomised study of radical surgery versus radiotherapy for stage Ib-IIa cervical cancer. Lancet 1997;350:535–540.
      1. Brooks RA, Wright JD, Powell MA, Rader JS, Gao F, Mutch DG, et al. Long-term assessment of bladder and bowel dysfunction after radical hysterectomy. Gynecol Oncol 2009;114:75–79.
      1. Koh WJ, Abu-Rustum NR, Bean S, Bradley K, Campos SM, Cho KR, et al. Cervical cancer, version 3.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 2019;17:64–84.
      1. 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;24:373–378.
      1. 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;26:1264–1273.
      1. 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.
      1. 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;27:1222–1227.
      1. 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;23:2953–2958.
      1. Park JY, Kim D, Suh DS, Kim JH, Kim YM, Kim YT, et al. The role of laparoscopic radical hysterectomy in early-stage adenocarcinoma of the uterine cervix. Ann Surg Oncol 2016;23:825–833.
      1. Wang W, Li L, Wu M, Ma S, Tan X, Zhong S. Laparoscopic vs. abdominal radical hysterectomy for locally advanced cervical cancer. Front Oncol 2019;9:1331.
      1. Uppal S, Gehrig PA, Peng K, Bixel KL, Matsuo K, Vetter MH, et al. Recurrence rates in patients with cervical cancer treated with abdominal versus minimally invasive radical hysterectomy: a multi-institutional retrospective review study. J Clin Oncol 2020;38:1030–1040.
      1. Kim SI, Lee M, Lee S, Suh DH, Kim HS, Kim K, et al. Impact of laparoscopic radical hysterectomy on survival outcome in patients with FIGO stage IB cervical cancer: a matching study of two institutional hospitals in Korea. Gynecol Oncol 2019;155:75–82.
      1. Paik ES, Lim MC, Kim MH, Kim YH, Song ES, Seong SJ, et al. Comparison of laparoscopic and abdominal radical hysterectomy in early stage cervical cancer patients without adjuvant treatment: ancillary analysis of a Korean Gynecologic Oncology Group Study (KGOG 1028). Gynecol Oncol 2019;154:547–553.
      1. Lee CL, Wu KY, Huang KG, Lee PS, Yen CF. Long-term survival outcomes of laparoscopically assisted radical hysterectomy in treating early-stage cervical cancer. Am J Obstet Gynecol 2010;203:165.e1–165.e7.
      1. Tantitamit T, Huang KG, Lee CL. Laparoscopic versus open radical hysterectomy in women with early stage cervical cancer: a systematic review and meta-analysis. Taiwan J Obstet Gynecol 2020;59:481–488.
      1. 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;379:1895–1904.
      1. 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;379:1905–1914.
      1. 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;30:564–571.
      1. Margul DJ, Yang J, Seagle BL, Kocherginsky M, Shahabi S. Outcomes and costs of open, robotic, and laparoscopic radical hysterectomy for stage IB1 cervical cancer. J Clin Oncol 2018;36:5502.
      1. Leitao MM Jr, Zhou QC, Brandt B, Iasonos A, Sioulas V, Lavigne Mager K, et al. The MEMORY study: MulticentEr study of Minimally invasive surgery versus Open Radical hYsterectomy in the management of early-stage cervical cancer: survival outcomes. Gynecol Oncol 2022;166:417–424.
      1. Lai CH, Chang CJ, Huang HJ, Hsueh S, Chao A, Yang JE, et al. Role of human papillomavirus genotype in prognosis of early-stage cervical cancer undergoing primary surgery. J Clin Oncol 2007;25:3628–3634.
      1. Austin PC. A comparison of 12 algorithms for matching on the propensity score. Stat Med 2014;33:1057–1069.
      1. 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;21:857–862.
      1. Shazly SA, Murad MH, Dowdy SC, Gostout BS, Famuyide AO. Robotic radical hysterectomy in early stage cervical cancer: a systematic review and meta-analysis. Gynecol Oncol 2015;138:457–471.
      1. Cao T, Feng Y, Huang Q, Wan T, Liu J. Prognostic and safety roles in laparoscopic versus abdominal radical hysterectomy in cervical cancer: a meta-analysis. J Laparoendosc Adv Surg Tech A 2015;25:990–998.
      1. Chiva L, Zanagnolo V, Querleu D, Martin-Calvo N, Arévalo-Serrano J, Căpîlna ME, et al. SUCCOR study: an international European cohort observational study comparing minimally invasive surgery versus open abdominal radical hysterectomy in patients with stage IB1 cervical cancer. Int J Gynecol Cancer 2020;30:1269–1277.
      1. 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;221:619.e1–619.24.
      1. Wang Y, Li B, Ren F, Song Z, Ouyang L, Liu K. Survival after minimally invasive vs. open radical hysterectomy for cervical cancer: a meta-analysis. Front Oncol 2020;10:1236.
      1. Chen X, Yu J, Zhao H, Hu Y, Zhu H. Laparoscopic radical hysterectomy results in higher recurrence rate versus open abdominal surgery for stage IB1 cervical cancer patients with tumor size less than 2 centimeter: a retrospective propensity score-matched study. Front Oncol 2021;11:683231
      1. 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;23:903–911.
      1. Sert BM, Boggess JF, Ahmad S, Jackson AL, Stavitzski NM, Dahl AA, et al. Robot-assisted versus open radical hysterectomy: a multi-institutional experience for early-stage cervical cancer. Eur J Surg Oncol 2016;42:513–522.
      1. Shah CA, Beck T, Liao JB, Giannakopoulos NV, Veljovich D, Paley P. Surgical and oncologic outcomes after robotic radical hysterectomy as compared to open radical hysterectomy in the treatment of early cervical cancer. J Gynecol Oncol 2017;28:e82
      1. 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;123:333–336.
      1. Lin F, Pan L, Li L, Li D, Mo L. Effects of a simulated CO2 pneumoperitoneum environment on the proliferation, apoptosis, and metastasis of cervical cancer cells in vitro. Med Sci Monit 2014;20:2497–2503.
      1. Volz J, Köster S, Spacek Z, Paweletz N. The influence of pneumoperitoneum used in laparoscopic surgery on an intraabdominal tumor growth. Cancer 1999;86:770–774.
      1. Kong TW, Chang SJ, Piao X, Paek J, Lee Y, Lee EJ, et al. Patterns of recurrence and survival after abdominal versus laparoscopic/robotic radical hysterectomy in patients with early cervical cancer. J Obstet Gynaecol Res 2016;42:77–86.
      1. Falconer H, Palsdottir K, Stalberg K, Dahm-Kähler P, Ottander U, Lundin ES, et al. Robot-assisted approach to cervical cancer (RACC): an international multi-center, open-label randomized controlled trial. Int J Gynecol Cancer 2019;29:1072–1076.
      1. Hwang JH. Urologic complication in laparoscopic radical hysterectomy: meta-analysis of 20 studies. Eur J Cancer 2012;48:3177–3185.
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