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Background:
Systematic Review

Surgical Treatment for Endometrial Cancer, Hysterectomy Performed via Minimally Invasive Routes Compared with Open Surgery: A Systematic Review and Network Meta-Analysis

by
Purushothaman Natarajan
1,2,
Gayathri Delanerolle
3,
Lucy Dobson
1,2,
Cong Xu
4,
Yutian Zeng
4,
Xuan Yu
4,
Kathleen Marston
1,
Thuan Phan
1,
Fiona Choi
1,2,
Vanya Barzilova
1,
Simon G. Powell
1,
James Wyatt
1,
Sian Taylor
2,
Jian Qing Shi
4,5 and
Dharani K. Hapangama
1,2,*
1
Department of Women’s & Children’s Health, Institute of Life Course and Medical Sciences, University of Liverpool, Liverpool L8 7SS, UK
2
Liverpool Women’s Hospital NHS Foundation Trust, Liverpool L8 7SS, UK
3
Institute of Applied Health Research, College of Medicine, University of Birmingham, Vincent Drive, Edgbaston B15 2TT, UK
4
Department of Statistics and Data Science, Southern University of Science and Technology, Shenzhen 518055, China
5
National Center for Applied Mathematics Shenzhen, Shenzhen 518038, China
*
Author to whom correspondence should be addressed.
Cancers 2024, 16(10), 1860; https://doi.org/10.3390/cancers16101860
Submission received: 21 February 2024 / Revised: 6 April 2024 / Accepted: 27 April 2024 / Published: 13 May 2024
(This article belongs to the Special Issue Surgical Innovations in Gynecologic Oncology: Endometrial and Ovarian Cancer)
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Abstract

:

Simple Summary

Keyhole surgery has replaced open surgery as the gold standard of care in the surgical treatment of cancer of the womb. Previous reviews comparing keyhole and open surgery exclusively analysed data from randomised control trials. We present a comprehensive review using randomised and non-randomised trials to compare keyhole surgery and open surgery. This review investigates benefits, complications and long-term outcomes in terms of survival after treatment of cancer of the womb, and it shows that keyhole surgery lessened blood loss and the length of hospital stay compared to open surgery. Among the keyhole methods, robotic surgery decreased some complications while rendering the return of cancer less likely.

Abstract

Background: Total hysterectomy with bilateral salpingo-oophorectomy via minimally invasive surgery (MIS) has emerged as the standard of care for early-stage endometrial cancer (EC). Prior systematic reviews and meta-analyses have focused on outcomes reported solely from randomised controlled trials (RCTs), overlooking valuable data from non-randomised studies. This inaugural systematic review and network meta-analysis comprehensively compares clinical and oncological outcomes between MIS and open surgery for early-stage EC, incorporating evidence from randomised and non-randomised studies. Methods: This study was prospectively registered on PROSPERO (CRD42020186959). All original research of any experimental design reporting clinical and oncological outcomes of surgical treatment for endometrial cancer was included. Study selection was restricted to English-language peer-reviewed journal articles published 1 January 1995–31 December 2021. A Bayesian network meta-analysis was conducted. Results: A total of 99 studies were included in the network meta-analysis, comprising 181,716 women and 14 outcomes. Compared with open surgery, laparoscopic and robotic-assisted surgery demonstrated reduced blood loss and length of hospital stay but increased operating time. Compared with laparoscopic surgery, robotic-assisted surgery was associated with a significant reduction in ileus (OR = 0.40, 95% CrI: 0.17–0.87) and total intra-operative complications (OR = 0.38, 95% CrI: 0.17–0.75) as well as a higher disease-free survival (OR = 2.45, 95% CrI: 1.04–6.34). Conclusions: For treating early endometrial cancer, minimal-access surgery via robotic-assisted or laparoscopic techniques appears safer and more efficacious than open surgery. Robotic-assisted surgery is associated with fewer complications and favourable oncological outcomes.

1. Introduction

Endometrial cancer (EC) is the sixth most common cancer in women and the 15th most common cancer overall. Its worldwide incidence is 8.7/10,000 (Age-standardized rate), with more than 417,000 new cases diagnosed in 2020 [1]. EC risk increases with age, and the highest rates are reported in women aged 75–79 [2]. A European Cancer Registry study demonstrated an overall survival of 76% in women diagnosed with EC in the years 2000–2007 [3].
EC typically presents early with postmenopausal bleeding but may also present with persistent intermenstrual and heavy vaginal bleeding associated with features of anovulation [4]. Diagnosis is accomplished through a histological evaluation of an endometrial sample, and surgery is the first-line treatment. The extent of surgery depends on histopathological features such as type, grade and International Federation of Gynaecology and Obstetrics (FIGO) stage. For early-stage EC (FIGO stage 1–2), total hysterectomy with bilateral salpingo-oophorectomy (BSO) is the standard treatment [5], and minimally invasive surgery (MIS) has become the preferred mode. Sentinel node dissection and omental biopsy may be considered in high-risk disease. In stage 2 disease, total hysterectomy with BSO is adequate, but a radical hysterectomy may be required to achieve margin-free resection. Exclusive open surgery (OS) is advocated in advanced disease (FIGO stages 3 and 4), where primary debulking surgery can be considered if associated morbidity and quality of life are acceptable. Palliative surgery also has a role in symptomatic women with advanced EC [5].
The rate of EC is estimated to be increasing, and as the awareness of associated symptoms increases, most women are expected to present with early stages of cancer, for which surgical treatment is often curative. The surgical management of EC, therefore, is an important area of clinical care and research. Current guidelines recommend MIS as the preferred route for early-stage EC (FIGO Stage 1 and 2) based on evidence from randomised control trials (RCTs) demonstrating low post-operative morbidity with comparable oncological outcomes [5,6]. These recommendations are associated with the widespread adoption of MIS in clinical practice. A recent Cochrane review has shown that laparoscopic surgery (LRS) is associated with similar overall survival and recurrence rates with reduced post-operative morbidity. Quality of life (QOL) was better in the LRS group for the first three years; however, after four years, QOL was similar in both groups [7]. RCTs have also demonstrated robotic surgery (RS) to be non-inferior to either standard LRS or OS; however, the available evidence is limited on long-term outcomes of the RS approach [5,8,9,10,11].
RCTs typically only report a handful of possible risks and outcomes. Further useful clinical information may be available from non-randomised studies. In this regard, there have not been sufficient attempts to capture all reported risks associated with the different surgical approaches available for hysterectomy indicated in early-stage EC, which includes evidence from non-randomised studies. Such data help patients with EC and their clinicians in shared decision making regarding surgical treatment while also informing healthcare providers to align their services.
With this background, our aim was to systematically collate the published evidence to determine the comparative surgical and oncological outcomes related to three different surgical treatment options for early stages of EC. Therefore, we systematically reviewed the published evidence from randomised and non-randomised studies reporting clinical and oncological outcomes of both MIS (laparoscopic or robotic) and OS in treating early-stage EC. We believe this will facilitate best practice in shared, informed decision making and the process of consent in the surgical treatment of early-stage EC.

2. Materials and Methods

2.1. Eligibility Criteria, Information Sources, Search Strategy

This study followed the PRISMA statement for systematic reviews and meta-analyses. The study protocol was prospectively registered with PROSPERO (CRD42020186959). A systematic literature search was conducted using PubMed (https://pubmed.ncbi.nlm.nih.gov/), EMBASE (https://www.wolterskluwer.com/en/solutions/ovid/ovid-medline-901), Science Direct (https://www.sciencedirect.com/) and the ISRCTN registry (https://www.wolterskluwer.com/en/solutions/ovid/embase-903), all last accessed on 29 October 2020. The use of MIS for treating EC is relatively recent [12], with the first RCT published in 2002 [13]. Thus, considering the need for at least three years of follow-up to complete long term oncological outcomes, the search was conducted to obtain all clinically relevant data from peer-reviewed, published studies conducted between 1 January 1995 and 31 December 2021. Following duplicate deletion, titles and abstracts were screened by one author (PN) to assess eligibility for full review. The full-text review papers were then evaluated by multiple authors (PN, LD, TP, KM, VB, FC), and the discrepancies were resolved through consensus discussion. Search results were supplemented with the forward and backward chaining of the references for the included studies.

2.2. Study Selection

All peer-reviewed and published studies, including randomised and non-randomised studies that reported outcomes for patients with early-stage EC undergoing a hysterectomy via RS, LRS or OS, were included. All studies reporting hysterectomy for endometrial hyperplasia, benign gynaecological conditions or non-endometrial cancer and studies reported in any other language but English were excluded.

2.3. Data Extraction

Data screening and extraction were completed in line with the inclusion and exclusion criteria by three independent reviewers. Effect sizes, odds ratios (OR), sample size, complication type and geographical location were extracted and developed within a specific data extraction template. All complication details identified within each study were then coded and defined prior to completing the statistical analyses.

2.4. Risk of Bias of Included Studies

The Newcastle Ottawa Quality Assessment Scale (NOS) was used to assess the risk of bias. The studies were evaluated using the following criteria: selection, comparability and exposure. A maximum of four stars was awarded for selection, two for comparability and three for outcomes, with a maximum of nine stars. NOS was used to assess the quality of both randomised and non-randomised studies. The studies were categorised into low risk if they scored 7–9 stars, moderate risk if they scored 5–6 stars and high risk if they scored 0–4 stars. Fifteen studies were in the high-risk group, and the majority (80) were in the low-risk group.

2.5. Synthesis of Results

The primary outcomes extracted from the studies include duration of operation, length of stay in hospital, intra-operative complications (e.g., blood loss), incidence of additional treatments (e.g., blood transfusion), post-operative complications (e.g., fever, infection, ileus), complications of uncertain timing (e.g., VTE), total complications, total intraoperative and post-operative complications and oncological outcomes of disease-free survival and recurrence.
Statistical analyses were undertaken on R version 4.0.2, with the packages “metafor”, “rjags”, and “gemtc”, and RStudio version 1.3.1073.
The ten binary outcomes (blood transfusion, fever, infection, ileus, VTE, total intra-operative complications, total complications, total post-operative complication, recurrence and disease-free survival) were assessed and reported with OR and the corresponding 95% credibility interval (CrI) calculated from absolute numbers or percentages. The four continuous outcomes (blood loss, duration of operating time, length of hospital stay and total number of lymph nodes dissected) were assessed and reported with mean difference (MD) and their computed variances. For studies where only median values and ranges (or interquartile ranges) of continuous outcomes were reported, the results were transformed into means and variances [14].
The network meta-analysis (NMA), a random-effect model, was expanded with a Bayesian method that allowed the inclusion of direct and indirect comparisons of the surgical techniques used, allowing for a better understanding of the data [15,16,17]. The simultaneous inference of the evidence, considering the three surgical interventions, was facilitated by a data structure that could be regarded as a k-comparison to synthesise the available evidence. In line with this, the research question: “What is the prevalence of complications associated with three surgical techniques used among EC patients?” was developed and answered via the following distinct aims. The prevalence of peri-operative and oncological complications associated with RS versus LRS versus OS, as well as their rating, assessment of performance and clinical effectiveness defined by the rate of complications associated with each surgical method, were investigated. The Markov Chain Monte Carlo (MCMC) simulation was applied to estimate the posterior distributions of the model parameters and generate the results. The convergence of the MCMC process was assessed by evaluating the trace plots, and the consistency assumption was checked by performing a node-split analysis, which evaluates every comparison of interest using a separate model [18].
For the interpretation of the Bayesian NMA results, Forest plots, Rankograms and surface under the cumulative ranking (SUCRA) plots were used [19,20]. Based on an interim empirical evaluation of the last decade, a trend of moving away from OS to LRS and RS was observed within the pooled studies. As a result, to assess the possible time trend of the outcomes, a meta-regression of each identified outcome based on the time period of the study was performed. The study year of all publications included was utilised as the midpoint of the study duration using the following formula:
Study year = (study start year + study end year)/2
The estimated regression coefficients of the study years were examined to report time trends based on current empirical evidence reported from practitioners.

3. Results

3.1. Study Characteristics

The initial search yielded 74,322 references, from which 59,783 duplicates were removed, and the remaining 14,539 records were screened to select 874 relevant publications to assess the abstracts for eligibility. A total of 194 studies [9,13,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132,133,134,135,136,137,138,139,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173,174,175,176,177,178,179,180,181,182,183,184,185,186,187,188,189,190,191,192,193,194,195,196,197,198,199,200,201,202,203,204,205,206,207,208,209,210,211,212,213,214], with 245,408 women, were included in the review (Table 1), and out of them, a total of 99 [9,23,24,26,30,32,36,39,42,43,47,49,51,52,53,54,56,57,59,63,67,68,70,71,76,77,78,79,81,82,84,85,87,88,89,90,94,96,100,102,105,110,111,112,113,114,119,122,123,124,128,132,134,135,136,138,139,143,145,153,154,159,164,165,167,168,169,170,171,172,173,177,178,180,181,182,183,184,186,187,188,190,192,194,195,196,198,200,201,202,208,209,210,212,213,214,215,216,217,218,219], comprising five RCTs and 94 cohort studies, were included in the NMA. The types of studies are detailed in the study characteristics and included 181,716 women. The PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) diagram (Figure 1) illustrates the process of elimination. Detailed characteristics and a quality analysis of a subset of the studies included in the current systematic review and meta-analysis are listed in Table 1. The NMA utilised 14 outcomes, while those for other outcomes reported in fewer than ten studies were omitted (Table 2).

3.2. Intra-Operative Outcomes (Figure 2 and Figure 3, Table 2, Table 3 and Table 4)

3.2.1. Blood Loss

Compared with OS, LRS and RS demonstrated statistically significant differences of −226.90 millilitre (mL) (95% CrI: −298.40–−155.90) and −257.20 mL (95% CrI: −351.20–−163.80) of Blood loss, respectively. This suggests that patients undergoing LRS or RS had significantly less blood loss than those undergoing OS. However, the difference between RS and LRS was not statistically significant, with an MD of −30.33 (95% CrI: −122.2–61.62).
Table 3. SUCRA (surface under the cumulative ranking) scores of the three surgical techniques (LRS: laparoscopic surgery, OS: open surgery, RS: robotic surgery) for the 14 outcomes from the Bayesian network meta-analysis. The significant differences are shown in bold.
Table 3. SUCRA (surface under the cumulative ranking) scores of the three surgical techniques (LRS: laparoscopic surgery, OS: open surgery, RS: robotic surgery) for the 14 outcomes from the Bayesian network meta-analysis. The significant differences are shown in bold.
OutcomeOSLRSRS
Blood Loss0.00000.62750.8725
Duration of Operation0.99960.44960.0508
Length of Stay in Hospital0.00000.65760.8424
Total Lymph Nodes0.59240.32000.5877
Blood Transfusion0.00020.66610.8338
Fever0.07830.66830.7533
Infection0.17570.93190.3925
Ileus0.00050.50550.9941
VTE0.15670.86880.4745
Disease-free Survival0.06160.45090.9876
Recurrence0.03930.76060.7001
Total Complications0.00000.61940.8806
Total Intra-operative Complications0.30170.20140.9969
Total Post-operative Complications0.00140.71180.7868
Table 4. Results of meta-regressions on study year for the 14 outcomes. The significant differences are demonstrated in bold.
Table 4. Results of meta-regressions on study year for the 14 outcomes. The significant differences are demonstrated in bold.
Outcome k β SE   of   β p-Value
Blood LossLRS vs. OS411.27849.75500.8957
RS vs. OS16−6.752917.61530.7015
RS vs. LRS1815.89814.39150.0003
Duration of OperationLRS vs. OS39−2.35691.19870.0493
RS vs. OS15−4.91623.29480.1357
RS vs. LRS140.69723.16500.8257
Length of Stay in HospitalLRS vs. OS440.02410.07020.7317
RS vs. OS130.07730.29570.7939
RS vs. LRS130.18580.17940.3003
Total Lymph NodesLRS vs. OS12−0.33100.22250.1368
Blood TransfusionLRS vs. OS19−0.09150.03800.0160
FeverLRS vs. OS100.00570.06990.9344
InfectionLRS vs. OS16−0.03950.05250.4523
Disease-free SurvivalLRS vs. OS110.00980.02620.7087
RecurrenceLRS vs. OS200.01300.03340.6983
Total ComplicationsLRS vs. OS240.04140.02130.0526
RS vs. LRS110.14150.06740.0357
Total Intra-operative ComplicationsLRS vs. OS14−0.04480.03780.2369
Total Post-operative ComplicationsLRS vs. OS20−0.00580.04380.8950
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Figure 2. Results of the node-split analysis checking consistency and assumptions. The effect sizes and 95% credible intervals from direct comparison, indirect comparison and the network combining the two are shown in Figure 2. The p-values in this context were used to test the consistency between direct and indirect comparisons. Figure 2 demonstrates that the consistency assumption is generally satisfied for 11 outcomes. The remaining three outcomes, fever, disease-free survival and total-intraoperative complications, were not shown due to insufficient data. (LRS: laparoscopic surgery, OS: open surgery, RS: robotic surgery).
Figure 2. Results of the node-split analysis checking consistency and assumptions. The effect sizes and 95% credible intervals from direct comparison, indirect comparison and the network combining the two are shown in Figure 2. The p-values in this context were used to test the consistency between direct and indirect comparisons. Figure 2 demonstrates that the consistency assumption is generally satisfied for 11 outcomes. The remaining three outcomes, fever, disease-free survival and total-intraoperative complications, were not shown due to insufficient data. (LRS: laparoscopic surgery, OS: open surgery, RS: robotic surgery).
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Figure 3. Shows the forest plots of the 14 outcomes, providing the pooled estimates of the effect size of each surgery technique compared to open surgery (OS). (LRS: laparoscopic surgery, OS: open surgery, RS: robotic surgery).
Figure 3. Shows the forest plots of the 14 outcomes, providing the pooled estimates of the effect size of each surgery technique compared to open surgery (OS). (LRS: laparoscopic surgery, OS: open surgery, RS: robotic surgery).
Cancers 16 01860 g003

3.2.2. Duration of Operating Time

There were statistically significant increases in the duration of operating time of 18.95 min (95% CrI: 7.68–30.20) with LRS and 29.00 min (95% CrI: 13.66–44.23) with RS compared with OS, respectively. This suggests that patients undergoing LRS or RS had a significantly longer duration of operation than those undergoing OS. The difference between RS and LRS is not statistically significant (MD = 10.05 min, 95% CrI: −5.60–25.48).

3.2.3. Total Lymph Nodes Resected

There was no statistically significant difference for LRS and RS, with mean differences of 0.4 (95% CrI: −1.18–2.01) and −0.06 (95% CrI: −2.91–2.69) compared with OS, respectively. Furthermore, the difference between RS and LRS is not statistically significant, with an MD of −0.46 (95% CrI: −2.91–2.09).

3.3. Post-Operative Outcomes (Figure 2 and Figure 3, Table 2, Table 3 and Table 4)

For the comparison between LRS and OS, there were statistically significant differences in the following post-operative binary outcomes: blood transfusion (OR = 0.30, 95% CrI: 0.19–0.48), fever (OR = 0.57, 95% CrI: 0.30–0.98), infection (OR = 0.50, 95% CrI: 0.28–0.93), ileus (OR = 0.46, 95% CrI: 0.29–0.68), total complications (OR = 0.38, 95% CrI: 0.29, 0.51), total post-operative complications (OR = 0.48, 95% CrI: 0.34–0.70). These results suggest that patients undergoing LRS had a significantly lower incidence of blood transfusion, fever, infection, ileus, recurrence, total complications and total post-operative complications than those undergoing OS. On the other hand, the incidence of VTE, disease-free survival and total intra-operative complications were not significantly different between LRS and OS.
Comparing RS with OS, there were statistically significant differences in the following binary post-operative outcomes: blood transfusion (OR = 0.26, 95% CrI: 0.12–0.53), ileus (OR = 0.18, 95% CrI: 0.08–0.41), total complications (OR = 0.34, 95% CrI: 0.22–0.51), total intra-operative complications (OR = 0.39, 95% CrI: 0.18–0.78), total post-operative complications (OR = 0.46, 95% CrI: 0.27–0.78). These results suggest that patients undergoing RS had a significantly lower incidence of blood transfusion, ileus, total complications, total intra-operative complications and total post-operative complications and better disease-free survival than those undergoing OS. On the other hand, the incidence of fever, infection and VTE was not significantly different between RS and OS.
When RS was compared with LRS, there were statistically significant differences in two binary post-operative outcomes: ileus (OR = 0.40, 95% CrI: 0.17–0.87) and total intra-operative complications (OR = 0.38, 95% CrI: 0.17–0.75). These results suggest that patients undergoing RS had a significantly lower incidence of ileus and total intra-operative complications than those undergoing LRS. The incidence of other binary outcomes was not significantly different between RS and LRS.

Length of Hospital Stay

Compared with OS, there was a statistically significant reduction in the length of hospital stay in women who underwent LRS and RS with mean differences of −3.54 days (95% CrI: −4.22–−2.87) and −3.79 days (95% CrI: −4.79–−2.79), respectively. This suggests that patients undergoing MIS had a significantly shorter length of stay in hospital than those undergoing OS. The difference between RS and LRS is not statistically significant (MD = −0.25 days, 95% CrI: −1.26–0.77).

3.4. Oncological Outcomes (Figure 2 and Figure 3, Table 2, Table 3 and Table 4)

There was a significant reduction in the binary outcomes of cancer recurrence (OR = 0.64, 0.47–0.84) with LRS compared to OS. The incidence of disease-free survival was not significantly different between LRS and OS.
When RS was compared with OS, there was a significantly higher disease-free survival (OR = 3.29, 95% CrI: 1.46–8.36) associated with this method, but recurrence was not significantly different between RS and OS.
Compared with LRS, RS was associated with significantly higher disease-free survival (OR = 2.45, 95% CrI: 1.04–6.34), but the other oncology outcomes appear to be similar between the two approaches.

3.5. Ranking Analysis (Figure 2 and Table 2 and Table 3)

Ranking analysis indicates that OS is the best technique when the duration of operation or total lymph nodes are considered, LRS is the best technique when incidences of infection, VTE and recurrence are considered, and RS is the best technique when blood loss, length of stay in hospital, disease-free survival and incidences of blood transfusion, fever, ileus, total complications, total intra-operative complications and total post-operative complications are considered.

3.6. Meta-Regression Analysis (Figure 4 and Table 4)

A meta-regression analysis was conducted for each outcome in line with the study timelines to study the possible time trend on the outcomes.
The study year did not significantly affect comparisons among the three surgical techniques on most outcomes. However, time trend was significant in four cases: comparison between LRS vs. OS on duration of operation (estimated regression coefficient −2.3596 (p = 0.0493)), comparison between RS vs. LRS on blood loss (estimated regression coefficient 15.8981 (p = 0.0003)), comparison between LRS vs. OS on blood transfusion (estimated regression coefficient −0.0915 (p = 0.0160)) and comparison between RS vs. LRS on total complications (estimated regression coefficient 0.1415 (p = 0.0357)) (Figure 4).
These data suggest that some differences between techniques appear to reduce in magnitude with time. For example, the initial longer duration of operation between LRS and OS became smaller over time. Similarly, the difference in blood loss between RS and LRS also reduced over time.
Conversely, the difference in a lower incidence of blood transfusion between LRS and OS increased over time. Although the earlier studies reported a lower incidence of total complications in patients undergoing RS vs. LRS, the more recent studies reported contrastingly lower total complication rates with LRS than RS.
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Figure 4. Forest plots of the Bayesian network meta-analyses for each of the 14 outcomes.
Figure 4. Forest plots of the Bayesian network meta-analyses for each of the 14 outcomes.
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4. Discussion

4.1. Principal Findings

4.1.1. Robotic-Assisted Surgery

The superiority of RS in disease-free survival, when compared with either OS or LRS, is of key interest. RS also demonstrated improved peri-operative outcomes, including a reduction in blood loss, length of stay in hospital, total intra-operative complications and incidences of blood transfusion, fever, ileus, total post-operative complications and total complications according to the ranking analysis. However, the recommendation of RS as the best option for hysterectomy for early EC should be made with caution since the meta-regression analysis demonstrated a possible increase in total complications associated with the RS route compared to LRSs. There has been an increasing number of surgeons learning and performing hysterectomies via the RS route in recent years as opposed to the highly experienced specialists as in early studies, and thus increasing numbers of RS cases may explain these findings. Nevertheless, future studies should focus on further examining this trend.

4.1.2. Laparoscopic Surgery

The LRS approach appears to be the best technique to consider when the reduction of incidences of infection, VTE, and recurrence is desired according to the ranking analysis. However, OS faired best when reducing the duration of operation or increasing the total number of lymph nodes to be harvested. This information is vital for service planning and future directions in the management of EC. The main disadvantage of LRS is that the duration of surgery appears to reduce with time, according to our meta-regression analysis, possibly due to increasing skills in LRS.

4.2. Comparison with Existing Literature

This study presents a comprehensive systematic review including 194 manuscripts and an NMA comprising 99 papers, demonstrating the significant superiority of MIS for early-stage EC, compared with OS in multiple aspects. Although the duration of surgery was slightly longer, MIS was associated with significantly lower rates of complications during and after surgery, in conjunction with a possible superiority in oncological outcomes, compared with those who underwent OS. MIS approaches were also associated with a reduced duration of hospital stay, which relates to reduced health service costs. Our findings are consistent with the Cochrane review [7] on LRS for EC and large RCTs such as LACE [21] and LAP2 [22]. OS was associated with a higher incidence of post-operative complications such as Fever, infection and ileus compared with MIS. Previous Cochrane reviews and other RCTs [23] have shown comparable rates of recurrence and disease-free survival with the OS or MIS approach, yet our review has shown that MIS (LRS or RS) is associated with lower recurrence and better disease-free survival. The reasons for these observations are unclear but may be due to increasing expertise in MIS over recent years and possible selection bias, where high-risk ECs were preferentially treated by OS. However, with the recent advent of robotic surgery, high-risk patients, for example, with morbid obesity have been particularly assigned to undergo surgery via MIS route, and thus this data may be a true reflection of superior outcomes.

4.3. Strengths and Limitations

The main strength of this study is the inclusion of all relevant published data from both RCTs and cohort studies. By including data from cohort studies that were excluded by previous systematic reviews, our study represents, to our knowledge, the most comprehensive summary to date of peri- and post-operative and oncological outcomes associated with surgical treatment for early EC. This data thus could provide a solid foundation for developing core outcomes for hysterectomy for EC. The inclusion of observational data limits causal inferences and inevitably is subjected to carryover confounding bias. Non-standardised outcome reporting limited the number of studies that could be included in the analysis. We did not formally investigate selection bias.
It is also important to note that trends in endometrial cancer staging surgery have changed over time (with improved pre-operative imaging and molecular subtyping influencing the extent of surgery [6]). In particular, the advent of sentinel lymph node biopsy has resulted in far fewer systematic pelvic and para-aortic lymph node dissections, thus reducing associated risks and morbidity. However, this practice varies considerably between institutions. Facilities for sentinel lymph node biopsy are not universally available, and not all institutions have the expertise to perform laparoscopic lymph node dissections. These variations in practice and techniques (e.g., new minimal access approaches including natural orifice transvaginal endoscopic surgery (NOTES), laparo-endoscopic single site (LESS) surgery and robotic single-site surgery) will introduce heterogeneity to the studies. Therefore, discussion regarding the risks of surgery should be tailored to the patient, surgeons and the cancer unit, considering the anticipated complexity of the planned operation and locally available expertise and resources when assessing the relevance of the outcomes reported here. The majority of studies included compared outcomes for different surgical approaches within the same institution(s), and we have included a large number of studies from a large geographical area. Thus, it is reasonable to assume heterogeneity within each surgical approach for the findings to be generalisable.

5. Conclusions

MIS, via either the robotic or the laparoscopic route, appears to be a safer and more efficacious approach when compared with OS for the treatment of early EC. The MIS approach is associated with fewer complications with favourable oncological outcomes. Time trends on outcomes, identified in our meta-regression analysis, provide vital information for policymakers and researchers to use in future-proofing health services and clinical trials.

Author Contributions

Conceptualization P.N., L.D., G.D. and D.K.H.; Data curation P.N., L.D., K.M., T.P., F.C., V.B., S.G.P. and J.W.; Formal analysis G.D., C.X., Y.Z., X.Y. and J.Q.S.; Methodology G.D. and J.Q.S.; Software G.D. and J.Q.S.; Supervision G.D., J.Q.S., S.T. and D.K.H.; Roles/Writing—original draft G.D., P.N., D.K.H.; and Writing—review & editing all authors. All authors have read and agreed to the published version of the manuscript.

Funding

P.N. and L.D. were supported by a Clinical Research Fellowship from the Liverpool Women’s Hospital NHS Foundation Trust. D.K.H. is supported by the Wellbeing of Women (RG2137) and MRC (MR/V007238/1). D.K.H. has received payment for presentations from Theramex and Gideon Richter.

Data Availability Statement

All data are available to share, either in the material submitted with the manuscript or upon request from the authors.

Acknowledgments

Liverpool Women’s Hospital Foundation Trust, Wellbeing of Women (RG2137) and MRC (MR/V007238/1).

Conflicts of Interest

P.N. and L.D. were supported by a Clinical Research Fellowship from the Liverpool Women’s Hospital NHS Foundation Trust. D.K.H. is supported by the Wellbeing of Women (RG2137) and MRC (MR/V007238/1). D.K.H. has received payment for presentations from Theramex and Gideon Richter. The remaining authors have no competing interests to report.

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Cancers 16 01860 g001
Figure 1. The PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) diagram.
Figure 1. The PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) diagram.
Cancers 16 01860 g001
Table 1. Characteristics of the 194 studies included in the qualitative synthesis.
Table 1. Characteristics of the 194 studies included in the qualitative synthesis.
AuthorYear of StudySample SizeType of StudyComparator
Abel et al. [21]20201805Retrospective Cohort Study Laparoscopic
Abitbol et al. [22]2016340Retrospective Cohort StudyRobotic
Agarwal et al. [23]2018133Retrospective Cohort StudyRobotic/Open
Aiko et al. [24]2020223Retrospective Cohort StudyLaparoscopic/Robotic
Ansar et al. [25]201860Prospective Non-Randomized Control Study Laparoscopic/Open
Api et al. [26]201379Retrospective Cohort StudyLaparoscopic/Open
Armfield et al. [27]2018404Randomized Controlled TrialLaparoscopic/Open
Avondstond et al. [28]201740Retrospective Cohort StudyRobotic
Backes et al. [29]2015543Retrospective Cohort StudyRobotic
Backes et al. [30]2016182Retrospective Cohort StudyRobotic/Open
Baek et al. [31]2014278Retrospective Cohort StudyLaparoscopic
Bajaj et al. [32]199970Retrospective Cohort StudyLaparoscopic/Open
Baker et al. [33]2013760Randomized Controlled TrialLaparoscopic/Open
Baker et al. [34]2015760Randomized Controlled TrialLaparoscopic/Open
Bakkum Gamez et al. [35]20131369Retrospective studyLaparoscopic/Robotic/Open/Vaginal
Ball et al. [36]2011289Retrospective Cohort StudyLaparoscopic/Open
Barber et al. [37]20169948Retrospective Cohort StudyMinimally Invasive/Open
Barnes et al. [38]2017210Retrospective Cohort studyLaparoscopic
Barnett et al. [39]2011376Retrospective Cohort StudyLaparoscopic/Open
Barnett et al. [40]20100Decision Model Analysis Laparoscopic/Robotic/Open
Barraez et al. [41]2014446Retrospective StudyRobotic
Barwijuk et al. [42]200525Retrospective StudyLaparoscopic/Open
Beck et al. [45]20183712Retrospective Cohort StudyLaparoscopic/Open
Bell et al. [43]2008110Retrospective StudyLaparoscopic/Robotic/Open
Bennich et al. [44]2016227Retrospective StudyLaparoscopic
Bergstrom et al. [46]20181621Retrospective Cohort Study Laparoscopic/Robotic/Vaginal
Bernardini et al. [47]201286Retrospective Cohort StudyRobotic/Open
Berretta et al. [48]201581Retrospective Cohort StudyLaparoscopic/Open/Vaginal
Bige et al. [49]2015140Prospective Non-Randomized Control Study Laparoscopic/Open
Bishop et al. [50]20181477Randomized Controlled TrialLaparoscopic/Open
Bogani et al. [51]2014125Retrospective StudyLaparoscopic/Open
Bogani et al. [52]2016638Retrospective Cohort StudyRobotic/Open
Boggess et al. [53]2008322Retrospective Cohort Study Laparoscopic/Robotic/Open
Boosz [215]2014267Retrospective StudyLaparoscopic/Open
Bourgin et al. [54]2017344Retrospective StudyLaparoscopic/Robotic/Open/Vaginal
Bouwman et al. [55]2015514Retrospective StudyLaparoscopic/Open
Casarin et al. [196]202035,224Retrospective StudyLaparoscopic/Robotic/Open
Casarin et al. [197]201812,283Retrospective Cohort Study Laparoscopic/Robotic/Open
Chan [198]20151087Retrospective StudyLaparoscopic/Robotic/Open
Chiou et al. [199]2015377Retrospective StudyRobotic
Cho et al. [201]2007288Retrospective StudyLaparoscopic (LAVH)/Laparoscopic (TLH)/Open
Chu et al. [202]2016151Retrospective Cohort StudyLaparoscopic/Open
Chung et al. [200]201915Retrospective StudyRobotic
Coronado et al. [203]2012347Retrospective StudyLaparoscopic/Robotic/Open
Corrado et al. [205]201650Retrospective StudyLaparoscopic
Corrado et al. [136]2015526Retrospective StudyLaparoscopic/Open
Corrado et al. [207]2018655Retrospective StudyLaparoscopic/Robotic
Corrado et al. [204]201845Prospective Cohort StudyRobotic
Corrado et al. [216]2016125Prospective Cohort StudyRobotic
Corrado et al. [206]201670Retrospective StudyRobotic
Cybulska et al. [208]2018760Retrospective StudyLaparoscopic/Robotic
Dai et al. [209]2020519Retrospective StudyLaparoscopic/Open
DeNardis et al. [210]2008162Retrospective StudyRobotic/Open
Deura et al. [211]2019120Retrospective StudyLaparoscopic/Open
Dietrich et al. [212]2019350Retrospective StudyMinimally Invasive/Open
Dowdy et al. [213]20121369 (of 1415 patients identified)Retrospective StudyMinimally Invasive/Open
Eltabbakh [62]200075Retrospective StudyLaparoscopic
Eltabbakh [63]2002186Retrospective StudyLaparoscopic/Open
Fader et al. [68]201632,560Retrospective StudyLaparoscopic/Open
Fader et al. [67]2012383Retrospective Cohort StudyLaparoscopic/Robotic/Open
Fagotti et al. [69]2012100Retrospective StudyLaparoscopic
Fagotti et al. [70]201357Retrospective StudyLaparoscopic
Fagotti et al. [71]2012150Retrospective StudyLaparoscopic/Robotic
Fanning et al. [72]2010235Retrospective StudyLaparoscopic
Farthing et al. [73]2012191Retrospective StudyLaparoscopic
Fleming et al. [74]201266Retrospective Cohort StudyLaparoscopic/Robotic/Open
Fleming et al. [75]2011181Retrospective Cohort StudyLaparoscopic/Robotic/Open
Fram et al. [13]200261Randomized Controlled TrialLaparoscopic (LAVH)/Open
Freeman et al. [94]20161433Retrospective StudyLaparoscopic/Robotic
Frey et al. [95]2015122Retrospective StudyLaparoscopic/Robotic
Frey et al. [58]2011129Retrospective Cohort StudyLaparoscopic/Robotic/Open
Frigerio et al. [96]2006110Retrospective StudyLaparoscopic (LAVH)/Open
Gambacorti-Passerini et al. [97]201983Prospective Observational StudyLaparoscopic
Gehrig et al. [76]200879Retrospective Cohort StudyLaparoscopic/Robotic
Gemignani et al. [77]1999320Retrospective StudyLaparoscopic (LAVH)/Open
Ghazali et al. [78]201940Retrospective Cohort StudyLaparoscopic/Open
Ghezzi et al. [79]2006101Prospective Cohort StudyLaparoscopic
Ghezzi et al. [80]200672Randomized Controlled TrialLaparoscopic (LAVH/TLH)
Ghezzi et al. [81]2009103Retrospective StudyLaparoscopic (Microlaparoscopy/Conventional Laparoscopy)
Ghezzi et al. [82]2010117Prospective Cohort StudyLaparoscopic/Open
Giannini et al. [98]2020100Retrospective StudyLaparoscopic/Open
Giannini et al. [83]2021147Retrospective StudyRobotic (DaVinci robot Si/XI)
Gildea et al. [99]201646,859Retrospective StudyLaparoscopic/Open
Gil-Moreno et al. [84]2006370Retrospective Cohort StudyLaparoscopic/Open
Giray et al. [181]2019121Retrospective StudyLaparoscopic/Open
Göçmen et al. [85]201022Prospective Cohort StudyRobotic/Open
Goel et al. [100]201197Retrospective StudyRobotic/Open
Grabosch et al. [101]20132Case seriesLaparoscopic
Graves et al. [102]2012760Randomized Controlled TrialLaparoscopic/Open
Gueli Alletti et al. [86]201689Retrospective Cohort StudyLaparoscopic/Robotic
Gunderson et al. [60]20142596Randomized Controlled TrialLaparoscopic/Open
Helm et al. [88]2011168Retrospective StudyLaparoscopic/Open
Herling et al. [89]2016360Retrospective Cohort StudyRobotic/Open
Hinshaw et al. [90]2016136Retrospective Cohort StudyRobotic/Open
Holloway et al. [91]2009100Retrospective StudyRobotic
Holtz et al. [92]201033Retrospective StudyLaparoscopic/Robotic
Holub et al. [93]2003108Prospective Cohort StudyLaparoscopic
Kalogiannidis et al. [135]2007169Prospective Cohort StudyLaparoscopic (LAVH)/Open
Kroft et al. [137]201512,104Retrospective Cohort StudyLaparoscopic/Open
Kuoppala et al. [138]200480Retrospective StudyLaparoscopic/Open
Lau et al. [56]2012303Retrospective Cohort StudyRobotic/Open
lavoue et al. [57]2014163Retrospective Cohort StudyRobotic/Open
Lee et al. [105]2014105Prospective Cohort StudyLaparoscopic
Lee et al. [106]2016287Prospective Cohort StudyLaparoscopic
Lee et al. [66]200835Retrospective StudyLaparoscopic
Lee et al. [65]201817,692Retrospective StudyLaparoscopic
Lee et al. [108]20169020Retrospective StudyLaparoscopic/Robotic
Lee et al. [109]2013110Randomized Controlled TrialLaparoscopic with/without manipulator
Lee et al. [107]20143Prospective StudyNOTES surgery
Lee et al. [104]20106Retrospective StudyRobotic
Leiserowtz et al. [110]200912,743Retrospective Cohort StudyLaparoscopic (LAVH)/Open
Leitao et al. [111]2013475Prospective Cohort StudyLaparoscopic/Robotic
Leitao et al. [112]2012752Prospective StudyLaparoscopic/Robotic/Open
Leitao et al. [113]2016426Retrospective StudyLaparoscopic/Robotic/Open/Vaginal
Li et al. [114]201186Retrospective StudyLaparoscopic/Open
Liang et al. [115]2013395Retrospective StudyRobotic
Liauw et al. [117]200330Retrospective StudyLaparoscopic
Lim et al. [119]200040Retrospective StudyLaparoscopic (LAVH)/Open
Lim et al. [120]200846Retrospective StudyLaparoscopic with/without manipulator
Limbachiya et al. [121]202088Retrospective StudyLaparoscopic
Lindfors et al. [122]2018278Retrospective StudyRobotic/Open
Lindfors et al. [123]2020217Retrospective StudyRobotic/Open
Liu et al. [124]2017211Retrospective StudyLaparoscopic/Open
Loaec et al. [125]201820Retrospective StudyRobotic
Lowe et al. [126]2010395Retrospective StudyRobotic
Lowe et al. [127]2009405Retrospective StudyRobotic
Lu et al. [128]2013272Randomized Controlled TrialLaparoscopic/Open
Lu et al. [129]2012238Retrospective StudyLaparoscopic/Open
Lunde et al. [130]2020207Nested Case Control StudyRobotic
Lundin et al. [131]202049Randomized Controlled TrialRobotic/Open
Lundin et al. [132]201950Randomized Controlled TrialRobotic/Open
Machida et al. [134]2018613Retrospective StudyLaparoscopic/Open
Machida et al. [133]2016333Case Control StudyLaparoscopic with cytology before and after manipulator
Mäenpää et al. [9]201699Prospective Cohort StudyLaparoscopic/Robotic
Malzoni et al. [170]2009159Randomized Controlled TrialLaparoscopic/Open
Peiretti et al. [219]200980Prospective StudyRobotic
Piovano et al. [140]2014271Prospective studySurgery/Radiotherapy
Praiss et al. [141]201917,935Retrospective StudyMinimally Invasive
Rabischong et al. [61]2011207Retrospective StudyLaparoscopic
Rajadurai et al. [139]201890Retrospective StudyLaparoscopic/Robotic
Raventos-Tato [142]2019138Retrospective StudyLaparoscopic/Robotic/Open
Roberts et al. [143]201195Retrospective StudyLaparoscopic (LAVH)/Laparoscopic (TLH)/Open
Rocha-Guevara et al. [144]201517,935Retrospective StudyMinimally Invasive
Safdieh et al. [145]201743,985Retrospective StudyRobotic/Open
Salehi et al. [146]2018120Randomized Controlled TrialLaparoscopic/Robotic
Sandadi et al. [147]2012573Retrospective StudyLaparoscopic/Robotic
Santi et al. [148]2010240Retrospective StudyLaparoscopic/Open
Scalici et al. [149]20152076Retrospective StudyLaparoscopic/Robotic
Scribner et al. [150]199936Retrospective StudyLaparoscopic/Open
Scribner et al. [151]2001125Retrospective StudyLaparoscopic/Open
Seamon [59]200979Retrospective studyRobotic
Seamon et al. [152]2009181Prospective/ retrospective StudyLaparoscopic/Robotic
Seracchioli [153]2005113Retrospective StudyLaparoscopic/Open
Seror [154]2014146Retrospective StudyLaparoscopic/Robotic
Siesto et al. [155]2010108Retrospective StudyLaparoscopic/Open
Simpson et al. [156]20204640Retrospective StudyLaparoscopic/Laparoscopic (LAVH)/Robotic/Open
Singh et al. [157]20179145Retrospective StudyLaparoscopic
Slaughter et al. [158]2014380Retrospective StudyLaparoscopic/Robotic
Sofer et al. [159]2020138Retrospective StudyRobotic/Open
Soliman et al. [160]201125Retrospective StudyLaparoscopic
Somashekar et al. [166]201450Randomized Controlled TrialRobotic/Open
Song et al. [161]2020135Retrospective StudyRobotic/Open
Sonoda et al. [162]2001377Retrospective StudyLaparoscopic (LAVH)/Open
Spencer et al. [163]2012133Retrospective StudyLaparoscopic
Spirtos et al. [164]199630Retrospective StudyLaparoscopic/Open
Subramania et al. [165]201173Retrospective StudyRobotic
Tanaka et al. [167]2020913Retrospective StudyLaparoscopic/Open
Tang et al. [168]2012239Retrospective Cohort studyRobotic/Open
Taşkın et al. [169]2012153Retrospective StudyLaparoscopic/Robotic/Open/Vaginal
Tinelli [171]201475Retrospective StudyLaparoscopic/Open
Tinelli et al. [217]2011226Retrospective StudyLaparoscopic/Open
Togami et al. [172]2020155Retrospective StudyLaparoscopic/Open
Tollund et al. [173]200686Retrospective StudyLaparoscopic (LAVH)/Laparoscopic (TLH)/Open
Tozzi et al. [175]2005122Randomized Controlled TrialLaparoscopic/Open
Turner et al. [87]2015335Retrospective StudyLaparoscopic/Robotic
Turunen et al. [214]2013227Retrospective StudyLaparoscopic/Robotic
Uccella et al. [176]20161266Retrospective StudyLaparoscopic/Open
Uccella et al. [177]20161606Retrospective StudyLaparoscopic/Open
Ulm et al. [178]2016325Retrospective StudyRobotic/Open
Vardar et al. [180]2019801Retrospective StudyLaparoscopic/Open
Venkat et al. [182]201254Retrospective StudyRobotic/Open
Walker et al. [183]20122181Randomized Controlled TrialLaparoscopic/Open
Wong et al. [184]200564Retrospective StudyLaparoscopic/Open
Wright et al. [186]20128018Retrospective StudyLaparoscopic/Open
Wright et al. [185]20166304Retrospective StudyLaparoscopic/Robotic/Open
Xu et al. [187]202081Prospective Observational StudyLaparoscopic/Open
Yin et al. [188]201532Retrospective StudyLaparoscopic
Yu et al. [189]20132247Retrospective StudyLaparoscopic/Robotic/Open
Zakhari et al. [190]201510,347Retrospective StudyLaparoscopic/Robotic
Zapico et al. [191]200590Retrospective StudyLaparoscopic/Open
Zhang et al. [192]2014458Retrospective StudyMinimally Invasive/Open
Zorlu et al. [193]200552Randomized Controlled TrialLaparoscopic/Open
Zullo et al. [194]200584Prospective long-term extension studyLaparoscopic/Open
Table 2. League table showing pairwise comparisons among the three surgical techniques (LRS: laparoscopic surgery, OS: open surgery, RS: robotic surgery) for the 14 outcomes from the Bayesian network meta-analysis. Rows represent the references, and columns represent the comparators. 95% credible intervals are included in parentheses. The clinically significant differences are shown in bold.
Table 2. League table showing pairwise comparisons among the three surgical techniques (LRS: laparoscopic surgery, OS: open surgery, RS: robotic surgery) for the 14 outcomes from the Bayesian network meta-analysis. Rows represent the references, and columns represent the comparators. 95% credible intervals are included in parentheses. The clinically significant differences are shown in bold.
Outcome OSLRSRS
Blood LossOS0 (0, 0)−226.90
(−298.40, −155.90)		−257.20
(−351.20, −163.80)
LRS226.90
(155.90, 298.40)		0 (0, 0)−30.33
(−122.20, 61.62)
RS257.20
(163.80, 351.20)		30.33
(−61.62, 122.2)		0 (0, 0)
Duration of OperationOS0 (0, 0)18.95
(7.68, 30.20)		29.00
(13.66, 44.23)
LRS−18.95
(−30.20, −7.68)		0 (0, 0)10.05
(−5.60, 25.48)
RS−29.00
(−44.22, −13.66)		−10.05
(−25.48, 5.60)		0 (0, 0)
Length of Stay in HospitalOS0 (0, 0)−3.54
(−4.22, −2.87)		−3.79
(−4.79, −2.79)
LRS3.54
(2.87, 4.22)		0 (0, 0)−0.25
(−1.26, 0.77)
RS3.79
(2.79, 4.79)		0.25
(−0.77, 1.26)		0 (0, 0)
Total Lymph NodesOS0 (0, 0)0.40
(−1.18, 2.01)		−0.06
(−2.72, 2.69)
LRS−0.40
(−2.01, 1.18)		0 (0, 0)−0.46
(−2.91, 2.09)
RS0.06
(−2.69, 2.72)		0.46
(−2.09, 2.91)		0 (0, 0)
Blood TransfusionOS1 (1, 1)0.30
(0.19, 0.48)		0.26
(0.12, 0.53)
LRS3.32
(2.09, 5.38)		1 (1, 1)0.85
(0.4, 1.79)
RS3.90
(1.89, 8.31)		1.17
(0.56, 2.50)		1 (1, 1)
FeverOS1 (1, 1)0.57
(0.30, 0.98)		0.42
(0.07, 2.21)
LRS1.75
(1.02, 3.29)		1 (1, 1)0.74
(0.11, 4.51)
RS2.37
(0.45, 14.38)		1.35
(0.22, 8.73)		1 (1, 1)
InfectionOS1 (1, 1)0.50
(0.28, 0.93)		0.84
(0.35, 2.01)
LRS1.99
(1.07, 3.60)		1 (1, 1)1.66
(0.69, 3.99)
RS1.20
(0.50, 2.84)		0.60
(0.25, 1.46)		1 (1, 1)
IleusOS1 (1, 1)0.46
(0.29, 0.68)		0.18
(0.08, 0.41)
LRS2.16
(1.47, 3.40)		1 (1, 1)0.40
(0.17, 0.87)
RS5.44
(2.43, 12.93)		2.50
(1.14, 5.74)		1 (1, 1)
VTEOS1 (1, 1)0.57
(0.36, 1.10)		0.80
(0.33, 1.86)
LRS1.75
(0.91, 2.79)		1 (1, 1)1.39
(0.55, 2.91)
RS1.26
(0.54, 3.01)		0.72
(0.34, 1.83)		1 (1, 1)
Disease-free SurvivalOS1 (1, 1)1.35
(0.80, 2.32)		3.29
(1.46, 8.36)
LRS0.74
(0.43, 1.26)		1 (1, 1)2.45
(1.04, 6.34)
RS0.30
(0.12, 0.69)		0.41
(0.16, 0.97)		1 (1, 1)
RecurrenceOS1 (1, 1)0.64
(0.47, 0.84)		0.64
(0.35, 1.19)
LRS1.57
(1.20, 2.15)		1 (1, 1)1.02
(0.55, 1.95)
RS1.55
(0.84, 2.86)		0.98
(0.51, 1.81)		1 (1, 1)
Total ComplicationsOS1 (1, 1)0.38
(0.29, 0.51)		0.34
(0.22, 0.51)
LRS2.61
(1.97, 3.45)		1 (1, 1)0.88
(0.58, 1.31)
RS2.97
(1.98, 4.55)		1.14
(0.76, 1.73)		1 (1, 1)
Total Intra-operative ComplicationsOS1 (1, 1)1.04
(0.75, 1.49)		0.39
(0.18, 0.78)
LRS0.96
(0.67, 1.33)		1 (1, 1)0.38
(0.17, 0.75)
RS2.55
(1.28, 5.47)		2.66
(1.34, 5.79)		1 (1, 1)
Total Post-operative ComplicationsOS1 (1, 1)0.48
(0.34, 0.70)		0.46
(0.27, 0.78)
LRS2.07
(1.43, 2.98)		1 (1, 1)0.95
(0.54, 1.63)
RS2.19
(1.29, 3.71)		1.05
(0.61, 1.84)		1 (1, 1)
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Natarajan, P.; Delanerolle, G.; Dobson, L.; Xu, C.; Zeng, Y.; Yu, X.; Marston, K.; Phan, T.; Choi, F.; Barzilova, V.; et al. Surgical Treatment for Endometrial Cancer, Hysterectomy Performed via Minimally Invasive Routes Compared with Open Surgery: A Systematic Review and Network Meta-Analysis. Cancers 2024, 16, 1860. https://doi.org/10.3390/cancers16101860

AMA Style

Natarajan P, Delanerolle G, Dobson L, Xu C, Zeng Y, Yu X, Marston K, Phan T, Choi F, Barzilova V, et al. Surgical Treatment for Endometrial Cancer, Hysterectomy Performed via Minimally Invasive Routes Compared with Open Surgery: A Systematic Review and Network Meta-Analysis. Cancers. 2024; 16(10):1860. https://doi.org/10.3390/cancers16101860

Chicago/Turabian Style

Natarajan, Purushothaman, Gayathri Delanerolle, Lucy Dobson, Cong Xu, Yutian Zeng, Xuan Yu, Kathleen Marston, Thuan Phan, Fiona Choi, Vanya Barzilova, and et al. 2024. "Surgical Treatment for Endometrial Cancer, Hysterectomy Performed via Minimally Invasive Routes Compared with Open Surgery: A Systematic Review and Network Meta-Analysis" Cancers 16, no. 10: 1860. https://doi.org/10.3390/cancers16101860

APA Style

Natarajan, P., Delanerolle, G., Dobson, L., Xu, C., Zeng, Y., Yu, X., Marston, K., Phan, T., Choi, F., Barzilova, V., Powell, S. G., Wyatt, J., Taylor, S., Shi, J. Q., & Hapangama, D. K. (2024). Surgical Treatment for Endometrial Cancer, Hysterectomy Performed via Minimally Invasive Routes Compared with Open Surgery: A Systematic Review and Network Meta-Analysis. Cancers, 16(10), 1860. https://doi.org/10.3390/cancers16101860

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