Abstract
Background:
Rectal cancer poses a significant global health burden. There is a lack of concrete evidence concerning the benefits of robotic-assisted surgery (RAS) for rectal cancer surgery as compared to laparoscopic and open techniques. To address this gap, we conducted a meta-analysis to assess the intraoperative, postoperative, and safety outcomes of robotic surgery in this context.
Research methodology:
A search of MEDLINE, Scopus and the Cochrane Library. Randomized and non-randomized studies up to February 2, 2024 comparing robotic surgery versus laparoscopic or open surgery for rectal cancer. The outcomes of interest were operative time, blood loss, harvested lymph nodes, conversion rate, postoperative hospital stay, survival to hospital discharge, urinary retention rate, and anastomotic leakage rate. A random-effects meta-analysis was performed to pool means and dichotomous data to derive weighted mean differences and odds ratios, respectively.
Results:
A total of 56 studies were shortlisted after the study selection process with a total of 25 458 rectal cancer patients. From the intraoperative outcomes, RAS was significantly associated with an increased operative time (WMD: 41.04, P<0.00001), decreased blood loss (WMD: −24.56, P<0.00001), decreased conversion rates (OR: 0.39, P<0.00001), lesser stay at the hospital (WMD: −1.93, P<0.00001), and no difference was found in lymph nodes harvested. Similarly, RAS group had a significantly greater survival to hospital discharge (OR: 1.90, P=0.04), decreased urinary retention rate (OR: 0.59, P=0.002), and no difference was seen in anastomotic leakage rate.
Conclusion:
RAS demonstrates favorable outcomes for rectal cancer patients, contributing to global prevention and control efforts, health promotion, and addressing non-communicable disease risk factors. Further research and public awareness are needed to optimize RAS utilization in this context.
Keywords: health promotion, non-communicable diseases, rectal cancer, risk factors, robotic-assisted surgery
Introduction
Highlights
Our study is a systematic analysis of recent studies, and comprehensive evaluation concluded that robotic-assisted surgery (RAS) demonstrates favorable outcomes for rectal cancer patients, contributing to global prevention and control efforts, health promotion, and addressing non-communicable disease risk factors.
This is the first systematic evaluation to validate the safety and feasibility of (RAS) and its application.
RAS is defined as robotic-assisted surgery.
Colorectal cancer treatment primarily relies on surgical resection as it offers the most effective means for achieving curative resection, accurate staging, favorable prognosis, and other therapeutic considerations1,2. The primary goal of cancer surgery revolves around improving survival rates and quality of life for patients while minimizing potential adverse effects3. To enhance outcomes related to functional, oncological, surgical, patient-reported, and financial aspects of colorectal cancer treatment, it is crucial to advance surgical procedures4.
Over the past two decades, there has been a notable inclination toward the adoption of minimally invasive procedures5. Despite initial skepticism, this approach has gained significant momentum since its initial description in 1991 and has now become the established standard of care in Western countries for both benign and malignant colorectal diseases5. Numerous randomized trials have unequivocally demonstrated the superiority of laparoscopic surgery over open surgery for colon cancer treatment6,7. This preference stems from its associated benefits, such as reduced blood loss, faster recovery of bowel motility, and shorter hospital stays, all without compromising oncologic outcomes. As a result, laparoscopic surgery has become the established standard method for colon cancer treatment. Nevertheless, the laparoscopic approach is not without its inherent technical limitations such as a restricted range of motion for elongated instruments within the confined pelvic cavity, two-dimensional visual perception, diminished tactile sensitivity, and poor ergonomics.
To surmount these challenges, the use of robotic-assisted surgery (RAS) was undertaken with the aim of addressing these limitations. The da Vinci system (Intuitive Surgical, Sunnyvale, CA, USA) is the first system approved by the FDA in 20008. Since the first robotic colectomy was performed in 2001, the use of robotics has been increasing ever since for both benign and malignant conditions. Because of the improved dexterity and the high-dimensional three-dimensional view, precise dissection and excellent exposure are observed with the use of robotic surgery for rectal cancers9.
The field of colorectal surgery has witnessed a remarkable transformation in the surgical management of rectal carcinomas with the advent of robotic surgery, leveraging cutting-edge technologies. This technique has gained significant popularity due to its potential advantages. However, despite the growing utilization of robotic surgery, the precise role it plays in colorectal cancer surgery remains largely uncertain. The question of whether robotic surgery offers substantial clinical benefits over laparoscopic surgery for the treatment of colorectal cancer remains unanswered. A recent meta-analysis comparing robotic and laparoscopic approaches for rectal cancers found no significant difference in overall survival and crucial postoperative complications between both groups10. Hence, we performed this systematic review and meta-analysis to compare RAS with conventional laparoscopic and open approaches to rectal cancers.
Methods
This study was registered on the PROSPERO website (CRD42023430839). This systematic review and meta-analysis were performed in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA)11, Cochrane Collaboration guidelines12, and was in compliance with A MeaSurement Tool to Assess systematic Reviews (AMSTAR-2) Checklist13.
Literature search and study selection
Databases such as MEDLINE, Scopus, and the Cochrane Library were searched from inception till 2nd February 2024. The following keywords were used in the search string: “rectal neoplasms”, “rectal cancers”, “robotic assisted”, “laparoscopic”, and “surgery”. The detailed search string is shown in Supplementary Material Table S1 (Supplemental Digital Content 1, http://links.lww.com/JS9/C308). Additionally, conference proceedings, www.clinicaltrials.gov, and bibliometrics of published articles were browsed to ensure no articles were missed.
Articles from the literature search were exported to Endnote Reference Library (Version X7.5; Clarivate Analytics, Philadelphia, Pennsylvania) software, where the duplicates were identified and removed. The remaining articles were then thoroughly reviewed by independent reviewers, ensuring that the selected articles met the defined eligibility criteria. The following inclusion criteria were used to shortlist studies: (1) adult patients with diagnosed rectal cancer, (2) robotic-assisted rectal cancer surgery being done, (3) compared with conventional laparoscopic or open surgery, and (4) randomized controlled trials and non-randomized studies. Studies published in the English language were shortlisted, and studies with small sample sizes (n<10) were excluded.
Data extraction and quality assessment
Data extraction was extracted and verified by two reviewers. Any discrepancies were resolved through discussion and consensus. Further random ball sampling was done to include all the relevant studies. Data extracted from each study included study design, study population, sample size, number of patients in each group, general patient characteristics (age and gender), pathological characteristics, and primary and secondary endpoints. Following were the outcomes of interest: survival to hospital discharge, lymph nodes harvested, operative time, postoperative hospital stay, blood loss, conversion rate, urinary retention rate, and anastomotic leakage rate.
The quality assessment of RCTs was done using the risk of bias-2 tool (RoB-2) of Cochrane Collaboration14. ROBINS-I was utilized for the risk of bias evaluation of non-randomized studies15.
Statistical analysis
Review Manager (version 5.4.1; The Nordic Cochrane Centre, The Cochrane Collaboration, 2020, Copenhagen) was used for all relevant meta-analyses of this study. A random-effects model was used due to the large number of studies, variability in study populations, differences in study designs and methods, and unknown sources of heterogeneity. This meta-analysis was performed to derive weighted mean differences (WMDs) and odds ratios (ORs) for continuous and dichotomous data, respectively. Publication bias was assessed by checking asymmetry in the funnel plots for outcomes with greater than 10 studies. A cumulative meta-analysis for the primary outcome of survival to hospital discharge was carried out using Open Meta-Analyst [Computer Program]. Egger’s regression test was performed to confirm the risk of publication bias. Subgroup analysis was performed based on a comparator (either laparoscopic or open) if the outcome had two or more studies of a specific subgroup. A P-value <0.05 was considered statistically significant for all outcomes. Heterogeneity was assessed with Higgin’s I 2 test. A value of I 2=25–50% was considered mild, 50–75% as moderate, and >75% as significant heterogeneity. Sensitivity analysis was performed by excluding the study comparing robotic approach with open approach, for outcomes with only one such study.
Results
A total of 2167 articles were identified from the literature search (Fig. 1). After deduplication and removing reviews, abstracts, editorials, and case reports, 126 studies were given a full-text evaluation, and 56 were finally included in the meta-analysis16–70. The risk of bias was low for 44 studies and the rest were moderate (Supplementary Fig. S1, Supplemental Digital Content 1, http://links.lww.com/JS9/C308 and Supplementary Fig. S2, Supplemental Digital Content 1, http://links.lww.com/JS9/C308).
Figure 1.
PRISMA flowchart.
Patient characteristics
A total of 25 458 rectal cancer patients were present in the 56 included studies (11 218 in the robotic group, 13 848 in the laparoscopic, and 392 in the open). The mean age of patients in the robotic and control groups was 61.5±16.7 and 63.6±12.3 years, respectively. The male sex percentage was 65.8% of the robotic arm compared to 62.3% in the control (Table 1). American Society of Anaesthesiologists (ASA) Physical Status Classification ≥III grade was present in 14.4% of patients in the RG group and 20.1% in the control group. Neoadjuvant chemotherapy was increasingly used more in the robotic group as compared to the control (41.2% vs. 32.8%). The proportion of rectal cancer being lower was 40.2% in the robotic group and 39% in the control group. Detailed characteristics are present in Table 2.
Table 1.
Patient characteristics of the included studies.
Robotic-assisted group | Laparoscopic group | Open group | ||||||||
---|---|---|---|---|---|---|---|---|---|---|
Study | Study design | No. | Age | Sex, male | No. | Age | Sex, male | No. | Age | Sex, male |
Ahmed et al., 201716 | PCD | 99 | 69±2 | 71.7% | 85 | 68±2 | 68.2% | |||
Ali et al., 202265 | RS | 64 | 61.7±12 | 62.5% | 91 | 62.7±11.2 | 64% | |||
Aselmann et al., 201817 | R-PCD | 44 | 61.1±11.5 | 59.1% | 41 | 65.1±12.0 | 58.5% | |||
Asklid et al., 201818 | RCS | 72 | 65.4±10.4 | 59.7% | 47 | 70.1±12.0 | 44.7% | |||
Baek et al., 201019 | PCD | 41 | 65.6±11.3 | 61.0% | 41 | 64.4±13.3 | 61.0% | |||
Baek et al., 201220 | PCD | 154 | 59.1±12.2 | 68.2% | 150 | 62.3±10.9 | 72.7% | |||
Baek et al., 201321 | RS | 47 | 50.8±12.9 | 66.0% | 37 | 61.8±12.8 | 75.7% | |||
Baik et al., 200822 | RCT | 18 | 57.3±6.3 | 77.8% | 18 | 62.0±9.0 | 77.8% | |||
Barnajian et al., 201423 | RS | 20 | 62.5±11 | 60.0% | 20 | 61.3±13 | 60.0% | |||
Bedirli et al., 201524 | RS | 35 | 64.7±8.5 | 68.6% | 28 | 60.4±7.1 | 67.9% | |||
Bedrikovetski et al., 202025 | RS | 117 | 61±9.3 | 63.2% | 1269 | 62.5±13.7 | 57.9% | |||
Bianchi et al., 201026 | PCD | 25 | 63.5±9.3 | 72.0% | 25 | 62.5±13.7 | 68.0% | |||
Bilgin et al., 202027 | R-PCD | 72 | 59.0±11.1 | 58.3% | 44 | 57.2±13.3 | 75.0% | |||
Chen et al., 201728 | RS | 4744 | NS | NS | 5578 | NS | NS | |||
Cho et al., 201529 | PCD | 278 | 57.4±11.6 | 65.5% | 278 | 58.3±10.4 | 66.2% | |||
Corbellini et al., 201670 | RCT | 65 | 60.3±29.7 | 53.8% | 40 | 60±33.5 | 57.5% | 55 | 60.6±30.5 | 65.5% |
Corrigan et al., 201830 | RCT | 237 | NS | 67.9% | 234 | NS | 67.9% | |||
Crolla et al., 201831 | RS | 168 | 67.0±9.64 | 67.3% | 184 | 68.1±10.7 | 56.0% | |||
D’Annibale et al., 201332 | RS | 50 | 66.0±12.1 | 60.0% | 50 | 65.7±11.6 | 60.0% | |||
de Jesus et al., 201633 | PCD | 59 | 56.8±14.7 | 61.0% | 41 | 55.5±16.7 | 58.0% | |||
de’Angelis et al., 202034 | PCD | 50 | 64.4±14.7 | 66.0% | 81 | 55.5±16.7 | 60.5% | |||
Esen et al., 201835 | PCD | 100 | 59±11 | 60.0% | 78 | 56±13 | 65.0% | |||
Feng et al., 202162 | RS | 137 | 58.3±11.2 | 54.7% | 137 | 59.5±11.2 | 59.1% | |||
Feng et al., 202266 | RCT | 586 | 585 | |||||||
Feng et al., 202268 | RCT | 174 | 58.2 (9.6) | 62.1% | 173 | 59.5 (10.9) | 65.3% | |||
Fernandez et al., 201357 | RS | 13 | 67.9±2.1 | 100% | 59 | 64.9±1.2 | 97% | |||
Feroci et al., 201636 | RS | 53 | 64.5±12.1 | 50.9% | 58 | 61.3±13.6 | 72.4% | |||
Garfinkle et al., 201937 | RS | 154 | 61.9±13.5 | 68.8% | 213 | 63.8±13.3 | 59.6% | |||
Ishihara et al. 201838 | PCD | 130 | 61.3 | 58.0% | 234 | 64.1 | 65.0% | |||
Jayne et al., 201739 | RCT | 237 | 64.4±11.0 | 67.9% | 234 | 65.5±11.9 | 67.9% | |||
Kang et al., 201340 | PCD | 165 | 61.2±11.4 | 63.0% | 165 | 60.4±11.8 | 58.8% | |||
Kethman et al. 202041 | Cohort | 192 | 61.7 | 69.0% | 206 | 62 | 63.4% | |||
Kim et al., 201242 | PCD | 30 | 54.13±8.52 | 60.0% | 39 | 56.85±11.14 | 51.3% | |||
Kim et al. 201643 | PCD | 33 | 57.0±9.6 | 69.7% | 66 | 58.2±9.8 | 69.7% | |||
Kim et al., 201844 | RCT | 66 | 60.4±9.7 | 77.3% | 73 | 59.7±11.7 | 71.2% | |||
Lawet al., 201771 | PCD | 220 | 63.5±9.3 | 67.3% | 171 | 63.3±12.2 | 56.7% | |||
Lim et al., 201646 | RS | 74 | 65.1±12.4 | 67.6% | 64 | 65.8±11.1 | 71.9% | |||
Liu et al., 201945 | RS | 80 | 62±9.64 | 66.3% | 116 | 59.57±10.3 | 62.1% | |||
Megevand et al., 201960 | PCD | 35 | 70 | 65.7% | 35 | 66 | 51.4% | |||
Ose et al., 202164 | RS | 713 | 67.3±10.1 | 66.3% | 1163 | 67.6±10.3 | 61.4% | 205 | 67±10.2 | 64.4% |
Park et al., 201147 | PCD | 52 | 57.3±12.3 | 53.8% | 123 | 65.1±10.3 | 56.9% | |||
Park et al., 201247 | RS | 40 | 57.3±12.1 | 70% | 40 | 63.3±10.6 | 62.5% | |||
Park et al., 202167 | RS | 118 | 60.0±10.8 | 76.3% | 118 | 60.3±11.1 | 73.7% | |||
Park et al., 202369 | RCT | 151 | 65.5±11.4 | 64.2% | 144 | 67.2±10.1 | 68.8% | |||
Patriti et al., 200948 | PCD | 29 | 68±10 | 57.7% | 37 | 69±10 | 33.3% | |||
Ramji et al., 201649 | RS | 26 | 62.1±9.1 | 73% | 27 | 63.7±11.2 | 70.0% | |||
Rouanet et al., 201850 | RS | 200 | 59.5±10 | 65.5% | 200 | 62±8.5 | 68.0% | |||
Shiomi et al., 201652 | RS | 127 | 62±9.3 | 73.2% | 109 | 654±10 | 59.6% | |||
Silva-Velazco et al., 201751 | RS | 66 | 56±13.8 | 75.8% | 118 | 59.8±9.8 | 55.9% | |||
Somashekhar et al., 201558 | PCD | 25 | 56.36 ± 8.21 | 68% | 25 | 59.56 ± 5.75 | 60% | |||
Song et al., 202161 | RS | 70 | 59.2 ± 37.8 | 65.7% | 29 | 58.7± 34.1 | 82.6% | |||
Sugoor et al., 201853 | PCD | 100 | 48.7±15.3 | 76.0% | 113 | 49.2±14.6 | 61.1% | |||
Tilney et al., 201963 | PCD | 204 | 64.4±11.4 | 77% | 133 | 66.6±12.2 | 62.4% | |||
Valverde et al., 201754 | PCD | 65 | 67±11 | 65.0% | 65 | 65±10 | 69.0% | |||
Yamaguchi et al., 201655 | RS | 203 | 64.8±10.8 | 69.0% | 239 | 65.9±10.8 | 64.4% | |||
Yang et al., 201859 | RS | 91 | 60±13.5 | 48.4% | 102 | 59.1±11.6 | 59.8% | 107 | 62.2±11.4 | 57.9% |
PCS, prospectively collected data; R-PCD, a retrospective analysis of prospectively collected data; RCT, randomized controlled trial; RS, retrospective study.
Table 2.
Baseline characteristics of the included studies.
Events/participants | ||||||
---|---|---|---|---|---|---|
Outcome | Number of studies | Robotic | Laparoscopic | Number of studies | Robotic | Open |
Sex, male | 52 | 3793/5733 (66.2%) | 4789/7662 (62.5%) | 4 | 569/894 (63.6%) | 247/392 (63%) |
American Society of Anesthesiologists (ASA) score | ||||||
1 class | 39 | 1250/4142 (30.1%) | 1636/5790 (28.2%) | 2 | 240/713 (33.7%) | 45/260 (17.3%) |
2 class | 39 | 2197/4142 (53%) | 3014/5790 (52.1%) | 2 | 424/713 (59.5%) | 141/260 (54.3%) |
3 class | 39 | 576/4142 (13.9%) | 1057/5790 (18.3%) | 2 | 109/713 (15.3%) | 72/260 (27.7%) |
4 class | 31 | 19/3392 (0.6%) | 52/5124 (1.0%) | 1 | 1/713 (0.1%) | 0/205 (0%) |
Neoadjuvant therapy | 29 | 1493/3626 (41.2%) | 1806/5472 (33%) | 2 | 163/804 (20.3%) | 90/312 (28.8%) |
Tumor location | ||||||
Upper rectum | 14 | 300/1733 (17.3%) | 607/3201 (19%) | 2 | 12/116 (10.1%) | 17/132 (12.5%) |
Middle | 15 | 963/1948 | 1565/3416 (45.8%) | 2 | 54/116 (49.1%) | 68/132 (51.5%) |
Lower | 20 | 1026/2552 (40.2%) | 1491/4032 (37%) | 2 | 32/116 (27.6%) | 28/132 (21.2%) |
Intraoperative and postoperative outcomes
Intraoperative outcomes consisted of operative time in minutes, intraoperative blood loss (ml), conversion to open surgery, and number of harvested lymph nodes. Robotic group was significantly associated with increased operative time when compared with the control group (WMD: 41.04 [28.15, 53.92], P<0.00001; I 2=98%) (Fig. 2). Upon subgroup analysis, robotic group had a greater operative time when compared with laparoscopic (WMD: 40.42 [26.70, 54.13], P<0.00001; I 2=98%) and open groups (WMD: 48.85 [7.44, 90.26], P=0.02; I 2=89%) independently. Operative time was compared between robotic and laparoscopic groups for randomized controlled trials. No significant association was seen across eight RCTs (WMD: 15.02 [−10.05, 40.08], P=0.24; I 2=97%) (Supplementary Fig. S3, Supplemental Digital Content 1, http://links.lww.com/JS9/C308). Patients in the robotic group had a significantly decreased loss of blood when compared with the control group (WMD: −24.56 [−41.44, −7.99], P<0.00001; I 2=97%) (Fig. 3). However, subgroup analysis showed no significant difference between robotic and the laparoscopic groups (WMD: −10.15 [−25.94, 5.65], P=0.21; I 2=97%) and decreased blood loss levels with robotic group when compared with open surgery (WMD: −182.17 [−304.76, −59.59], P=0.004; I 2=95%). Blood loss was also compared between robotic and laparoscopic groups for randomized controlled trials. No significant association was seen across six RCTs (WMD: 8.74 [−50.53, 68.01], P=0.77; I 2=99%) (Supplementary Fig. S4, Supplemental Digital Content 1, http://links.lww.com/JS9/C308). The robotic group was associated with decreased conversion rates to open surgery as compared to the laparoscopic approach (OR: 0.39 [0.32, 0.47], P<0.00001; I 2=0%) (Fig. 4). No significant difference was observed between the robotic and control groups comparing the number of harvested lymph nodes (WMD: −0.05 [−0.84, 0.75], P=0.91; I 2=85%) (Fig. 5). However, subgroup analysis showed robotic group to be significantly superior to open group in harvesting lymph nodes (WMD: 2.00 [1.09, 2.92], P<0.0001; I 2=0%). Postoperative hospital stay was found to be significantly lower in the robotic group as compared to the control group (WMD: −1.93 [−2.72, −1.13], P<0.00001; I 2=99%) (Fig. 6). Upon subgroup analysis, robotic approach was found to be superior to laparoscopic group (WMD: −1.78 [−2.54, −1.01], P<0.00001; I 2=99%) and open surgery group (WMD: −5.54 [−7.38, −3.70], P<0.00001; I 2=83%) as it had a lesser postoperative hospital stay.
Figure 2.
Forest plot for operative time.
Figure 3.
Forest plot for intraoperative blood loss.
Figure 4.
Forest plot for open surgery conversion rates.
Figure 5.
Forest plot for the number of harvested lymph nodes.
Figure 6.
Forest plot for postoperative hospital stay.
Safety outcomes
Survival to hospital discharge, urinary retention rate, and anastomotic leakage rate were included in the safety outcomes. The robotic group was significantly associated with increased survival at discharge from the hospital when compared with the control group (OR: 1.90 [1.03, 3.48], P=0.04; I 2=38%). For urinary retention rate, patients in the robotic group had significantly lesser urinary retention rates than the control group (OR: 0.59 [0.39, 0.82], P=0.002; I 2=23%). A sensitivity analysis was carried out removing Somashekhar et al.58 as it was the only study comparing the robotic group with open surgery (OR: 0.57 [0.39, 0.84], P=0.005; I 2=26%) (Supplementary Fig. S5, Supplemental Digital Content 1, http://links.lww.com/JS9/C308). No significant difference was observed for anastomotic leakage rate between the groups (OR: 0.91 [0.76, 1.10], P=0.34; I 2=0%). Additionally, no subgroup differences were observed for the laparoscopic and the open groups (P=0.93) (Figs 7–9).
Figure 7.
Forest plot for survival to hospital discharge.
Figure 9.
Forest plot for anastomotic leakage rate.
Figure 8.
Forest plot for urinary retention rate.
Publication bias and cumulative meta-analysis
For the assessment of publication bias, funnel plots were generated to ensure there was no asymmetry in the funnel plot. For the outcomes of operative time, blood loss, and postoperative hospital stay, asymmetry was observed in the funnel plots; thus, Egger’s regression test was performed to confirm the risk of publication bias. After Egger’s test, publication bias was confirmed for only postoperative hospital stay length (P=0.004). All funnel plots are shown in Supplementary Material Figures S6–S13 (Supplemental Digital Content 1, http://links.lww.com/JS9/C308). A umulative meta-analysis stratifying by year was performed to determine the outcome of survival to hospital discharge. This analysis showed the overall effect size to converge over time, indicating consistency of the pooled result (Supplementary Fig. S14, Supplemental Digital Content 1, http://links.lww.com/JS9/C308).
Discussion
We performed this meta-analysis by pooling all the data to date on robotic surgery and by including the most recent randomized controlled trials on this topic. In this meta-analysis, many significant findings were established. The survival rate for hospital discharge was found to be significantly higher in the robotic group. The robotic group was associated with an increased operative time, decreased postoperative hospital stay, decreased intraoperative blood loss, decreased conversion rates, and a decreased urinary retention rate.
A study found that robotic techniques in surgery offer visual advantages, including binocular vision with three-dimensional imaging, increased freedom of movement, and an ergonomic position. Robotic surgery reduces tremors and human errors, improving maneuverability. The learning curve is like laparoscopic training, and it may be easier to learn than laparoscopic surgery. Robotic surgery enables minimally invasive approaches even in challenging procedures or anatomically difficult regions, benefiting less experienced surgeons72,73.
In many observational studies and meta-analyses, robotic surgery for rectal cancers significantly reduced open conversions, postoperative complications, hospital stays, and urinary function74,75. However, the ROLARR trial conducted by Jayne et al. 39 found no significant differences in these outcomes. It overestimated the open surgery conversion rate for both the robotic and the laparoscopic group. Hence, a more robust COREAN trial40 found the conversion rate to be 1.2% in the laparoscopic group. Our meta-analysis with over 10 000 patients for this outcome found the open surgery conversion rate to be significantly lower in the robotic group. These findings are consistent with a recent meta-analysis conducted by Safiejko et al.10. Robotic surgery could provide higher surgical quality and avoid these open conversions, consistent with the technical advantages of robotic surgery. Robotic systems offer three-dimensional high-definition visualization, providing surgeons with a detailed and magnified view of the surgical field. This enhanced visibility can be particularly advantageous in rectal surgeries where precise dissection is crucial. Improved visualization may reduce the likelihood of complications, leading to a lower conversion rate39. Additionally, robotic systems offer ergonomic advantages, allowing surgeons to operate from a console in a comfortable seated position. This can lead to reduced fatigue during lengthy procedures, potentially decreasing the likelihood of conversion due to surgeon exhaustion29,40.
The decreased intraoperative blood loss seen in this meta-analysis is similar to the findings of previous RCTs(22,48). Robotic surgery was associated with decreased hospital stay in our meta-analysis. Patients undergoing surgery for rectal cancers by the robotic approach recover faster with lesser postoperative complications, leading to longer hospital stays. These findings are consistent with previous studies59,62,68. Additionally, the minimally invasive nature of robotic surgery involves smaller incisions compared to open surgery. This results in less tissue trauma, reduced pain, and quicker recovery76.
In our meta-analysis, no difference was seen in the number of harvested lymph nodes. The mean number of retrieved lymph nodes is an important criterion for judging whether the tumor will be cured. In 1990, the World Congress of Gastroenterology in Sydney recommended the removal of 12 lymph nodes77. These findings are consistent with recent RCTs conducted by Park et al.69 and Feng et al.68. A previous meta-analysis also found no significant association between the harvested lymph nodes and the robotic approach10. However, a study conducted in 2022 found increased lymph nodes harvested with the robotic approach65. These findings might be different from our pooled analysis due to the retrospective nature of the study.
According to our findings, anastomotic leaking was not significantly different between the robotic and the laparoscopic surgery groups. The 3D dimension and articulating equipment used in robotic surgery may make anastomosis easier. However, pooled analysis failed to match this hypothesis. These findings were also reported in the meta-analysis conducted by Safiejko et al.10.
Our meta-analysis found a significant association between increased survival to hospital discharge and the robotic approach. These findings are novel, as previous meta-analyses have failed to show this association10. This might be because we have performed our meta-analysis with recent large-scale studies showing lower mortality with the robotic approach63,64.
The robotic approach emerges as the most favorable option for managing rectal cancer when compared to open, laparoscopic, or transanal techniques, as it delivers the finest blend of oncological, functional, and patient recovery outcomes. The digital interface of surgical robots enables a shift in the paradigm of surgical training, facilitating shorter learning curves that are more comprehensive and, notably, reducing the morbidity and mortality associated with them. It is imperative for surgical societies to take the initiative in this transformative process and establish efficacious training programs for colorectal robotic surgery.
Our study is not without its limitations. We conducted this meta-analysis by pooling observational studies and randomized controlled trials in which patients have been matched according to different variables. Few studies have kept in place a 1:1 randomization. Neoadjuvant chemotherapy was significantly greater in the robotic arm, which may lead to edema and fibrotic changes, thus influencing the outcomes. RAS for rectal cancers, in comparison to laparoscopic and open approaches, is available at a higher cost, thus influencing the lower availability of the procedure. The studies conducted for the open approach were mostly in languages other than English; hence, they were excluded from our meta-analysis. Laparoscopic is the conventional approach to rectal cancers nowadays hence, a smaller number of studies were found comparing robotic and open surgery.
Conclusion
Robotic-assisted techniques showed numerous differences as compared to laparoscopic and open techniques, as it significantly increased the operative time. However, the robotic group showed decreased intraoperative blood loss, reduced hospital stays, significantly lower conversion of the procedure to open surgery, lower risk of urinary risk retention, and increased survival to discharge rate.
Ethical approval
My research is a meta-analysis that integrates existing data and does not involve experiments on humans or animals, so it is not applicable, and there are no ethical issues.
Consent
Not applicable.
Sources of funding
Not applicable. This is a systematic review and meta-analysis that does not apply and does not exist to patients.
Author contribution
C.Z., H.T., and H.X.: conceived the study and carried out the research; C.Z. and H.T.: prepared the first draft of the manuscript; C.Z., H.T., and J.D.: directed the manuscript to completed. All authors were involved in the revision of the draft manuscript and have agreed to the final content.
Conflicts of interest disclosure
The authors declare that they have no conflicts of interest and no financial interests related to the material of this manuscript.
Research registration unique identifying number (UIN)
CRD42023430839
Guarantor
The scientific guarantor of this publication is Chenxiong Zhang from the Department of Anorectal Surgery, Yubei Hospital of Traditional Chinese Medicine/Guangzhou University of Chinese Medicine.
Data availability statement
Data sharing is not applicable to this article as no new data were created or analyzed in this study.
Provenance and peer review
Not commissioned, externally peer-reviewed.
Supplementary Material
Footnotes
Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.
Supplemental Digital Content is available for this article. Direct URL citations are provided in the HTML and PDF versions of this article on the journal's website, www.lww.com/international-journal-of-surgery.
Published online 27 March 2024
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Chenxiong Zhang, Email: 18602340540@163.com.
Hao Tan, Email: tanhao@stu.gzucm.edu.cn.
Han Xu, Email: xuhan@stu.gzucm.edu.cn.
Jiaming Ding, Email: 20201120124@stu.gzucm.edu.cn.
References
- 1. Varela C, Kim NK. Surgical treatment of low-lying rectal cancer: updates. Ann Coloproctol 2021;37:395–424. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Piozzi GN, Kim SH. Robotic intersphincteric resection for low rectal cancer: technical controversies and a systematic review on the perioperative, oncological, and functional outcomes. Ann Coloproctol 2021;37:351. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. Oh CK, Huh JW, Lee YJ, et al. Long-term oncologic outcome of postoperative complications after colorectal cancer surgery. Ann Coloproctol 2020;36:273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. Jalloun HE, Lee IK, Kim MK, et al. Influence of the enhanced recovery after surgery protocol on postoperative inflammation and short-term postoperative surgical outcomes after colorectal cancer surgery. Ann Coloproctol 20201;36:264–272. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Shah MF, Nasir IUI, Parvaiz A. Robotic surgery for colorectal cancer. Visc Med 2019;35:247–251. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Bonjer HJ, Skullman S, Haglind E, et al. COLOR: a randomized clinical trial comparing laparoscopic and open resection for colon cancer. Dig Surg 2000;17:617–622. [DOI] [PubMed] [Google Scholar]
- 7. Nelson H Sargent DJ Wieand HS et al. Clinical Outcomes of Surgical Therapy Study Group . A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 2004;350:2050–2059. [DOI] [PubMed] [Google Scholar]
- 8. Ngu J, Tsang C, Koh D. The da Vinci Xi: a review of its capabilities, versatility, and potential role in robotic colorectal surgery. Robot Surg 2017;4:77–85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Kim HJ, Choi GS, Park JS, et al. Multidimensional analysis of the learning curve for robotic total mesorectal excision for rectal cancer: lessons from a single surgeon’s experience. Dis Colon Rectum 2014;57:1066–1074. [DOI] [PubMed] [Google Scholar]
- 10. Safiejko K, Tarkowski R, Koselak M, et al. Robotic-assisted vs. standard laparoscopic surgery for rectal cancer resection: a systematic review and meta-analysis of 19,731 patients. Cancers 2022;14:180. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Int J Surg 2021;88:105906. [DOI] [PubMed] [Google Scholar]
- 12. Higgins JPT, Thomas J, Chandler J, et al. Cochrane Handbook for Systematic Reviews of Interventions, version 6.3 (updated February 2022). Cochrane, 2022. www.training.cochrane.org/handbook
- 13. AMSTAR - Assessing the Methodological Quality of Systematic Reviews Accessed 1 July 2023. https://amstar.ca/Amstar_Checklist.php [Google Scholar]
- 14. Sterne JAC, Savović J, Page MJ, et al. RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ 2019;366:4898. [DOI] [PubMed] [Google Scholar]
- 15. Sterne JA, Hernán MA, Reeves BC, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ 2016;355:i4919. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Ahmed J, Cao H, Panteleimonitis S, et al. Robotic vs laparoscopic rectal surgery in high-risk patients. Colorectal Dis 2017;19:1092–1099. [DOI] [PubMed] [Google Scholar]
- 17. Aselmann H, Kersebaum JN, Bernsmeier A, et al. Robotic-assisted total mesorectal excision (TME) for rectal cancer results in a significantly higher quality of TME specimen compared to the laparoscopic approach-report of a single-center experience. Int J Colorectal Dis 2018;33:1575–1581. [DOI] [PubMed] [Google Scholar]
- 18. Asklid D, Gerjy R, Hjern F, et al. Robotic vs laparoscopic rectal tumour surgery: a cohort study. Colorectal Dis 2019;21:191–199. [DOI] [PubMed] [Google Scholar]
- 19. Baek JH, Pastor C, Pigazzi A. Robotic and laparoscopic total mesorectal excision for rectal cancer: a case-matched study. Surg Endosc 2011;25:521–525. [DOI] [PubMed] [Google Scholar]
- 20. Baek SJ, Kim SH, Cho JS, et al. Robotic versus conventional laparoscopic surgery for rectal cancer: a cost analysis from a single institute in Korea. World J Surg 2012;36:2722–2729. [DOI] [PubMed] [Google Scholar]
- 21. Baek SJ, Al-Asari S, Jeong DH, et al. Robotic versus laparoscopic coloanal anastomosis with or without intersphincteric resection for rectal cancer. Surg Endosc 2013;27:4157–4163. [DOI] [PubMed] [Google Scholar]
- 22. Baik SH, Ko YT, Kang CM, et al. Robotic tumor-specific mesorectal excision of rectal cancer: short-term outcome of a pilot randomized trial. Surg Endosc 2008;22:1601–1608. [DOI] [PubMed] [Google Scholar]
- 23. Barnajian M, Pettet D, Kazi E, et al. Quality of total mesorectal excision and depth of circumferential resection margin in rectal cancer: a matched comparison of the first 20 robotic cases. Colorectal Dis 2014;16:603–609. [DOI] [PubMed] [Google Scholar]
- 24. Bedirli A, Salman B, Yuksel O. Robotic versus laparoscopic resection for mid and low rectal cancers. JSLS 2016;20:e2015.00110. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Bedrikovetski S, Dudi-Venkata NN, Kroon HM, et al. Outcomes of minimally invasive versus open proctectomy for rectal cancer: a propensity-matched analysis of bi-national colorectal cancer audit data. Dis Colon Rectum 2020;63:778–787. [DOI] [PubMed] [Google Scholar]
- 26. Bianchi PP, Ceriani C, Locatelli A, et al. Robotic versus laparoscopic total mesorectal excision for rectal cancer: a comparative analysis of oncological safety and short-term outcomes. Surg Endosc 2010;24:2888–2894. [DOI] [PubMed] [Google Scholar]
- 27. Bilgin IA, Bas M, Aytac E, et al. Operative and long-term oncological outcomes in patients undergoing robotic versus laparoscopic surgery for rectal cancer. Int J Med Robot 2020;16:1–10. [DOI] [PubMed] [Google Scholar]
- 28. Chen ST, Wu MC, Hsu TC, et al. Comparison of outcome and cost among open, laparoscopic, and robotic surgical treatments for rectal cancer: a propensity score matched analysis of nationwide inpatient sample data. J Surg Oncol 2018;117:497–505. [DOI] [PubMed] [Google Scholar]
- 29. Cho MS, Baek SJ, Hur H, et al. Short and long-term outcomes of robotic versus laparoscopic total mesorectal excision for rectal cancer: a case-matched retrospective study. Medicine 2015;94:e522. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30. Corrigan N, Marshall H, Croft J, et al. Exploring and adjusting for potential learning effects in ROLARR: a randomised controlled trial comparing robotic-assisted vs. standard laparoscopic surgery for rectal cancer resection. Trials 2018;19:339. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31. Crolla RMPH, Mulder PG, van der Schelling GP. Does robotic rectal cancer surgery improve the results of experienced laparoscopic surgeons? An observational single institution study comparing 168 robotic assisted with 184 laparoscopic rectal resections. Surg Endosc 2018;32:4562–4570. [DOI] [PubMed] [Google Scholar]
- 32. D’Annibale A, Pernazza G, Monsellato I, et al. Total mesorectal excision: a comparison of oncological and functional outcomes between robotic and laparoscopic surgery for rectal cancer. Surg Endosc 2013;27:1887–1895. [DOI] [PubMed] [Google Scholar]
- 33. de Jesus JP, Valadão M, de Castro Araujo RO, et al. The circumferential resection margins status: a comparison of robotic, laparoscopic and open total mesorectal excision for mid and low rectal cancer. Eur J Surg Oncol 2016;42:808–812. [DOI] [PubMed] [Google Scholar]
- 34. de’Angelis N, Notarnicola M, Martínez-Pérez A, et al. Robotic versus laparoscopic partial mesorectal excision for cancer of the high rectum: a single-center study with propensity score matching analysis. World J Surg 2020;44:3923–3935. [DOI] [PubMed] [Google Scholar]
- 35. Esen E, Aytac E, Ağcaoğlu A, et al. Totally robotic versus totally laparoscopic surgery for rectal cancer. Surg Laparosc Endosc Percutan Tech 2018;28(4):245–249. [DOI] [PubMed] [Google Scholar]
- 36. Feroci F, Vannucchi A, Bianchi PP, et al. Total mesorectal excision for mid and low rectal cancer: laparoscopic vs robotic surgery. World J Gastroenterol 2016;22:3602–3610. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37. Garfinkle R, Abou-Khalil M, Bhatnagar S, et al. A comparison of pathologic outcomes of open, laparoscopic, and robotic resections for rectal cancer using the ACS-NSQIP proctectomy-targeted database: a propensity score analysis. J Gastrointest Surg 2019;23:348–356. [DOI] [PubMed] [Google Scholar]
- 38. Ishihara S, Kiyomatsu T, Kawai K, et al. The short-term outcomes of robotic sphincter-preserving surgery for rectal cancer: comparison with open and laparoscopic surgery using a propensity score analysis. Int J Colorectal Dis 2018;33:1047–1055. [DOI] [PubMed] [Google Scholar]
- 39. Jayne D, Pigazzi A, Marshall H, et al. Effect of robotic-assisted vs conventional laparoscopic surgery on risk of conversion to open laparotomy among patients undergoing resection for rectal cancer: the ROLARR randomized clinical trial. JAMA 2017;318:1569–1580. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40. Kang J, Yoon KJ, Min BS, et al. The impact of robotic surgery for mid and low rectal cancer: a case-matched analysis of a 3-arm comparison--open, laparoscopic, and robotic surgery. Ann Surg 2013;257:95–101. [DOI] [PubMed] [Google Scholar]
- 41. Kethman WC, Harris AHS, Morris AM, et al. Oncologic and perioperative outcomes of laparoscopic, open, and robotic approaches for rectal cancer resection: a multicenter, propensity score-weighted cohort study. Dis Colon Rectum 2020;63:46–52. [DOI] [PubMed] [Google Scholar]
- 42. Kim JY, Kim NK, Lee KY, et al. A comparative study of voiding and sexual function after total mesorectal excision with autonomic nerve preservation for rectal cancer: laparoscopic versus robotic surgery. Ann Surg Oncol 2012;19:2485–2493. [DOI] [PubMed] [Google Scholar]
- 43. Kim YS, Kim MJ, Park SC, et al. Robotic versus laparoscopic surgery for rectal cancer after preoperative chemoradiotherapy: case-matched study of short-term outcomes. Cancer Res Treat 2016;48:225–231. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44. Kim MJ, Park SC, Park JW, et al. Robot-assisted versus laparoscopic surgery for rectal cancer: a phase II open label prospective randomized controlled trial. Ann Surg 2018;267:243–251. [DOI] [PubMed] [Google Scholar]
- 45. Liu W-H, Yan P-J, Hu D-P, et al. Short-term outcomes of robotic versus laparoscopic total mesorectal excision for rectal cancer: a cohort study. Am Surg 2019;85:294–302. [PubMed] [Google Scholar]
- 46. Lim DR, Bae SU, Hur H, et al. Long-term oncological outcomes of robotic versus laparoscopic total mesorectal excision of mid-low rectal cancer following neoadjuvant chemoradiation therapy. Surg Endosc 2017;31:1728–1737. [DOI] [PubMed] [Google Scholar]
- 47. Park JS, Choi GS, Lim KH, et al. S052: a comparison of robot-assisted, laparoscopic, and open surgery in the treatment of rectal cancer. Surg Endosc 2011;25:240–248. [DOI] [PubMed] [Google Scholar]
- 48. Patriti A, Ceccarelli G, Bartoli A, et al. Short- and medium-term outcome of robot-assisted and traditional laparoscopic rectal resection. JSLS 2009;13:176. [PMC free article] [PubMed] [Google Scholar]
- 49. Ramji KM, Cleghorn MC, Josse JM, et al. Comparison of clinical and economic outcomes between robotic, laparoscopic, and open rectal cancer surgery: early experience at a tertiary care center. Surg Endosc 2016;30:1337–1343. [DOI] [PubMed] [Google Scholar]
- 50. Rouanet P, Bertrand MM, Jarlier M, et al. Robotic versus laparoscopic total mesorectal excision for sphincter-saving surgery: results of a single-center series of 400 consecutive patients and perspectives. Ann Surg Oncol 2018;25:3572–3579. [DOI] [PubMed] [Google Scholar]
- 51. Silva-Velazco J, Dietz DW, Stocchi L, et al. Considering value in rectal cancer surgery: an analysis of costs and outcomes based on the open, laparoscopic, and robotic approach for proctectomy. Ann Surg 2017;265:960–968. [DOI] [PubMed] [Google Scholar]
- 52. Shiomi A, Kinugasa Y, Yamaguchi T, et al. Robot-assisted versus laparoscopic surgery for lower rectal cancer: the impact of visceral obesity on surgical outcomes. Int J Colorectal Dis 2016;31:1701–1710. [DOI] [PubMed] [Google Scholar]
- 53. Sugoor P, Verma K, Chaturvedi A, et al. Robotic versus laparoscopic sphincter-preserving total mesorectal excision: a propensity case-matched analysis. Int J Med Robot 2019;15:e1965. [DOI] [PubMed] [Google Scholar]
- 54. Valverde A, Goasguen N, Oberlin O, et al. Robotic versus laparoscopic rectal resection for sphincter-saving surgery: pathological and short-term outcomes in a single-center analysis of 130 consecutive patients. Surg Endosc 2017;31:4085–4091. [DOI] [PubMed] [Google Scholar]
- 55. Yamaguchi T, Kinugasa Y, Shiomi A, et al. Robotic-assisted vs. conventional laparoscopic surgery for rectal cancer: short-term outcomes at a single center. Surg Today 2016;46:957–962. [DOI] [PubMed] [Google Scholar]
- 56. Park SY, Choi GS, Park JS, et al. Short-term clinical outcome of robot-assisted intersphincteric resection for low rectal cancer: a retrospective comparison with conventional laparoscopy. Surg Endosc 2013;27:48–55. [DOI] [PubMed] [Google Scholar]
- 57. Fernandez R, Anaya DA, Li LT, et al. Laparoscopic versus robotic rectal resection for rectal cancer in a veteran population. Am J Surg 2013;206:509–517. [DOI] [PubMed] [Google Scholar]
- 58. Somashekhar SP, Ashwin KR, Rajashekhar J, et al. Prospective randomized study comparing robotic-assisted surgery with traditional laparotomy for rectal cancer—Indian study. Indian J Surg 2015;77(Suppl 3):788. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59. Yang S-X, Sun Z-Q, Zhou Q-B, et al. Security and radical assessment in open, laparoscopic, robotic colorectal cancer surgery: a comparative study. Technol Cancer Res Treat 2018;17:1533033818794160. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60. Mégevand JL, Lillo E, Amboldi M, et al. TME for rectal cancer: consecutive 70 patients treated with laparoscopic and robotic technique-cumulative experience in a single centre. Updates Surg 2019;71:331–338. [DOI] [PubMed] [Google Scholar]
- 61. Song SH, Choi GS, Kim HJ, et al. Long-term clinical outcomes of total mesorectal excision and selective lateral pelvic lymph node dissection for advanced low rectal cancer: a comparative study of a robotic versus laparoscopic approach. Tech Coloproctol 2021;25:413–423. [DOI] [PubMed] [Google Scholar]
- 62. Feng Q, Ng SSM, Zhang Z, et al. Comparison between robotic natural orifice specimen extraction surgery and traditional laparoscopic low anterior resection for middle and low rectal cancer: a propensity score matching analysis. J Surg Oncol 2021;124:607–618. [DOI] [PubMed] [Google Scholar]
- 63. Tilney HS, Huddy JR, Nizar AS, et al. Minimal access rectal cancer surgery: an observational study of patient outcomes from a district general hospital with over a decade of experience with robotic rectal cancer surgery. Colorectal Dis 2021;23:1961–1970. [DOI] [PubMed] [Google Scholar]
- 64. Ose I, Perdawood SK. A nationwide comparison of short-term outcomes after transanal, open, laparoscopic, and robot-assisted total mesorectal excision. Colorectal Dis 2021;23:2671–2680. [DOI] [PubMed] [Google Scholar]
- 65. Ali M, Zhu X, Wang Y, et al. A retrospective study of post-operative complications and cost analysis in robotic rectal resection versus laparoscopic rectal resection. Front Surg 2022;9:969038. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66. Feng Q, Yuan W, Li T, et al. Robotic versus laparoscopic surgery for middle and low rectal cancer (REAL): short-term outcomes of a multicentre randomised controlled trial. Lancet Gastroenterol Hepatol 2022;7:991–1004. [DOI] [PubMed] [Google Scholar]
- 67. Park SY, Lee SM, Park JS, et al. Robot surgery shows similar long-term oncologic outcomes as laparoscopic surgery for mid/lower rectal cancer but is beneficial to ypT3/4 after preoperative chemoradiation. Dis Colon Rectum 2021;64:812–821. [DOI] [PubMed] [Google Scholar]
- 68. Feng Q, Tang W, Zhang Z, et al. Robotic versus laparoscopic abdominoperineal resections for low rectal cancer: a single-center randomized controlled trial. J Surg Oncol 2022;126:1481–1493. [DOI] [PubMed] [Google Scholar]
- 69. Park JS, Lee SM, Choi GS, et al. Comparison of laparoscopic versus robot-assisted surgery for rectal cancers: the COLRAR randomized controlled trial. Ann Surg 2023;278:31–38. [DOI] [PubMed] [Google Scholar]
- 70. Corbellini C, Biffi R, Luca F, et al. Open, laparoscopic, and robotic surgery for rectal cancer: medium-term comparative outcomes from a multicenter study. Tumori 2016;102:414–421. [DOI] [PubMed] [Google Scholar]
- 71. Law WL, Foo DCC. Comparison of short-term and oncologic outcomes of robotic and laparoscopic resection for mid- and distal rectal cancer. Surg Endosc 2017;31:2798–2807. [DOI] [PubMed] [Google Scholar]
- 72. Mushtaq HH, Shah SK, Agarwal AK. The current role of robotics in colorectal surgery. Curr Gastroenterol Rep 2019;21:11. [DOI] [PubMed] [Google Scholar]
- 73. Spinoglio G, Summa M, Priora F, et al. Robotic colorectal surgery: first 50 cases experience. Dis Colon Rectum 2008;51:1627–1632. [DOI] [PubMed] [Google Scholar]
- 74. Sun Y, Xu H, Li Z, et al. Robotic versus laparoscopic low anterior resection for rectal cancer: a meta-analysis. World J Surg Oncol 2016;14:61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 75. Kowalewski KF, Seifert L, Ali S, et al. Functional outcomes after laparoscopic versus robotic-assisted rectal resection: a systematic review and meta-analysis. Surg Endosc 2021;35:81–95. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 76. Trastulli S, Farinella E, Cirocchi R, et al. Robotic resection compared with laparoscopic rectal resection for cancer: systematic review and meta-analysis of short-term outcome. Colorectal Dis 2012;14:e134–5. [DOI] [PubMed] [Google Scholar]
- 77. Ong MLH, Schofield JB. Assessment of lymph node involvement in colorectal cancer. World J Gastrointest Surg 2016;8:179. [DOI] [PMC free article] [PubMed] [Google Scholar]
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