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. Author manuscript; available in PMC: 2024 Mar 1.
Published in final edited form as: Ann Surg. 2022 Sep 8;277(3):387–396. doi: 10.1097/SLA.0000000000005698

The RECOURSE Study: Long-term oncologic outcomes associated with Robotically assisted minimally invasive procedures for Endometrial, Cervical, cOlorectal, lUng, or pRoState cancEr: a systematic review and meta-analysis

Mario M Leitao Jr 1,2,*, Usha S Kreaden 3, Vincent Laudone 4, Bernard J Park 5, Emmanouil P Pappou 6, John W Davis 7, David C Rice 8, George J Chang 9, Emma C Rossi 10, April E Hebert 3, April Slee 11, Mithat Gonen 12
PMCID: PMC9905254  NIHMSID: NIHMS1832957  PMID: 36073772

Abstract

Objective:

To assess long-term outcomes with robotic versus laparoscopic/thoracoscopic and open surgery for colorectal, urologic, endometrial, cervical, and thoracic cancers.

Summary Background Data:

Minimally invasive surgery provides perioperative benefits and similar oncological outcomes compared with open surgery. Recent robotic surgery data have questioned long-term benefits.

Methods:

A systematic review and meta-analysis of cancer outcomes based on surgical approach was conducted based on PRISMA guidelines using Pubmed, Scopus, and Embase. HRs for recurrence, disease-free survival (DFS), and overall survival (OS) were extracted/estimated using a hierarchical decision-tree and pooled in RevMan 5.4 using inverse-variance fixed effect (heterogeneity non-significant) or random effect models.

Results:

Of 31,204 references, 199 were included (7 randomized, 23 database, 15 prospective, 154 retrospective studies)—157,876 robotic, 68,007 laparoscopic/thoracoscopic, and 234,649 open cases. Cervical cancer: OS and DFS were similar between robotic and laparoscopic (1.01[0.56, 1.80], p=0.98) or open (1.18[0.99, 1.41], p=0.06) surgery; two papers reported less recurrence with open surgery (2.30[1.32, 4.01], p=0.003). Endometrial cancer: the only significant result favored robotic over open surgery (OS; 0.77[0.71, 0.83], p<0.001). Lobectomy: DFS favored robotic over thoracoscopic surgery (0.74[0.59, 0.93], p=0.009); OS favored robotic over open surgery (0.93[0.87, 1.00], p=0.04). Prostatectomy: recurrence was less with robotic versus laparoscopic surgery (0.77[0.68, 0.87], p<0.0001); OS favored robotic over open surgery (0.78[0.72, 0.85], p<0.0001). Low-anterior resection: OS significantly favored robotic over laparoscopic (0.76[0.63, 0.91], p=0.004) and open surgery (0.83[0.74, 0.93], p=0.001).

Conclusion:

Long-term outcomes were similar for robotic versus laparoscopic/thoracoscopic and open surgery, with no safety signal or indication requiring further research (PROSPERO Reg#CRD42021240519).

Keywords: robotic-assisted surgery, colorectal cancer, urologic cancer, endometrial cancer, cervical cancer, thoracic cancer

MINI-ABSTRACT

Findings of recent cervical cancer trials have demonstrated compromised outcomes with minimally invasive surgery, leading to a decline in its usage. We assessed long-term outcomes associated with robotic-assisted surgery compared to laparoscopic/thoracoscopic or open surgery for specific types of procedures for the treatment of colorectal, urologic, endometrial, cervical, and thoracic cancers. Long-term outcomes, including recurrence and survival, were similar among the three surgical approaches, and in some cases favored robotic-assisted surgery.

INTRODUCTION

Minimally invasive surgery (MIS) is an ever evolving and increasingly accepted approach for the management of patients with solid tumors, albeit with reservation by some surgeons. Specifically, the reliance on an endoscopic camera, insufflation, and long instruments without direct manual palpation may limit dexterity, compromise the ability to achieve a complete resection, or cause cancer cell contamination in the operative space. Although the majority of the literature regarding conventional laparoscopy is retrospective, the results of randomized trials have also shown its safety and efficacy compared to open surgery in endometrial,1–4 rectal,5–11 and colon cancer.11–14

Robotically assisted (computer-enhanced) laparoscopic surgery (RAS) is another form of MIS, which began gaining traction after the approval of the da Vinci™® surgical system (Intuitive Surgical®, Sunnyvale, CA, USA) in 2000. The potential technical advantages of RAS over conventional laparoscopic/thoracoscopic or open surgery include stable 3D high-definition video, multiple wristed instruments for greater maneuverability, and digital processing to scale motion and filter out physiologic tremor for more precise dissection. Ergonomic advantages include the surgeon’s ability to operate in a neutral, comfortable posture, minimizing fatigue.15 Despite these advantages, recent studies have shown worse long-term outcomes with MIS versus open surgery in the management of cervical cancer,16–17 leading to a decline in its use for this indication.18–19

We performed a systematic literature review and meta-analysis to assess outcomes, including recurrence and survival, associated with representative procedures used in colorectal, urologic, gynecologic, and thoracic cancer surgery performed via RAS versus a laparoscopic/thoracoscopic or open approach. The procedures—low-anterior resection (LAR), prostatectomy, hysterectomy for endometrial or cervical cancer, and pulmonary lobectomy—were selected for analysis as they are high-volume, highly adapted procedures using the various surgical approaches. We hypothesized that oncologic outcomes associated with RAS are not inferior to those of the more established MIS and open techniques.

METHODS

This systematic literature review and meta-analysis was conducted in accordance with Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA; Supplementary Tables 1 and 2) and is registered in the PROSPERO international prospective register of systematic reviews (CRD42021240519). PubMed, Scopus, and Embase databases were searched using combinations of robotic terms (e.g., robot*, “da Vinci”, davinci, “Intuitive Surgical”), procedure terms (e.g., prostatectomy, hysterectomy, lobectomy, low-anterior resection), anatomical or system terms (e.g., prostate or urology, cervical or gynecology, lung, rectum), and indication terms (e.g., cancer, malignant, neoplasm, etc.). Separate searches were performed for each procedure spanning 1/2010–9/2020 (Supplementary Tables 3-5).

Three researchers screened the references, with random-sample validation checking. Randomized controlled trials (RCTs), independent database studies, and retrospective or prospective studies comparing robotic to non-robotic MIS, laparoscopic, thoracoscopic, or open surgery (with ≥20 cases for each comparator) were eligible. Reviews, meta-analyses, case series, case reports, editorials, and other studies were excluded. Studies included were in English, reported on adults, included surgeries performed using standard techniques (i.e., no transanal or single-port procedures), and stratified the analysis for at least one data point, such that all of the following were true: cancer cases were separate from benign cases; robotic cases were separate from other surgical cases; the procedure of interest was separate or comprised the majority of cases; at least one outcome of interest was reported (long-term [≥12 months] recurrence, disease-free/recurrence-free survival [DFS/RFS], biochemical recurrence [BCR]-free/progression-free survival [PFS], or overall survival [OS]); and patient populations were not duplicated. Data measured as the time from surgery to first recurrence or death from any cause, with patients censored when lost to follow-up, was preferentially used in the DFS analysis.20 The details of the methods of data extraction and analysis are described elsewhere.21

A statistician and independent, outside researcher reviewed the data for accuracy and extracted, calculated, derived, or estimated the hazard ratio (HR) and confidence interval (CI) for each study and comparison using one of four methods in order, based on the data provided: 1) used the HR and CI reported in the paper, 2) estimated the HR using the event n and a log-rank or Cox proportional hazard p-value, 3) derived the HR by digitizing the KM curve and using the algorithm by Guyot,22 or 4) estimated the HR using the KM estimate and a log-rank or Cox proportional hazard p-value.21 Supplementary Figure 1 details the decision tree used. Discrepancies were reviewed by the statistician and resolved via consensus of three researchers. If an HR could not be calculated, derived, or estimated, a risk ratio was calculated. When only a single paper reported data for a comparison or an outcome of interest, the results could not be pooled and were reported separately.

Comparisons and outcomes with available HRs for at least two papers were pooled in an “unadjusted HR analysis”. Papers reporting multivariable, adjusted, or matched data, and papers with comparable cohorts made up the main “adjusted HR analysis”, with the two groups (adjusted/matched and comparable) treated as subgroups. Cohorts were deemed comparable when parameters known to influence survival outcomes were not significant (e.g., stage, grade, resection margins, PSA, lymph node yield, etc.). Forest Plots and pooled HR analyses were performed with RevMan 5.4. A fixed-effect model was used when heterogeneity was not significant (p≥0.05 or I2≤50%); a random-effects model was used when it was significant. The comparator group was treated as the reference group in all comparisons. The Cochrane Risk of Bias 2 (RoB 2) tool was used to assess risk of bias in randomized trials,23 and the Risk of Bias in Non-randomized Studies – of Interventions (ROBINS-I) tool was used to assess risk of bias in non-randomized trials.24 Assessments were performed by procedure, by comparison, and by outcome of interest.

RESULTS

Following PRISMA guidelines, the searches identified 53,277 overall references, 31,204 unique references, 8,967 relevant references, and 1,555 studies comparing robotic surgery to another surgical approach; 199 studies met the inclusion criteria and were included in the review (flowcharts in Supplementary Figures 2-6). Of these, 7 were RCTs, 23 were database studies, 15 were prospective cohort comparison studies, and 154 were retrospective cohort comparison studies (bibliography in Supplementary Appendix A). An HR was available or calculated for at least one outcome in 139 studies, and 116 studies provided sufficient data to include them in the adjusted HR analysis.

Study characteristics by disease site for papers included in the HR analysis are provided in Supplementary Tables 6-9, with pathological outcomes for these papers provided in Supplementary Table 10; study characteristics for the remaining papers are provided in Supplementary Table 11. The seven RCTs showed high bias in the measurement of the outcome due to shorter than ideal follow-up for survival outcomes. The non-randomized studies showed moderate-to-critical bias for confounding and selection of participants domains, as well as low-to-moderate bias for the majority of procedures, comparisons, and outcomes for the remaining domains (risk of bias in Supplementary Tables 12, 13).

The forest plots for our meta-analysis where an adjusted/balanced HR could be obtained from at least two studies are detailed in Figures 1–5 and Supplementary Figure 7 and funnel plots are provided in Supplementary Figure 8. A summary of the results of the unadjusted HR analysis is provided in Supplementary Table 14.

Figure 1. Cervical Cancer Forest Plots.

Figure 1.

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Forest plots showing hazard ratios for individual papers as well as pooled outcomes for cervical cancer for A) incidence of recurrence for RAS vs OPEN, B) disease-free survival (DFS) for RAS vs LAP, and C) for RAS vs OPEN, D) overall survival (OS) for RAS vs LAP, and E) for RAS vs OPEN. RAS=robotic-assisted surgery, LAP=laparoscopy, OPEN=open surgery, CI=confidence interval, BMI=body mass index, KM=Kaplan-Meier, yr=year, mo=month, HR=hazard ratio, FU=follow-up, sig=significant, diff=different, PFS=progression-free survival, calc=calculated, DOD=dead of disease, DOO=dead of other, AWD=alive with disease.

Figure 5. Forest Plots for Low-Anterior Resection for Rectal Cancer.

Figure 5.

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Forest plots of hazard ratios for low-anterior resection for rectal cancer. A) local recurrence RAS vs. LAP, and B) for RAS vs. OPEN, C) Disease-Free Survival (DFS) for RAS vs. LAP, and D) for RAS vs. OPEN, E) Overall Survival (OS) for RAS vs. LAP, and F) for RAS vs. OPEN.

For cervical cancer, only two papers reported on recurrence, with less recurrence in the open approach (HR: 2.30 [1.32, 4.01], p=0.003). There were no significant differences in DFS or OS between RAS and laparoscopy or open hysterectomy (Figure 1). There was a possible OS trend favoring open surgery over RAS (HR: 1.18 [0.99, 1.41], p=0.06) driven by the subgroup of matched/adjusted studies (subgroup HR: 1.39 [1.14, 1.69], p=0.001). The subgroup of papers with comparable cohorts favored RAS (subgroup HR: 0.67 [0.46, 0.97], p=0.04; Figure 1E).

For endometrial cancer, OS favored RAS over open surgery (HR: 0.77 [0.71, 0.83], p<0.001) (Figure 2).

Figure 2. Endometrial Cancer Forest Plots.

Figure 2.

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Forest plots showing hazard ratios for individual papers as well as pooled outcomes for endometrial cancer for A) disease-free survival (DFS) for RAS vs. LAP, and B) for RAS vs. OPEN, C) overall survival for RAS vs. LAP, and D) for RAS vs. OPEN. RAS=robotic-assisted surgery, LAP=laparoscopy, OPEN=open surgery, CI=confidence interval, BMI=body mass index, KM=Kaplan-Meier, yr=year, mo=month, HR=hazard ratio, FU=follow-up, sig=significant, diff=different, PFS=progression-free survival, calc=calculated, DOD=dead of disease, DOO=dead of other, AWD=alive with disease.

For lobectomy for lung cancer (Figure 3), DFS favored RAS over video-assisted thoracoscopic surgery (VATS; HR: 0.74 [0.59, 0.93], p=0.009) and OS favored RAS over open surgery (HR: 0.93 [0.87, 1.00], p=0.04).

Figure 3. Lobectomy for Lung Cancer Forest Plots.

Figure 3.

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Forest plots showing hazard ratios for individual papers as well as pooled outcomes for lobectomy for lung cancer for A) disease-free survival (DFS) for RAS vs. VATS, and B) for RAS vs. OPEN, C) overall survival (OS) for RAS vs. VATS, and D) for RAS vs. OPEN. RAS=robotic-assisted surgery, VATS=video-assisted thoracoscopic surgery, OPEN=open surgery, CI=confidence interval, KM=Kaplan-Meier, ref=reference group, sig=significant, diff=different, clin=clinical, pt=patient.

For prostatectomy for prostate cancer (Figure 4), BCR favored RAS over laparoscopy (HR: 0.77 [0.68, 0.87], p<0.0001) and OS favored RAS over open surgery (HR: 0.78 [0.72, 0.85], p<0.0001).

Figure 4. Prostatectomy Forest Plots.

Figure 4.

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Forest plots showing hazard ratios for individual papers as well as pooled outcomes for prostate cancer for A) Biochemical-recurrence (BCR) for RAS vs. LAP (BCR for RAS vs. OPEN is in Supplementary Figure 7), B) BCR-Free Survival (BCRFS) for RAS vs. LAP and for C) RAS vs. OPEN, D) Overall Survival (OS) for RAS vs. LAP and for E) RAS vs. OPEN. RAS=robotic-assisted surgery, LAP=laparoscopy, OPEN=open surgery, CI=confidence interval, KM=Kaplan-Meier, GS=gleason score, NS=not significant, yr=year, mo=month, HR=hazard ratio, ref=reference group, sig=significant, calc=calculated.

For LAR for rectal cancer (Figure 5), OS favored RAS over laparoscopy (HR: 0.76 [0.63, 0.91], p=0.004) and open surgery (HR: 0.83 [0.74, 0.93], p=0.001).

DISCUSSION

To our knowledge, this is the largest analysis of cancer survival and recurrence across multiple RAS procedures, with 199 publications and more than 400,000 patients. We did not find an overarching association of adverse oncologic outcomes with four RAS procedures for the treatment of rectal, prostate, cervical, endometrial, and lung cancer. We did not find an overall safety signal for RAS that inherently makes it inferior to open or non-robotic MIS.

In early 2019,25 and updated in 2021,26 the FDA released a safety communication advising caution when using the robotic surgical platform for cancer-related surgeries due to a lack of established evidence. Our findings, however, did not show statistically worse outcomes with RAS; in fact, some results showed statistically improved outcomes. We do, however, recognize a worse OS trend with RAS over open surgery in cervical cancer, and a higher recurrence rate in the only two studies used for this metric.

To overcome the lack of standardized methodology for reporting cancer outcomes in surgical studies, we applied a uniform statistical approach to calculate HRs for cancer recurrence, DFS, and OS; and although the approach has limitations, it is supported by other publications and the Cochrane manual—the gold standard for meta-analyses.27

Outside of surgical approach, there are numerous variables associated with oncologic outcomes, including accurate staging and type of postoperative therapy used. In addressing the issue of whether poor technique was compensated for with non-operative therapy, we found the relationship between short-term oncologic results and long-term recurrence was directionally similar (data not shown). However, the skill, experience, and mindset of the surgeon cannot be overlooked. For example, in the Australasian Laparoscopic Cancer of Rectum (AlaCaRT) randomized trial, intraoperative surgical skill assessment was significantly associated with clinical and pathologic outcome.28 Furthermore, outcomes can vary across institutions, particularly with complex cancer surgeries, based on volume, experience, and skill.29,30

A strength of our study is the comprehensive approach in including all data from all types of studies. The limitations of our study include the vast amount of retrospective data, with minimal patient data from prospective trials or RCTs, which are considered highest level evidence. Real-world evidence, however, particularly when summarized in a meta-analysis or systemic literature review, can complement RCT data.31

Hysterectomy for Cervical Cancer

Only two studies reported recurrence rates between RAS and open surgery, making the significance of the findings unclear. One of these studies was included in the DFS analysis.32 Compared with laparoscopy, RAS was not associated with differences in DFS or OS, and there was no difference in DFS for RAS compared with open surgery. However, while not statistically significant, RAS compared with open surgery was associated with a trend toward worse OS, with the OS data heavily weighted by one study.16 Surgical modalities can influence OS directly through increased perioperative morbidity and mortality, which has not been observed with RAS,33 or through inadequate or inappropriate cancer resection, leading to recurrences and corresponding impaired DFS (not observed in this study). Beyond this, the inferior OS between one cancer surgical modality and another is likely the result of unmeasured confounders and not the inferiority of a specific surgical modality.

The Laparoscopic Approach to Cervical Cancer (LACC) trial has been the only RCT in this setting,17 demonstrating worse oncologic outcome with MIS (the majority were laparoscopies) over open surgery in patients with cervical cancer undergoing radical hysterectomy. It has also been the only RCT in any cancer to demonstrate worse oncologic outcomes with MIS. We included this study in our DFS but not OS analysis, as we could not derive HRs specific to RAS and laparoscopy or open surgery. Criticisms of the LACC trial include the lack of tumor containment and differences in surgeon experience, among others. There are two ongoing RCTs for women with cervical cancer undergoing radical hysterectomy—the RACC (Robot-assisted Approach to Cervical Cancer) trial, which is comparing RAS to open surgery,34 and a trial in China, which is comparing MIS to open surgery.35 The ROCC (Robotic versus Open Radical Hysterectomy for Cervical Cancer) trial, which will soon open in the US, will compare RAS to open surgery.36

Hysterectomy for Endometrial Cancer

RAS was associated with better OS compared to open surgery; DFS was statistically similar. The reason for this improvement is unclear but may be due to unmeasured confounders. Patients who have endometrial cancer staging surgery via MIS, particularly RAS, are more likely to undergo comprehensive staging,37 which has been shown to minimize overtreatment with toxic adjuvant therapies.38 This thoroughness of staging with RAS may indirectly improve OS for patients with endometrial cancer by minimizing non-surgical treatment-related harms. Compared to laparoscopy, there were no differences in DFS or OS associated with RAS. Our findings are in line with published RCTs establishing MIS as the standard approach in women with endometrial cancer.1–4 The MIS arms of these RCTs were all laparoscopic, as they were conducted prior to the widespread adoption of RAS in gynecologic oncology. Our analysis does not show adverse oncologic outcomes with RAS in endometrial cancer.

Lobectomy for Lung Cancer

RAS was associated with better DFS over VATS, in agreement with a recent, smaller meta-analysis.39 There was no difference in DFS between RAS and open surgery (Figure 3B). RAS was associated with better OS compared with open surgery and a trend toward better OS compared with VATS. A 2020 paper by Cui et al.,40 which was indexed in Pubmed after our search end date, reported worse OS with RAS compared with VATS for a small subset of patients with stage I non–small cell lung cancer (NSCLC) and tumors smaller than 20 mm at a follow-up starting 12 months after surgery. However, a paper by Hennon et al.,41 which was included in our unadjusted analysis, reported on a subgroup propensity-weighted analysis of all stage I patients using the same database, the same time frame, and nearly identical patients as those of the Cui study and demonstrated no difference in 5-year OS (p=0.0651). Further studies to determine the best treatment for specific subpopulations may be warranted.

Prostatectomy for Prostate Cancer

In the matched analyses, robotic-assisted prostatectomy was associated with decreased recurrence compared with laparoscopy and increased OS compared with open surgery. DFS could not be analyzed, as BCR-free survival was often reported in its place. It is possible that robotic over laparoscopic instrumentation provides technical advantages deep in the pelvis that lessen the risk of recurrence, but this should hold true for hysterectomy and LAR as well.

The first laparoscopic prostatectomy was performed in 1991,42 and the first robotic-assisted prostatectomy was performed in 2001.43 Since then, the thousands of peer-reviewed papers on robotic-assisted prostatectomy almost all have focused on surgical technique, operative results, pathologic findings, postoperative recovery, or mid-term outcomes related to urinary and sexual function. Few have reported long-term oncologic outcomes, and those that do are generally limited to BCR, which is dependent upon a wide variety of clinical factors and is a poor predictor of disease-specific survival (DSS) or OS.44 With regard to localized prostate cancer, robust outcomes require large patient cohorts and follow-up of at least 10–15 years given the generally slow pace of disease development and the multiple competing causes of death in this older population.45 The overwhelming adoption of RAS for the treatment of prostate cancer makes it unlikely there will ever be a meaningful comparison with open surgery. The short-term benefits of minimally invasive prostatectomy coupled with the promising oncological outcomes reported in robotic, single-arm studies46–48 suggest this type of comparison is moot.

LAR/Total Mesorectal Excision for Rectal Cancer

There were no significant differences in rate of recurrence or DFS between RAS and laparoscopic or open surgery. This is consistent with data from other systematic reviews, including one that compared oncologic outcomes between laparoscopic and RAS proctectomy and included one randomized study (ROLARR trial) and 27 comparative studies, which concluded that oncological variables such as recurrence, number of harvested nodes, positive circumferential resection margin risk, and distal resection margin were all similar in both groups.49 Similarly, findings from a recent network meta-analysis of 30 RCTs (and six updates) with 5586 patients with rectal cancer demonstrated no differences in long-term oncologic outcomes between open, laparoscopic, robotic-assisted, and transanal proctectomy approaches.50 It is not clear why RAS was associated with OS improvement in our study; we did not perform an analysis of short-term morbidity or other non-oncologic outcomes. Furthermore, the RAS versus open surgery analysis was heavily weighted by a non-randomized, observational study by Chapman et al.,51 which used the National Cancer Database and is therefore subject to a significant risk of selection bias.

Conclusion

This was an extensive review covering 2 decades of literature on cancer outcomes associated with five procedures for the treatment of cervical, endometrial, colorectal, lung, and prostate cancer. We show that RAS is associated with similar outcomes to those of laparoscopic/thoracoscopic and open surgery. RAS was not associated with worse outcomes with any procedure; in contrast, RAS was associated with better outcomes in certain settings. The clinical significance of these findings is unclear given the various methods of measuring cancer outcomes, the effect of adjuvant therapy, and the role of the surgeon and patient variables.

Supplementary Material

Supplemental Data File

Acknowledgements

The authors would like to acknowledge the contributions of the following individuals: Samira Massachi participated in reference screening. Ana Yankovsky and Samira participated in data extraction, data quality checks, and risk of bias assessments. Dongjing Guo and Yang Li helped with data extraction and data quality checking. Shih-Hao Lee and Yuki Liu performed the method 3 simulations. Angela Soito supervised data collection and interpreted results.

Funding:

Drs. Leitao, Laudone, Park, and Pappou are funded in part by the NIH/NCI Cancer Center Support Grant P30 CA008748.

Footnotes

Conflict of Interest Statement

MM Leitao reports personal fees from Johnson and Johnson/Ethicon and Takeda, as well as grants paid to the institution from KCI/Acelity; he is also an ad hoc speaker for Intuitive Surgical, Inc. US Kreaden and AE Hebert are employees of Intuitive Surgical, Inc. BJ Park reports personal fees from Intuitive Surgical Inc. and AstraZeneca, as well as stock ownership of CEERVA. EC Rossi reports personal fees from Intuitive Surgical, Inc. JW Davis reports personal fees from Intuitive Surgical, Inc. and research funding from Janssem. GJ Chang reports personal fees from Medicaroid. DC Rice reports personal fees and research funding from Intuitive Surgical, Inc.

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