Conventional and robot-assisted minimally invasive esophagectomy: literature review of the current state and future directions

Introduction

According to the Global Cancer Statistics 2020, esophageal cancer is the 11^th most commonly diagnosed cancer and is the seventh leading cause of cancer death worldwide (1). Though surgery remains integral to most curative intent esophageal cancer treatment plans, esophagectomy continues to be associated with significant morbidity and mortality, reduced quality of life (QOL), and limited 5-year survival rates (30–50%) (2,3).

Minimally invasive techniques for esophagectomy, including conventional laparoscopic/thoracoscopic minimally invasive esophagectomy (MIE) and robot-assisted minimally invasive esophagectomy (RAMIE) have been increasingly incorporated into surgical practice (4). However, there continues to be variation in surgical technique employed and the superiority of any one technique is unclear given their differing operative and postoperative outcomes and complexities. Thus, the aim of this narrative review is to compare published outcomes of open esophagectomy, MIE, and RAMIE for esophageal cancer, as well as future perspectives for the field of surgical treatment of esophageal cancer. We present this article in accordance with the Narrative Review reporting checklist (available at https://vats.amegroups.com/article/view/10.21037/vats-24-22/rc).

Methods

We performed a review of relevant studies surrounding MIE and RAMIE using PubMed (Table 1). We identified studies that were published in the English language. Randomized controlled trials (RCTs) had no publication date restriction. Meta-analyses were restricted by publication on or after January 2014. The literature was evaluated in respect to perioperative outcomes, postoperative outcomes, long-term outcomes, and learning curve, and focused on comparison between esophagectomy for esophageal cancer performed by different surgical techniques. Evaluation for inclusion was based on title and abstract. Meeting abstracts and duplicate publications were excluded.

Results

MIE vs. open esophagectomy: improvements in postoperative outcomes and QOL

Observational data has demonstrated the benefits of minimally invasive esophagectomies over open approaches. Meta-analyses published since 2014 comparing MIE to open esophagectomy have shown lower rates of overall morbidity, equivalent (or reduced) postoperative mortality, equivalent (or shorter) length of hospital stay, less blood loss, lower rates of pulmonary complications, equivalent (or lower) rates of major cardiovascular complications, and equivalent (or lower) rates of wound infections (5-15). There are no differences in anastomotic complications (indicating that MIE does not compromise the technical quality of the operation), recurrent laryngeal nerve palsy, intensive care unit stay, and rates of reoperations (5,7,8,15,16). The sum of the evidence also suggests that there are no significant differences in overall survival, disease-free survival, or recurrence rates (5-8,11,13,15,17,18). Importantly, 3 meta-analyses showed that patients who underwent a MIE had higher risks of paraconduit hernias, though recent evidence suggests that such hernias that are minimally symptomatic can be managed expectantly (19-22). Data on hybrid vs. total MIE are limited (23).

Because esophagectomy alters anatomy which can have gastrointestinal side effects and because esophageal cancer has a limited survival rate, optimizing QOL after esophagectomy is essential. One meta-analysis specifically compared QOL measures over the 6-month period following open esophagectomy and MIE found benefits in global health, social functioning and emotional functioning in favor of MIE, as compared to those who underwent an open procedure, but no difference in physical symptoms (24). Another analysis found similar results, showing better global QOL, physical functioning, less fatigue and lower pain scores at 3 months following surgery in the MIE group; however, these differences were no longer statistically significant after 6 and 12 months (25).

Several RCTs have been performed in the last 12 years analyzing outcomes of MIE as compared to an open procedure. Biere et al. published the first of these in The Lancet in 2012, the TIME (Traditional Invasive vs. Minimally Invasive Esophagectomy) trial, in which 115 patients with resectable esophageal and gastroesophageal junction cancers from 5 centers in Netherlands, Spain, and Italy were randomized to undergo either open esophagectomy or MIE 6–8 weeks after neoadjuvant therapy. About 60% in each group had adenocarcinomas and 95% were middle or lower third tumors. Most were treated with neoadjuvant chemoradiation therapy (92%) and most (about 65%) underwent modified McKeown esophagectomy. The primary outcome of interest was pulmonary infection in the first two weeks (26).

They found that the risk of pulmonary complications was significantly lower in the MIE group (9%) than the open group (29%). The trial has been criticized by the significantly higher rate of pulmonary complications in the open group, as compared with the rate of pneumonia reported in seminal case series of open esophagectomy, which inflated the difference between the groups. They also found lower rates of vocal-cord paralysis, shorter hospital stays, and better short-term health related QOL (HRQOL) scores (across domains of physical well-being and function, talking, and pain) in the MIE group. Importantly, there were no differences in the completeness of resections, number of lymph nodes, reoperations, in-hospital mortality, and 30-day mortality, thus demonstrating that MIE had short term benefits over an open procedure with no compromise in the quality of the resection (26). A follow-up of this study was performed at 1 year analyzing QOL and late complications. MIE resulted in durable QOL benefits after 1 year in terms of physical activity, global health, and pain as compared to open esophagectomy. There were no statistical differences in terms of anastomotic strictures, paraconduit hernias, recurrence, distant metastasis or survival (27). At 3-year follow-up, there was no differences in rates of overall and disease-free survival between the two groups (28). Taken together, these data from the TIME trial demonstrated that MIE resulted in less pulmonary complications and durable QOL benefits that extended to a year postoperatively without compromising the quality of the operation, including R0 resection rates, lymph node yields, anastomotic complications and survival (26-28).

The MIRO (OesphagectoMIe Pour Cancer paR Voie Conventionnelle ou CoeliO-Assiste) Trial was another multicenter trial of 13 institutions which randomized patients to open (n=103) or hybrid (laparoscopic and right thoracotomy approach; n=104) Ivor Lewis esophagectomy. Similar to TIME, about 60% of patients had adenocarcinomas and >70% had neoadjuvant therapy. The primary outcome was any complication at 30 days. Patients who underwent hybrid MIE had significantly less complications (36%) as compared with open Ivor Lewis esophagectomy (64%). Similar to TIME, the trial has been criticized for higher complication rates in the open group, as compared with outcomes reported in seminal series of open Ivor Lewis esophagectomy. On multivariable analysis, this translated in to 77% lower odds of major complications [adjusted odds ratio (aOR) 0.23; 95% confidence interval (CI): 0.12–0.44] and 50% lower odds of respiratory complications (aOR 0.50; 95% CI: 0.26–0.96), after adjusting for American Society of Anesthesiologists (ASA) score, neoadjuvant therapy use, tumor location, histology, R0 status, T stage, N stage and institution (29).

Similar to TIME, hybrid MIE did not compromise the quality, evidenced by no difference in lymph node counts, R0 resection rates, overall survival, and disease-free survival at 3- and 5-year follow-up (29,30). The hybrid procedure had short-term HRQOL benefits at 30 days (less reduction in role functioning and social functioning) and durable benefits at 3 years (better social function) and less chronic pain at 30 days (31). Overall, this study parallels that of TIME in demonstrating that a minimally invasive approach reduces pulmonary complications, has HRQOL benefits, and demonstrates equivalency in survival and oncological outcomes. Reduction in pulmonary complications as seen in the minimally invasive approach may provide benefit in terms of survival, as these complications are an independent risk factor for reduced survival.

A similar study, the ROMIO (Randomised Oesophagectomy: Minimally Invasive or Open) trial, is currently ongoing comparing hybrid esophagectomy through minimally invasive gastric mobilization and right thoracotomy with open surgery with respect to speed of recovery and comparison of 2-year outcomes of survival and clinical and patient-reported outcomes measures in 606 patients. Seventy-three of these participants were randomized to a totally minimally invasive procedure of which results will be reported separately. Current results of this study at 3-month post-randomization showed no statistically significant differences in total hospital stay, post-surgical stay, mortality within 30 or 90 days, and death during initial hospital stay. Further, there were no differences in positive resection margins, occurrence and severity of complications such as chest infection, and measures of post-surgical recovery including physical functioning. Body mass index (BMI) was identified as a factor affecting post-surgical recovery with data showing that patients who underwent hybrid surgery with a lower BMI had a faster recovery (32). Thus, the ROMIO trial did not replicate the results of the MIRO trial which may be attributable to patients in the ROMIO trial being of older age, of higher BMI, and having a higher prevalence of adenocarcinoma, and the study having higher R1 rates in both subgroups. A two-year follow up of this study will inform whether the equivalency in outcomes and survival between groups persists.

Observational results in conjunction with results from RCTs indicate that a conventional laparoscopic/thoracoscopic and hybrid MIE has lower complication rates and durable HRQOL benefits without compromising oncological outcomes. The outcomes of total vs. hybrid MIE require further study.

RAMIE vs. open esophagectomy

Minimally invasive procedures performed laparoscopically are limited by a two-dimensional view of a three-dimensional field and rigid instruments, whereas robot-assisted minimally invasive surgery offers the advantage of 7 degrees of freedom of movement, a stabilized three-dimensional, magnified view with articulating instruments allowing for greater visualization and precision (33). The first RAMIE was performed in 2003 on a patient with esophageal adenocarcinoma (34). Since then, a number of observational studies, RCTs, and meta-analyses have sought to elucidate the safety, feasibility, and potential benefits of utilization of a robot-assisted approach.

Indeed, observational studies and meta-analyses comparing RAMIE with open esophagectomy have shown that robot-assisted surgery may be superior or equivalent in lymph node yield, length of hospital stay, and R0 resection, and superior in terms of blood loss, wound infections, cardiac complications (i.e., atrial fibrillation) and pulmonary complications (4,35-40). Anastomotic leakage, a major complication of esophagectomy, has been noted to be increased in a robotic approach in an analysis (4). HRQOL measures such as pain scores have been shown to be better with RAMIE (39). While most studies suggest no difference in anastomotic complications and 30- and 90-day mortality rates (4,35-40), one meta-analysis (35) found that RAMIE had superior one- and five-year survival rates, as compared with open esophagectomy.

ROBOT-1 was the first RCT to compare RAMIE versus an open approach. This single institution study compared modified McKeown esophagectomy via a completely robotic (n=54) vs. an open approach (n=55). There were significantly less overall major complications at 30 days (the primary outcome) in the RAMIE (59%) vs. open approach (80%). Secondary outcomes showed lower rates of pulmonary complications and cardiac complications, higher functional recovery within the first 2 weeks post-surgery, less postoperative pain, and better QOL. In particular, there were higher HRQOL scores (specifically physical functioning) at discharge and 6 weeks in the robotic group. There were no statistically significant differences found in other complications including anastomotic leakage, mediastinitis, empyema, chylothorax, recurrent laryngeal nerve injury, and wound infections. No differences were found in readmission to the intensive care unit (ICU), reoperations, and oncological outcomes, including R0 resection and lymph node count, in-hospital mortality, or 30-, 60-, and 90-day mortality between groups (41). A follow up of this study after 5 years showed no difference in overall survival, disease-free survival, or recurrence (42). An important consideration in this study is that it was conducted in a single center in which surgeons had a joint experience of over 170 RAMIEs.

The results of the analyzed studies comparing RAMIE with an open approach indicate a superiority of a robotic approach in reducing post-operative complications and better HRQOL, without compromising oncological outcomes.

Conventional MIE vs. RAMIE

There is level 1 evidence supporting the benefits of conventional MIE and RAMIE over open esophagectomy. However, the data comparing MIE and RAMIE is less robust. Observational studies and meta-analyses comparing MIE and RAMIE have shown mixed results. While some studies have shown lower complication rates (especially pulmonary complications), lower anastomotic leak rates, and less blood loss with RAMIE, others have shown no difference in morbidity or 30- and 90-day mortality (37,43-54). Similarly, some meta-analysis suggest RAMIE offers higher R0 resection rates, lymph node yields (especially recurrent laryngeal lymph nodes), and 3-year survival rates, other studies found no difference in lymph node counts, R0 rates or survival (43,45,48,50,52,53).

Importantly, several studies have analyzed the impact of the learning curve for MIE vs. RAMIE on outcomes (55-57). These studies have indicated that although RAMIE comes with its own learning curve, it is often shorter than MIE for surgeons to gain proficiency and implementation of a structured training program can reduce the learning curve without compromising outcome. Gaining proficiency in MIE requires between 33–119 cases, whereas proficiency with RAMIE requires only 19–80 cases (55-63). An international consensus statement published in the Journal of Thoracic Disease indicated RAMIE is the preferred approach when a robotic surgical system is available regardless of the clinical stage or neoadjuvant therapy received (64).

Several RCTs are being conducted in order to better elucidate the differences in outcomes between these two approaches. The first of these studies is the RAMIE Trial, which began recruitment in 2017 to investigate the efficacy and safety of RAMIE and MIE in 362 patients in 6 high-volume centers in China (65). Results of the study thus far have demonstrated RAMIE to have a shorter operative duration and higher efficacy in terms of thoracic lymph node dissection, specifically recurrent laryngeal lymph nodes in patients that received neoadjuvant therapy. Comparable outcomes were found for major complications, pulmonary complications, cardiac complications, anastomotic leakage, vocal cord paralysis, chylothorax, wound infections, ICU stay, readmission to ICU, in hospital mortality, 30-day mortality, and 90-day mortality. Other comparable results included blood loss, conversion to open procedure, radicality of surgery, number of lymph nodes resected, and pathological status. We await follow-up of these data which will compare long-term survival (66).

REVATE is another randomized-controlled trial that is being conducted to specifically analyze whether RAMIE is superior to conventional thoracoscopic MIE in terms of radical lymph node dissection along the left recurrent laryngeal nerve. Primary outcomes of this trial will be measured by unsuccessful lymph node dissection along the left recurrent laryngeal nerve, meaning failure to remove lymph nodes along this nerve or recurrent laryngeal nerve palsy following the lymph node dissection. Secondary endpoint of the trial will include the number of lymph nodes removed along both the right and left recurrent laryngeal nerve, incidence of pneumonia, incidence of other postoperative complication, in-hospital mortality, 30-day mortality, 90-day mortality, R0 resection, blood loss, conversion to open procedure, ICU stay, and QOL metrics. The trial began in 2018 at two high-volume surgical centers in Taiwan and China and is expected to last 8 years (67).

Finally, the ROBOT-2 Trial is ongoing, which is comparing RAMIE to MIE for treatment of resectable esophageal adenocarcinoma in the Western World at high volume centers in Germany, the Netherlands, and Switzerland. The primary endpoint is the extent of lymph node dissection. Secondary outcomes include overall postoperative complications, ICU length of stay, hospital length of stay, in hospital mortality, 30-, 60-, and 90-day mortality, pathology results, overall and disease-free survival at 2, 3, and 5 years, operation time, pain, HRQOL metrics, cost analysis, conversion to open, surgeon fatigue, and postoperative function recovery. This study began recruitment in 2021 and is expected to complete recruitment in 2028 (68).

In summary, there are mixed results in the literature comparing the benefits of RAMIE over MIE. We await the results of active RCTs to better understand these differences. Given the high capital costs associated with robotic surgical systems, future studies should include a more holistic assessment of the healthcare economics of MIE vs. RAMIE, which take into consideration capital costs, disposables, operating room (OR) time, hospital length of stay, and the cost of complications. In addition to HRQOL for patients undergoing MIE vs. RAMIE, future studies should also compare surgeon fatigue and QOL, which is a secondary outcome being assessed in ROBOT-2.

Controversies and future directions

Outside of conventional MIE vs. RAMIE, a number of other technical controversies remain. First, the outcomes of MIRO (Ivor Lewis via a laparoscopic/right thoracotomy vs. a laparotomy/right thoracotomy) approach are intriguing. Extrapolating from the thoracoscopic vs. open lobectomy data, many assumed that that the benefit of MIE was largely derived from avoidance of a thoracotomy. MIRO indicates that this assumption was incorrect. While additional studies are needed to better understand the benefit of hybrid vs. total MIE, these data from MIRO provide evidence that surgeons who do not currently offer MIE/RAMIE can safely transition to a minimally invasive approach, perhaps starting in a staged hybrid fashion in which either the abdominal or thoracic portion of the operation is performed in a minimally invasive fashion rather than trying to tackle a complete MIE/RAMIE. Even a hybrid approach offers benefit over a completely open esophagectomy.

A tubularized gastric conduit is the most frequently used condition for esophageal replacement. Ischemia of the tip of the conduit is a contributing factor to anastomotic leakage. Ischemic preconditioning is a procedure that is performed several weeks prior to esophagectomy during which flow through the left gastric artery, left gastroepiploic artery and splenic arteries is occluded (either by laparoscopic ligation or embolization in interventional radiology, which (theoretically) allows the gastric fundus to more slowly adapt to ischemic conditions and theoretically reduce the risk of anastomotic leakage (69). Several meta-analyses have shown reduction in incidence and/or severity of anastomotic leakage after gastric ischemic preconditioning (70-72). However, a RCT (LOGIC) showed equivalency in perfusion of the gastric conduit tip between groups that received laparoscopic ischemic conditioning, as compared to those who did not (73). Further studies are thus needed to determine the group of patients most likely to benefit from gastric ischemic preconditioning (e.g., smokers).

Bilateral truncal vagotomies are intrinsic to nearly all esophagectomies, rendering patients susceptible to delayed gastric emptying. However, the questions of whether, how, and when to intervene on the pylorus in an attempt to promote emptying, either with a temporary (endoscopic dilatation or onabotulinum toxin) and permanent (pyloromyotomy, pyloroplasty or endoscopic per oral endoscopic pyloromyotomy) intervention has not been addressed by randomized trials.

In the future, technology will augment our ability to perform high quality, minimally invasive esophagectomies. Currently in its infancy, such technology is largely limited to near infrared spectroscopy with indocyanine green (ICG) to assess perfusion of the gastric conduit, to identify the thoracic duct and for lymph node mapping (74-76). The potential, however, is endless. Embedded technology (for robotic platforms) and standalone systems (for conventional MIE) could augment our visualization of tumor margins, identification of lymph node metastases, and enhance our ability to educate practicing surgeons and trainees.

Discussion

In this narrative review, we captured the direction of the art of esophagectomy—towards minimally invasive techniques. Much of the available evidence in support of conventional MIE and RAMIE is limited to single institution observational trials, and, hence, these data have the inherent shortcomings of such studies (primarily bias and confounding) which constrains their ability to draw causal inferences. Nonetheless, the outcomes of a few single- and multi-institutional, randomized clinical trials, the body of the evidence of these observational studies, and the results of meta-analyses of these data support several key findings. First, conventional MIE and RAMIE are both safe and effective. While the learning curve may seem steep (approximately 30 to 50 cases) especially when one’s institution volume may be limited, it should not deter us surgeons from adopting MIE techniques. This learning curve can be surmounted by approaching it in a mindful manner, such as beginning with hybrid approaches, performing parts of the operation with minimally invasive approaches (e.g., lymphadenectomy and gastric mobilization) before converting to an open approach (e.g., for conduit construction or creation of the anastomosis) until one’s level of comfort improves, partnering with other surgeon colleagues, and growing one’s benign minimally invasive esophageal and foregut practice to increase the number of regular repetitions with these techniques.

Second, data from the available evidence from clinical trials indicate that conventional MIE and RAMIE are associated with lower complication rates (especially pneumonia). These data are limited by the significantly higher rates of complications in the control (open) group as compared to historically reported rates of complication reported by seminal studies in the literature. An underperforming control group with high complication rates will magnify the perceived differences with the experimental group (conventional MIE or RAMIE) and hence potentially confound associations. Nonetheless, the sum of the evidence from these clinical trials, observational studies and meta-analyses all suggests that hybrid, conventional MIE and RAMIE are associated with lower complication rates. Importantly, studies have shown that perioperative complications impact long-term survival after esophagectomy. As such, processes (such as minimally invasive techniques) should be adopted that optimize the chance of long-term, QOL survival.

Importantly, conventional MIE and RAMIE do not compromise the technical quality, in terms of anastomotic leakage rates, or oncological quality of the operation, in terms of R0 resection rates, lymph node counts, and survival rates. Regardless of the operation, minimally invasive techniques should not compromise the quality-of-care we surgeons provide—they should only enhance it.

Finally, as compared with open esophagectomy, data from the available clinical trials indicate that conventional MIE and RAMIE are associated with durable QOL benefits that extend to at least 1 to 3 years after esophagectomy. Given the limited survival rates from esophageal cancer and the inherent anatomy altering effects of esophagectomy, optimizing postoperative QOL is of vital importance and deserves greater attention in future studies.

While the available evidence supports minimally invasive over open esophagectomy techniques, further study is need to better understand the benefits of hybrid vs. total MIE as well as between conventional MIE and RAMIE. The latter is especially important given the added cost and limited availability of robotic surgical platforms. Consequently, such studies should focus on both the health care economics of and patient-centered outcomes with RAMIE.

Conclusions

As compared with open esophagectomy, both conventional laparoscopic/thoracoscopic MIE and RAMIE are associated with lower complication rates and durable QOL benefits without compromising the oncological quality of the operation, including lymph node counts, R0 resection rates and survival. Consequently, future studies are needed to better understand the benefits of RAMIE, as compared with MIE, including morbidity, mortality, oncological quality, patient-reported outcomes and surgeon-reported outcomes. Adjunctive technology is in its infancy and will likely play a greater role in enhancing the potential higher quality surgical care in the future.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://vats.amegroups.com/article/view/10.21037/vats-24-22/rc

Peer Review File: Available at https://vats.amegroups.com/article/view/10.21037/vats-24-22/prf

Funding: None.

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://vats.amegroups.com/article/view/10.21037/vats-24-22/coif). S.S.G. is a proctor and speaker for Intuitive Surgical Inc. (Sunnyvale, CA). The other author has no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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