Robotic-assisted minimally invasive esophagectomy—technical considerations and outcomes

Introduction

Esophageal cancer is recognized as the seventh most common cancer and sixth deadliest cancer worldwide (1,2). The standard curative treatment approach for resectable cases involves a radical esophagectomy and extended lymphadenectomy—a technically demanding procedure associated with high morbidity and mortality rates (3,4). Since the pioneering esophagectomy performed for intrathoracic esophageal cancer in 1913, significant advancements have occurred in both technique and approach (5).

Historically, open esophagectomy (OE), which usually involves a thoracotomy and laparotomy, was the standard approach until the advent of minimally invasive esophagectomy (MIE) in 1992 (6). This shift was marked by a hybrid approach that combined thoracoscopic and laparoscopic techniques, as seen in the MIRO trial. This randomized control trial highlighted a reduction in major complications with the hybrid approach compared to OE, though it also brought to light concerns about the high rates of pulmonary complication linked to thoracotomy (7).

By 2011, the pivotal TIME trial established the superiority of a total MIE over OE by comparing multiple perioperative parameters (8). This trial, employing the McKeown procedure, demonstrated that MIE could reduce postoperative pulmonary infections, operative blood loss, postoperative pain scores, and hospital length of stay, while improving overall quality of life. Importantly, MIE achieved these benefits while maintaining equivalent long-term oncologic outcomes (8). Subsequent systematic reviews have reaffirmed these findings, solidifying MIE as a preferred approach in many centers (9,10). However, concerns emerged regarding the safety of MIE, citing higher rates of reinterventions compared to OE (11-15). Additionally, MIE is not without its challenges, including limited instrument movement that decreases surgical dexterity and a steep learning curve that necessitates a high volume of cases to achieve proficiency (1,16).

In response to the limitations and technical challenges associated with conventional MIE, robotic-assisted MIE (RAMIE) was introduced in 2004 with further developments documented in a 2006 case series (17,18). RAMIE employs state-of-the-art robotic systems that offer articulated instruments with seven degrees of freedom, tremor-filtering, and enhanced magnification (19). The introduction of RAMIE has marked a significant shift in surgical practice, with a notable increase in the number of esophagectomies performed robotically between 2009 and 2016 (20).

This review seeks to comprehensively analyze the existing literature on RAMIE, comparing it with traditional MIE and OE approaches. We will explore the various techniques within RAMIE and assess how its outcomes measure up against those of OE and MIE. It underscores the necessity for thoracic surgeons to remain well-versed in the latest developments within the field of robotic esophagectomy to enhance patient outcomes and adapt to the evolving landscape of surgical techniques.

RAMIE technical considerations

Approach

RAMIE, encompassing both transhiatal and transthoracic approaches, has seen varying adoption rates across different regions influenced by histologic subtypes of cancer, patient conditions, and surgeon preference. The McKeown approach, prevalent in Asia, places emphasis on cervical lymph node dissection, aligning with the typical location of esophageal squamous cell carcinoma (SCC) in the proximal or mid-esophagus (21,22). Conversely, the Ivor-Lewis or transhiatal approach are predominately utilized in America and Europe where adenocarcinoma in the lower esophagus is more common (23,24). The first transhiatal robotic-assisted esophagectomy was reported by Horgan et al. in 2003 (25) and has since remained a promising approach for esophagectomy. This technique is noted for its shorter learning curves and comparable operative times, mortality rates, blood loss, and lengths of hospital stay (26).

Additionally, the application of robotics in esophagectomy varies widely. In the McKeown approach, some surgeons only use the robot during the thoracic phase, while others extend its use to the abdominal phase as well. For the Ivor-Lewis approach, there are significant technical challenges associated with performing the intrathoracic esophagogastrostomy with conventional MIE. However, robotic assistance can facilitate this complex intrathoracic anastomosis, making fully or partially robotic-assisted Ivor-Lewis procedures increasingly more common (27).

Patient positioning

When planning patient positioning for each RAMIE approach, it is crucial to tailor positioning to the specific phases of the procedure to optimize surgical access and maneuverability. For an Ivor-Lewis RAMIE, the patient is positioned supine during the abdominal phase and shifts to a left lateral decubitus position for the thoracic phase. In contrast, a McKeown RAMIE involves the patient remaining supine during both the cervical and abdominal phases, while starting with the left lateral decubitus position for the thoracic phase. Notably, while thoracoscopic MIE approaches are typically performed in the left lateral decubitus position, Otsubo et al. have reported improved postoperative oxygenation when the thoracic phase is conducted with the patient in a supine position (28). Meanwhile, in a transhiatal RAMIE, the patient remains in a supine position throughout both the abdominal and cervical phases. This strategic positioning facilitates optimal access and maneuverability during each distinct phase of the RAMIE procedures.

Anastomosis

Anastomotic leakage stands out as the most critical and life-threatening complication post-esophagectomy, and surgeons have continually sought to address this problem by investigating various techniques over the years. When opting for a cervical anastomosis, as seen with McKeown and transhiatal esophagectomy, the procedure typically involves a left cervical incision, which remains consistent across both open and minimally invasive approaches (1). However, performing an intrathoracic anastomosis, characteristic of Ivor-Lewis esophagectomy, can pose technical challenges, particularly with conventional thoracoscopic MIE methods due to rigid instruments and limited thoracic mobility (1). With RAMIE, articulated instruments allow for a broader range of motion within the osseous thorax. While a circular stapled anastomosis is the standard technique in thoracoscopic approaches, RAMIE also offers the versatility of a hand-sewn anastomosis (29).

When comparing the various robotic esophagectomy anastomotic techniques, it is essential to acknowledge that whether employing circular stapled, linear stapled, or handsewn methods, each technique strives to achieve a tension-free, well-vascularized, patent anastomosis with adequate tumor resection margins. The circular stapled technique, known for its straightforward and reproducible approach, involves placing an anvil within the esophagus and using the circular stapler within the conduit. This technique typically reports anastomotic leak rates between 5% and 10% (30-33) and stricture rates, while infrequently reported, have reached as high as 19% (33), with postoperative dysphagia occurring around 17% (34). The linear-stapled, or hybrid, technique, requires aligning the esophagus and conduit side-to-side, then using a linear stapler to create a common channel. The final closure of the common defect is performed by hand. This technique shows anastomotic leak rates ranging from 4% to 8% and stricture rates between 6% and 16% (34-37). Lastly, the handsewn technique, which is the most time-consuming, involves the surgeon hand sewing the anastomosis entirely using the robotic console. Leak rates for this technique have been reported from 0% to 30%, with stricture rates largely unreported (38-41).

Lymphadenectomy

Finally, in terms of overall survival, the thoroughness of lymphadenectomy during esophagectomy holds paramount importance. A lymph node harvest of a minimum of 15 nodes correlates with enhanced overall survival rates (42). RAMIE facilitates meticulous lymph node dissection, particularly in complex regions previously subjected to irradiation, ensuring comprehensive treatment (32). Some investigations suggest RAMIE yields an increased lymph node harvest compared to conventional MIE, particularly in Asia, where consistent data supports a more thorough mediastinal lymph node dissection (43,44). Despite variations in findings, an overwhelming majority of consensus experts agree on RAMIE’s potential superiority over MIE in terms of extensive mediastinal lymphadenectomy (45).

Total mesoesophagus excision (TME)

A TME is a technique derived from rectal cancer surgery that has been advocated for by Japanese surgeons as the optimal resection approach for esophagectomy, emphasizing its potential to maximize en bloc excision by leveraging the anatomical space surrounding the esophagus (45). Identifying the mesoesophagus can pose a challenge with the conventional MIE approach, particularly in cases where patients have undergone neoadjuvant radiotherapy. However, the improved visual field provided by robotic technology facilitates the TME technique, making it more feasible. However, the adoption of TME remains predominantly within Asian surgical practices, with ongoing debates surrounding its efficacy in increasing lymph node excision and reducing mediastinal lymph node recurrence rates (46).

Thoracic duct resection

Similarly, the routine resection of the thoracic duct during RAMIE remains controversial due to associated postoperative complications, such as chylothorax, long-term immune alterations, hemodynamic shifts, and changes in nutrient absorption, though it may potentially remove a source of metastatic tumor cells or future lymph node metastatic sites (47-49). By employing the RAMIE approach, the thoracic duct can be precisely identified and resected with the 10-fold magnification and stable three-dimensional view that the robotic platform allows (50).

Outcomes of robotic esophagectomy

RAMIE is predominantly utilized in patients with esophageal cancer, and its efficacy has been evaluated through prospective randomized controlled trials (RCTs) (51,52) as well as numerous meta-analyses and retrospective studies (53,54). These studies have compared RAMIE’s operative, postoperative, and oncologic outcomes with those of OE and MIE.

Intraoperative blood loss

Studies consistently show that RAMIE results in lower intraoperative blood loss compared to OE (55,56). When comparing RAMIE with MIE, the findings are mixed in comparison—some studies report similar amounts of blood loss (51,57-61), while others indicate it is lower in RAMIE (62-64).

Anastomotic leak

Comparative studies using the McKeown and Ivor-Lewis techniques reveal that RAMIE and MIE show comparable anastomotic leak rates, with no significant differences observed across multiple studies (65-69). Similarly, when comparing RAMIE to OE, the research indicates that there are no significant differences in anastomotic leak rates between these surgical approaches (52,70-75).

Lymph node harvest

When evaluating the capacity for a larger lymph node harvest, the findings from various studies present a complex yet insightful picture. Propensity-matched studies have consistently shown superior lymph node yields with RAMIE, as evidenced by two extensive reports (22,76). However, this outcome is contrasted by another matched study which found a more effective lymph node harvest with MIE as compared to RAMIE (31). Further analysis through a RCT supports the efficacy of RAMIE, demonstrating a more favorable lymph node harvest with this technique (77).

Comparative assessments between RAMIE and traditional OE reveal mixed outcomes. While one RCT reported no significant differences in lymph node harvest between the two techniques (31), three additional observational studies observed a greater lymph node yield with RAMIE compared to OE (72,73,76).

A particularly notable finding emerges when considering patients who received neoadjuvant therapy. In this specific subset, those who underwent RAMIE harvested significantly more lymph nodes than those who underwent MIE, despite there being no significant differences in the total number of lymph nodes harvested across the entire study population (21,31,78). This highlights RAMIE’s potential in achieving a more thorough lymph node dissection, enhancing its role in the treatment of esophageal cancer.

Oncologic outcomes

A RCT with a follow-up median of 21 months indicated that the cancer recurrence rates for RAMIE and VAMIE were 14.9% and 25.5%, respectively, although these differences were not statistically significant (77). Furthermore, an observational study echoed these findings, showing no significant differences in overall recurrence rates, with RAMIE at 11.8% and VAMIE at 10.2%. Locoregional recurrence rates were also similar between the two methods (RAMIE 3.5%, VAMIE 3.9%), despite RAMIE having a longer median follow-up time of 17.2 months compared to 9.3 months for VAMIE (69). Additionally, one RCT and an observational study found no difference in either locoregional or distant recurrence between RAMIE and OE (52,75).

Operative time

Operative times for RAMIE tend to be longer when compared to OE (55,56) and MIE (57,62,63) in several studies. However, results from the RAMIE trial, a randomized control trial comparing MIE and RAMIE, suggest a shorter operative time with RAMIE compared to previous findings, attributed to more efficient docking processes and the advanced capabilities of wristed robotic instruments and 3D visualization (51). Notably, while one randomized control trial by van der Sluis et al. reported a longer operative time for RAMIE compared to OE (349 vs. 296 minutes) (52), additional observational studies did not report any statistical difference between the two techniques (66,71,74).

Cost

The robotic platform, while initially expensive to acquire and maintain, shows promise in reducing overall healthcare costs. Early data suggest that while the cost per procedure is higher for RAMIE, the total expenses—including those associated with treating complications—may be lower due to fewer complications (52,79). Furthermore, the potential integration of artificial intelligence and future technological advancements could significantly enhance the effectiveness and cost-efficiency of robotic surgeries.

Learning curve

Chan et al. conducted a recent systematic review that analyzed a substantial body of research addressing the learning curves associated with various esophagectomy techniques. Their findings indicate that mastering a total MIE approach typically requires approximately 69 cases. In contrast, the learning curve for a total RAMIE approach is notably shorter, with an estimated 36 cases needed for proficiency. It is important to note that some surgeons’ prior experience with the MIE technique, years of experience as a thoracic faculty, as well as familiarity with the robotic platform from performing other robotic-assisted thoracic cases could potentially contribute to the reduced number of cases required to overcome the learning curve for RAMIE (16).

Conclusions

In conclusion, RAMIE has established itself as a robust and effective approach for treating esophageal cancer. By harnessing advanced robotic technology, RAMIE addresses the limitations often encountered with conventional MIE, such as restricted instrument mobility and a challenging learning curve. Since its introduction, RAMIE has not only captured the attention of the surgical community but has also demonstrated its capability to enhance perioperative outcomes and oncologic efficacy.

The accumulated evidence robustly positions RAMIE as a superior alternative to traditional esophagectomy methods, particularly for esophageal cancer treatment. With its demonstrated potential to improve surgical precision and patient recovery, RAMIE is shaping the future of minimally invasive esophageal surgery, making advanced surgical techniques more accessible and effective for a wider range of patients.

Acknowledgments

Funding: None.

Footnote

Peer Review File: Available at https://aoe.amegroups.com/article/view/10.21037/aoe-24-18/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://aoe.amegroups.org/article/view/10.21037/aoe-24-18/coif). The authors have 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.

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