Initial experience of complete portal robotic esophagectomy for esophageal carcinoma in semi-prone position under single-lumen insertion for anaesthesia

Introduction

Esophageal cancer (EC) is the seventh leading cause of cancer-related deaths globally, and esophageal squamous cell carcinoma (ESCC) comprises approximately 90% of all cases (1). Currently, the esophagectomy is still the primary choice to treat EC, which is a complicated surgical procedure that involves excision and reconstruction of the digestive tract (2). Minimally invasive esophagectomy (MIE) has been widely applied in treatment of resectable EC due to fewer complications, faster recovery, and better quality of life than traditional open esophagectomy (3-5). In the early 2000s, robot-assisted MIE (RAMIE) was first applied for the surgical treatment of EC (6,7). Since then, RAMIE has been rapidly developed worldwide, and many studies have demonstrated its safety and feasibility (8-11). Although numerous studies of RAMIE have been reported, there are still no unified surgical approach and technique among surgeons. RAMIE is still a challenging procedure with deep learning curve and further studies are essential to elucidate this technique (12-17).

Herein, we described our initial experience of robotic portal esophagectomy with four arms (RPE-4) with CO₂ insufflation, under single-lumen but not double-lumen insertion for anaesthesia in EC patients, using prospective collected data. Using these data, this study aimed to analyse its safety and feasibility, emphasising its advantage in flatting the learning curve of RAMIE to promote the wide spread of this technology for EC patients. We present this article in accordance with the SUPER reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1410/rc).

Preoperative preparations and requirements

This study was approved by the Institutional Review Board of Sun Yat-sen University Cancer Center (approval number: B2023-596-01), which is a world-class and domestic leading cancer center in China, Affiliated to Sun Yat-sen University as a Tertiary teaching hospital. All procedures performed in this study were in accordance with the Helsinki Declaration (as revised in 2013). Informed consent for our study was waived because the patients’ information was retrospectively collected and the study did not involve any therapy beyond those routinely performed and administered during standard patient care before, during, and after surgery. Early in June 2018, our team led by Dr. Hao-Xian Yang as attending surgeon began to perform robot-assisted thoracic surgeries, and since then, we have been collecting the data to build a database, as described elsewhere (18-20). The inclusion criteria were as follows: (I) patients pathologically diagnosed with EC; (II) clinical stage T1-3, N0-2, and M0 according to the 8th American Joint Committee on Cancer staging system; and (III) patients who underwent RPE-4. All the included patients received robotic McKeown or Ivor-Lewis esophagectomy using Da Vinci Si/Xi system produced by Intuitive Surgical Inc. from the USA. A comprehensive case report form (CRF) was designed for each included case to collect the data perioperatively (18-20). The cost of time for each step of the operation, and other perioperative factors such as blood loss and conversion, were recorded simultaneously during the operation. Operative complications were recorded and classified according to the Clavien-Dindo classification system (21). The cost of a patient was defined as the total expense from admission to discharge of this patient before reimbursement by Medicare, which was retracted from our Hospital Information System. Then, costs were converted to U.S. dollar ($) with a 2023 intermediate exchange rate of the RMB against the U.S. dollar.

Totally 22 patients were included in this study. Their detailed clinicopathological characteristics are listed in Table 1. The mean age of the entire cohort was 62.4±5.4 years, and 77.3% (17/22) of the patients were male. More than half of the patients had never smoked (12/22, 54.5%). Nine cases (40.9%) had comorbidities, including four with hypertension, one with diabetes and hypertension, one with myocardial infarction, one with hepatitis B, one with depression, and one with chronic obstructive pulmonary disease. Most patients received McKeown esophagectomy (20/22, 90.9%). Squamous cell carcinoma was the predominant histological type (19/22, 86.4%), and most patients were diagnosed with pathological stage II (7/22, 31.8%). Three patients (13.6%) received neoadjuvant therapy, in which two of them achieved pathological complete response.

Step-by-step description

General anesthesia method

Single-lumen tracheal tube insertion was performed for anaesthesia with the advantages of not only reducing the complexity of the procedure and the potential injury to the tracheal mucosa, but also facilitating the dissection of the lymph nodes (LNs) along the left recurrent laryngeal nerve (RLN), which was shown in Figure 1. As shown in Figure 1A, the space around the trachea of a patient with single-lumen tracheal tube was exposed easily, but according to Figure 1B, the trachea of a patient was obviously swelled by double-lumen tracheal, hampering the dissection of the LNs along the left RLN. In fact, double-lumen tube is significantly larger than the single-lumen tube, and the comparison of these two types of tubes at the panoramic level and at the cross-section level was shown in Figure 1C,1D, respectively.

Figure 1 Comparison of single-lumen and double-lumen tracheal tubes. (A) Tracheoesophageal groove regions of patient with single-lumen tracheal tube; (B) tracheoesophageal groove regions of patient with double-lumen tracheal tube; (C) comparison of single-lumen and double-lumen tracheal tubes at panoramic level; (D) comparison of single-lumen and double-lumen tracheal tubes at the cross-section level.

Patient position and port location strategy

A 4-arm complete robotic portal technique with a 12-mm assistant port was used for all the included patients. The five portal incisions were sufficiently large to match the sizes of the individual trocars. Each adjacent port was made 8–10 cm apart to avoid obstruction between the instruments.

In terms of patient’s position, the patients were placed in a right-side semi-prone position (30°–45°) for the thoracic procedure, as shown in Figure 2A, and the patients were placed in the supine position for the abdominal procedure (Figure 2B). In terms of port location strategy, the port location for the thoracic procedure is shown in Figure 3A. The camera port (12 mm in Si system and 8 mm in Xi system) was placed in the 5th intercostal space (ICS) along the anterior axillary line, and CO₂ insufflation was set at 6–8 mmHg. The robot’s left arm (8 mm trocar) was placed in the 8th ICS at the posterior axillary line. The robot’s right arm (8 mm trocar) was placed in the 3rd ICS along the mid-axillary line. The robot’s assistant arm (8 mm trocar) was placed in the 10th ICS along the tip of the scapula line. The port for physician assistant (12 mm trocar) was placed in the 7th ICS at the anterior axillary line. The port location for the abdominal procedure is shown in Figure 3B. The camera port was placed at the bottom of the navel, and CO₂ insufflation was performed at 12–14 mmHg. The robot’s left arm was placed 8–10 cm away from the camera port on the left side. The robot’s right arm was placed below the costal arch along the left anterior axillary line. The robot’s assistant arm was placed below the costal arch along the right anterior axillary line. An assistant port was placed between the camera port and robotic right arm.

Figure 2 Patient position for (A) thoracic procedure, (B) abdominal procedure.

Figure 3 Port strategy for (A) thoracic procedure, (B) abdominal procedure. H, side of head; F, side of foot; C, camera; A, assistant port; 1, arm 1 of the robot; 2, arm 2 of the robot; 3, arm 3 of the robot.

Thoracic procedure

When the robot was docked, robot’s assistant arm was used to ventrally push aside the right-side lung to expose the area of posterior mediastinum. We first divided the pleura at the apex of thoracic cavity using permanent cautery hook combined with the Maryland bipolar forceps or ultrasonic scalpel if necessary to expose and dissect the LNs along the right RLN (Figure 4). Then we divide the upper third of the esophagus along the posterior line of it. For advanced cases, we transect the arch of azygous vein for a better exposure. In the next step, we continue to divide the esophagus along the descending aorta. The proper esophageal artery to the esophagus was transected with robotic ultrasonic scalpel (Figure 5). The thoracic duct was exposed or dissected in advanced cases with suspicious of tumor invasion. During this procedure, the para-esophageal LNs were dissected by en bloc method. After a thorough division, the esophagus was transected above the arch of the azygos vein using a stapler (Figure 6). The distant residual of the esophagus was then lifted for a complete division of the esophagus. By this way, the subcarinal zone could be well exposed and enabled us a convenient LN dissection (Figure 7). The last step of thoracic procedure is dissecting the LNs along the left RLN. The single-lumen tracheal tube insertion during anaesthesia enabled the assistant to push the trachea anteriorly using a suction for a better exposure of the LNs along the left RLN (Figure 8). At last, a chest tube was inserted regularly through the camera port.

Figure 4 Use Maryland bipolar forceps (A) and ultrasonic scalpel (B) to dissect right RLN LNs. RLN, recurrent laryngeal nerve; LNs, lymph nodes.

Figure 5 Use the ultrasonic scalpel to transect the proper esophageal artery to the esophagus.

Figure 6 Use a stapler to transect the esophagus above the arch of the azygos vein.

Figure 7 Dissect subcarinal zone lymph nodes.

Figure 8 Exposure of the left recurrent laryngeal nerve.

Abdominal procedure

When the robot was docked, we first divided the omentum ligament using ultrasonic scalpel until to the short gastric artery (Figure 9). With the help of robot’s assistant arm, the liver could be easily lifted to expose the lesser omentum (Figure 10). After division of the lesser omentum, the left gastric artery and veins could be well exposed and divided using hem-o-lok (Figure 11). After clipping and cutting off the left gastric artery and vein, the lesser curvature was completely divided to the hiatus (Figure 12). During this procedure, LNs alongside the left gastric artery, common hepatic artery, celiac trunk, lesser curvature, and cardia were all completely dissected. Once the whole stomach was fully dissociated, a gastric conduit was created using the stapler from the lesser curve to the fundus (Figure 13). Finally, anastomosis was completed in the neck or thorax. Postoperatively, the patient was transported to the intensive care unit (ICU) with nasogastric and nasoduodenal nutrition tubes.

Figure 9 Use the ultrasonic scalpel to divide the omentum ligament.

Figure 10 Use the robotic assistant arm to lift the liver.

Figure 11 Use the hem-o-lok to clamp the left gastric artery.

Figure 12 Divide the lesser curvature completely to the hiatus.

Figure 13 Use the stapler to create a gastric conduit.

Here, we presented two surgical videos of two included patients: One underwent robotic McKeown esophagectomy and the other underwent robotic Ivor-Lewis esophagectomy, which was shown in Video 1 and Video 2, respectively.

Postoperative considerations and tasks

The postoperative management of RPE-4 is like that of MIE or open esophagectomy. After RPE-4, patients were transformed from operative room to ICU, and every patient should stay in ICU for at least one night. Chest X-ray was performed on postoperative day (POD) 1 to determine if pulmonary complications occurred. Dual antibiotics were routinely used to control postoperative infections. Gastrointestinal decompression was routinely performed using a nasogastric tube, and the nasogastric tube should be removed before discharge. Total parenteral nutrition (TPN) was performed for 3–5 days after surgery. Then with the increasing amount of enteral nutrition, the amount of TPN could be gradually reduced until no need of TPN, but the nasoduodenal nutrition tube should be kept for at least 2 weeks because patients should keep fasting for at least 2 weeks to avoid anastomotic fistula. Before removing the nasoduodenal nutrition tube, patient should routinely receive an esophageal barium swallow to confirm that no anastomotic fistula occurred. All included patients were followed every 2 weeks using telephone or outpatient follow-up until 90 days after surgeries.

Tips and pearls

In the surgical treatment of EC, complete portal robotic esophagectomy with 4 arms under single-lumen tracheal tube insertion in semi-prone position has advantages in dissection of LNs alongside the left RLN, in reduction of the damage of tracheal mucosa caused by tracheal intubation, in simplifying surgical procedures and flatting the learning curve.

Discussion

With flexible robotic arms and a high-definition three-dimensional view, the robot-assisted surgical system can overcome the inherent defects of traditional endoscopic surgery. Therefore, an increasing number of thoracic surgeons worldwide have adopted RAMIE as a safe and efficient surgical technique (8-11). However, the surgical procedures of esophagectomy are extremely complex, and there is currently no unified standard surgical technique for RAMIE. Therefore, thoracic surgeons from different medical centers should compile their RAMIE surgical techniques to further advance and broaden the application of this method.

In this study, perioperative factors of patients with RPE-4 were summarized in Table 2. All the patients completed RPE-4s successfully, and none of them experienced perioperative death. The median total operative time was 325.0 min [interquartile range (IQR), 296.3–391.3 min], and the median thoracic docking and console time were 7.5 (IQR, 5.0–10.0) and 79.0 (IQR, 65.3–102.3) min, respectively. The median abdominal docking and console time were 7.0 (IQR, 5.0–9.3) and 84.5 (IQR, 67.0–118.8) min, respectively. Besides, the median time of switching patients’ position was 56.0 (IQR, 49.0–60.3) min. The median estimated blood loss during surgery was 100.0 (IQR, 100.0–125.0) mL. The median number of harvested LNs was 28.0 (IQR, 21.3–45.3), and the median length of postoperative stay was 9.0 (IQR, 6.8–12.5) days. The mean number of harvested RLN LNs was 3.6 (median: 2.0), and the achievement rates of the dissection of RLN LNs was 90.9% (20/22). There were no intraoperative complications and conversion to open surgery. Four patients experienced postoperative complications. Patient A had anastomotic fistula on POD 7, then we opened the cervical incision and created a negative pressure suction device. After 20 days, the anastomotic fistula was cured. Patient B had right-side pneumothorax on POD 4, then a closed thoracic drainage was performed, and the pneumothorax disappeared next day. Patient C had left-side pleural effusion on POD 1, then ultrasound-guided thoracentesis was performed and a drainage tube was placed. Finally, the drainage tube was removed on POD 4. Patient D had respiratory failure on POD 1, then the patient was transferred to ICU. After 8 days of symptomatic treatment, patient D was successfully transferred out of ICU. All these four patients were cured and discharged from hospital successfully. No RLN palsy occurred. The median total cost during hospitalization was $20,997.8 (IQR, 18,921.1–24,511.6). According to our results, we demonstrated our experience of RPE-4 with single-lumen anesthesia and CO₂ insufflation was a safe and effective surgical technique, which could also flatten the learning curve of RAMIE.

Reasonable patient positioning is an important factor for safe and smooth operative progress. The patient position for RAMIE is similar to that of traditional MIE, which mainly includes the left lateral (22-24) and prone positions (13) for the thoracic procedure. In early 2010, Kim et al. proposed RAMIE in the prone position, and their results showed that this technique is technically feasible and safe (13). The patient was placed in a prone position to facilitate mediastinal dissection and minimize lung injury (25). However, Kim et al. also found that the prone position could cause an elevation in central venous pressure and mean pulmonary arterial pressure and a decrease in static lung compliance (13). In addition, prone position is not convenient for conversion to thoracotomy when necessary. Therefore, most thoracic surgeons are more likely to choose the left lateral position as the standard patient position for RAMIE. After comparing the advantages and disadvantages of these two patient positions, we propose the semi-prone position to complete RPE-4. In this position, gravity is used to naturally move the right lung to the ventral side, thereby fully exposing the esophageal region of the posterior mediastinum with the help of assistant arm of Da Vinci System, which was shown in Figure 1A,1B. Additionally, this position does not cause excessive pressure on the heart and lungs and does not damage the patient’s cardiopulmonary function. Even if operative complication occurs, it’s convenient to transfer to open thoracotomy. Based on our study, all 22 patients receiving RAMIE with semi-prone position had satisfactory short-term outcomes. Therefore, we propose that semi-prone position is a good position for RAMIE, but randomized controlled trial (RCT) is essential to compare different positions for operation to draw a definite conclusion.

Regarding the anesthesia intubation method, both double-lumen and single-lumen insertion for anaesthesia have extensive applications in RAMIE, but there is still no definitive conclusion on which of the two techniques is better currently. The advantage of double-lumen tracheal tube is to collapse the lung on the side of surgery to provide a capacious surgical field, and to effectively prevent the secretions and blood of the affected lung from contaminating the healthy lung. However, the double-lumen tracheal tube is larger in diameter than the single-lumen tracheal tube, which could cause greater damage to the patient’s tracheal mucosa, leading to cough and lung infection after surgery. Besides, double-lumen tracheal tube insertion is a more challenging technique, which is time-consuming and energy-draining. An additional benefit of single-lumen tracheal tube insertion is cost savings for patients. In our hospital, one double-lumen tracheal tube costs $300 more than one single-lumen tracheal tube. In mainland China, the total cost of esophagectomy is only about $1,000, and mainland China accounts for more than half of the world’s EC patients. Therefore, saving $300 per patient is not a small amount. More importantly, single-lumen tracheal tube insertion however, is easy to complete for anaesthesiologists and is beneficial for exposing the tracheoesophageal groove region and protecting intraoperative lung function (25,26). With the assistance of low tidal volume and artificial pneumothorax, the surgical field of view was not significantly restricted (as shown in our videos), and the surgical procedure remained smooth. Based on our results, the mean number of harvested RLN LNs was 3.6, and the achievement rate of the dissection of RLN LNs was 90.9%, indicating the feasibility and efficiency of our surgical technique. Of course, RCT is essential to compare single-lumen insertion and double-lumen insertion for anesthesia in RAMIE.

In terms of short-term outcomes, it should be noted that the number of resected LNs in our study (mean: 33.6) was much more than those of ROBOT trial (mean: 27) (27) and RAMIE trial (mean: 23) (8). Regarding the perioperative complications, the overall complication rate was lower in our study (18.2%) compared with ROBOT trial (59%) (27) and RAMIE trial (48.6%) (8). More importantly, there was only one patient having anastomotic fistula and no one had hoarseness after surgery. Although the patients included in our study were the first 22 cases treated by RPE-4, but the number of examined LNs in our study was more than those of ROBOT trial and RAMIE trial with acceptable operative time. More harvested LNs in this study but no patient having hoarseness after surgery suggests that our technique could not only guarantee the completeness of surgery, but might also reduce the surgical complications, especially for the protection of RLN. It is worth noting that although there were only 22 cases included in this study, during the study period, our surgical team also performed robotic lobectomies (18), robotic segmentectomies (20), and robotic mediastinal tumor resection (28). Additionally, in clinical practice, whether three-port or four-port RAMIE is adopted depends on several factors, including the surgeon’s technical expertise, as well as the economic conditions of the region. For instance, in mainland China, RAMIE is not yet covered by medical insurance. To economize costs, many surgeons from mainland China choose to use three robotic arms instead of four, supplemented by an additional incision of approximately 3–4 cm to facilitate the smooth progression of the surgery (15,29).

There are some limitations in this study. First, this was a single-arm study that only included 22 patients with RPE-4, and whether this technique was superior to conventional MIEs or other types of RAMIEs needs further investigation. Second, all included RPE-4s were performed by an experienced team in MIE in large volume cancer center, and the results might differ from those of other surgical teams. Third, this study only explored the short-term outcomes of RPE-4, and the long-term outcomes of this technique need to be further investigated.

Conclusions

In conclusion, this study demonstrated that RPE-4 under single-lumen tracheal tube insertion, CO₂ insufflation, and semi-prone position for thoracic procedure is a safe and effective technique for MIE in EC patients. It has advantages in LN dissection, reducing complications, and flattening the learning curve with satisfied short-term outcomes. Further prospective comparative trials are warranted to testify our results.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the SUPER reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1410/rc

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1410/prf

Funding: This work was supported in part by Sun Yat-sen University Clinical Research 5010 Program (No. 2019012 RAVAR trial), and the Excellent Surgery Study Project of Bethune Charitable Foundation (No. CESS2021LB15 LOFTY trial).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1410/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. This study was approved by the Institutional Review Board of Sun Yat-sen University Cancer Center (approval number: B2023-596-01). All procedures performed in this study were in accordance with the Helsinki Declaration (as revised in 2013). Informed consent for our study was waived because the patients’ information was retrospectively collected and the study did not involve any therapy beyond those routinely performed and administered during standard patient care before, during, and after surgery.

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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