Esophageal cancer is one of the most common digestive tract cancers in the world (1). According to the Cancer Statistics in China, esophageal cancer ranks fourth in the incidence of malignant tumors (2). Most of the patients are in advanced stage at the time of diagnosis, and surgery is the cornerstone of the treatment for esophageal cancer (3). Open esophagectomy is usually accompanied by numerous complications and a high mortality rate (4,5). The presence of minimally invasive esophagectomy (MIE) significantly improved perioperative outcomes, without the compromise of long-term survival (6-8).
In the past two decades, robot-assisted thoracic surgery has been increasingly applied in clinical practice. Compared with video-assisted thoracoscopic surgery, robotic system provides a three-dimensional, higher definition view, and better dexterity in operation (9). The procedure of robot-assisted Ivor-Lewis Esophagectomy (RAILE) is a robotic esophageal cancer resection via right chest approach based on the technique of open and thoracoscopic Ivor-Lewis esophagectomy, which has the potential advantages in reducing postoperative complications (10) and performing intrathoracic hand-sewn anastomosis (11). The safety and technique feasibility of RAILE has been demonstrated by several studies (12-14). Here, we perform a literature review of published studies regarding the surgical outcomes of RAILE in different centers.
RAILE begins with abdominal phase and patient is in the supine reverse Trendelenburg position. Four-arm approach is used in our center: a camera port is positioned in the subumbilical site, three robotic ports are placed in the right and left subcostal regions, with one assistant port placed on the left midclavicular line. After the gastric artery is transected, a complete celiac lymphadenectomy is performed. Then the stomach is fully mobilized with the gastroepiploic arcade and the right gastroepiploic vessels preserved. The gastric conduit is then created by assistant with several fires of stapler. A jejunostomy is usually performed during abdominal phase for enteral nutrition support postoperatively in our department.
For the thoracic phase, the patient is positioned in the left lateral decubitus position, and one-lung ventilation is provided. Five ports are placed in the following position: a robotic camera trocar (12 mm) in the 5th intercostal space (ICS) on the anterior axillary line. The right robotic trocar (8 mm) was in the 8th ICS and the left robotic trocar (8 mm) was in the 3th ICS anterior to the scapular rim, an 8-mm port in the tenth ICS posteriorly to the posterior axillary line for the third robotic arm, and a 12-mm assistant’s port in the 7th ICS near the costal margin. Thoracic phase usually begins with the lymph nodes dissection along right recurrent laryngeal nerve (RLN). The azygos vein is then divided by a stapler. The esophagus is then totally mobilized down to the gastroesophageal junction with dissection of all surrounding lymph nodes, including subcarinal areas, periaortic and periesophageal areas, as well as the lymph nodes along the left RLN. After the proximal esophagus is transected, intrathoracic anastomosis will be performed. For the digestive reconstruction, both stapled and hand-sewn intrathoracic anastomosis have been demonstrated as safe and technically feasible approaches (9).
The mean operation times of RAILE are variant among different institutions (12,15-19), range from 303 to 661 min. Generally, the average operation time of RAILE was significantly longer than thoracoscopic-assisted Ivor Lewis esophagectomy (TAILE). According to the reported of Nora et al. (20), the mean operation time of RAILE was 409 minutes, which was longer than thoracoscopic procedure (299 min, P=0.001). A comparative study in our center (17) also showed that the mean operation time of RAILE was significantly longer than TAILE (303 vs. 277 min, P=0.001).The reason for this mainly due to the additional installation time required for robotic surgery. Therefore, many centers performed laparoscopic combined with robotic surgery to shorten the operation time (13,21).
Meredith et al. (22) found that the blood loss in RAILE group was less than that in TAILE group (155±107 vs. 189±188 mL, P=0.03), by using a prospective database. However, according to the cases series in our center (17), no significant difference was found between RAILE and TAILE with respect to blood loss (200 vs. 200 mL, P=0.100).
The conversion rate of RAILE was relative low according to current literature (15,19,23), range from 0 to 4%. In a retrospective study including 61 cases in our center, only 1 case was converted to open (18).
Short term outcomes
In ROBOT trial, van der Sluis et al. (24) demonstrated that three stage robot-assisted minimally invasive esophagectomy (RAMIE) associated with better short-term outcomes in terms of intraoperative blood loss, postoperative complications, quality of life and postoperative pain compared to open esophagectomy. With numerous evidence supported three-stage RAMIE, it can be regarded as a good alternative to both open and thoracoscopic esophagectomy.
For the application of two stage RAMIE, several case series have demonstrated the surgical efficacy recently (20,21). de la Fuente et al. (21) reported an initial experience with 50 patients underwent RAILE: 14 patients (28%) had postoperative complications, including 5 (10%) with pneumonia and 1 (2%) with anastomotic leakage. In another retrospective study (20), which included 144 cases of RAILE, demonstrated that the incidence of postoperative complications was 23.6% (34 cases), with cardiac arrhythmias occurred most frequently (17.4%), and the incidence of anastomotic leakage was 2.8%. For the occurrence of anastomotic leakage, some studies suggested that it is related to anastomosis methods (25-29). Harustiak et al. (30) demonstrated that hand-sewn anastomosis appears to have a higher incidence of anastomotic leakage, compared to staple anastomosis (20.9% vs. 10.0%; P=0.002). Another retrospective study conducted in Japan also yielded similar results (31). However, a retrospective study conducted by Zhang et al. (18) in our department didn’t find any difference of anastomotic leakage between two anastomosis approaches. The incidence of anastomotic leakage was 11.4% when using staple, while the rate of anastomotic leakage was 7.7% in hand-sewn group (P=0.960).
RLN is frequently and easily damaged when performing lymph nodes dissection, and causing paresis or palsy of the vocal cords, which seriously damaging patients’ quality of life (32). According to current studies, the incidence of RLN injury in MIILE, is 0 to 13.6% (7,33-35). Suda et al. (36) demonstrated the incidence of vocal cord paralysis (P=0.018) and hoarseness (P=0.015) can be reduced when using robot assistant, compared to control group. In our department, the incidence of vocal cord paralysis was 8.2% in a case series of RAILE (18).
According to the repot of Biere et al. (7), the median length of hospital stay was 11 days, and the mortality rate at 30 days was 2%. A propensity score-matched study (17) conducted by Zhang and colleagues showed that the length of hospital stay in the RAILE group was similar to TAILE group (9 vs. 9 d, P=0.517), and 30-day and in-hospital mortality is 0. What’s more, a propensity-matched study conducted by Tagkalos et al. (14) demonstrated that ICU stay was shorter in the patient who underwent RAILE, compared to patient underwent TAILE (1 vs. 2 d, P=0.029).
As a relatively new technology, data on the oncological outcomes of RAILE has always been the focus of attention. A lot of studies confirmed that a high lymph node yield significantly improve survival after esophagectomy (37-39). The ROBOT trial showed that the mean number of lymph nodes dissection was similar between three stage RAMIE and OTE (27 vs. 25, no significantly different) (24).
RAILE also can retrieve adequate lymph nodes according to previous studies, with a satisfactory radical resection (R0 resection) rate. A study (19) including 23 case of RAILE showed that RAMIE had a R0 resection rate of 96% (24/25), and the mean number of harvested lymph nodes was 26. Furthermore, Meredith et al. (22) demonstrated that RAILE can obtain better R0 resection rate and more harvest LN, compared to TAILE group (TAILE 93.5% vs. RAILE 100%, P=0.01; LN: TAILE 14±7 vs. RAILE 20±9, P<0.001).
The dissection of the paratracheal lymph nodes has a high therapeutic value for long-term survival, especially for patients with mid- to distal esophageal tumors (40). However, there are important structures nearby paratracheal lymph nodes, such as the superior vena cava and RLN. Severe bleeding and vocal cord paralysis will appear, when these structures were damaged (10). The advantages of robotic surgery might enable a meticulous and safe lymphadenectomy in paratracheal regions.
Horgan et al. (41) reported the completion of the world’s first RAMIE in 2003. The development time of RAILE is even later, so few studies report the long-term survival data on patients. Weksler et al. (6) compared overall survival of patients underwent RAMIE, MIE, and OTE. No significant differences in survival were revealed, with a median survival of 48 months after RAMIE, 49 months after MIE, and 44 months after OTE (P=0.53).
Based on current evidence, RAILE is safe and technique feasible for the management of operable esophageal cancer. In terms of bleeding loss, rate of conversion, number of dissected lymph nodes, hospital stay, postoperative morbidity and mortality, RAILE has acceptable surgical outcomes. However, due to the short development of RAILE, long-term survival data is still lacking. What’s more, high quality evidence is urgently needed to investigate whether RAILE can be considered as an alternative minimally invasive method for TAILE or open Ivor Lewis esophagectomy for the treatment of middle or distal esophageal cancer.
Funding: This work was supported by the Science and Technology Commission of Shanghai Municipality Medical Guidance Science & Technology Support Project (16411966100), the Shanghai Municipal Education Commission-Gaofeng Clinical Medicine Grant Support (20172005), and the Shanghai Municipal Commission of Health and Family Planning Outstanding Academic Leaders Training Program (2017BR055).
Conflicts of Interest: 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.
- Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68:394-424. [Crossref] [PubMed]
- Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin 2016;66:115-32. [Crossref] [PubMed]
- Ajani JA, D'Amico TA, Bentrem DJ, et al. Esophageal and Esophagogastric Junction Cancers, Version 2.2019, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw 2019;17:855-83. [Crossref] [PubMed]
- Takahashi C, Shridhar R, Huston J, et al. Esophagectomy from then to now. J Gastrointest Oncol 2018;9:903-9. [Crossref] [PubMed]
- Yerokun BA, Sun Z, Yang CFJ, et al. Minimally Invasive Versus Open Esophagectomy for Esophageal Cancer: A Population-Based Analysis. Ann Thorac Surg 2016;102:416-23. [Crossref] [PubMed]
- Weksler B, Sullivan JL. Survival After Esophagectomy: A Propensity-Matched Study of Different Surgical Approaches. Ann Thorac Surg 2017;104:1138-46. [Crossref] [PubMed]
- Biere SSAY, van Berge Henegouwen MI, Maas KW, et al. Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet 2012;379:1887-92. [Crossref] [PubMed]
- Wang H, Shen Y, Feng M, et al. Outcomes, quality of life, and survival after esophagectomy for squamous cell carcinoma: A propensity score-matched comparison of operative approaches. J Thorac Cardiovasc Surg 2015;149:1006-14; discussion 1014-5.e4.
- Okusanya OT, Hess NR, Luketich JD, et al. Technique of robotic assisted minimally invasive esophagectomy (RAMIE). J Vis Surg 2017;3:116. [Crossref] [PubMed]
- Kingma BF, de Maat MFG, van der Horst S, et al. Robot-assisted minimally invasive esophagectomy (RAMIE) improves perioperative outcomes: a review. J Thorac Dis 2019;11:S735-42. [Crossref] [PubMed]
- Jin R, Xiang J, Han D, et al. Robot-assisted Ivor-Lewis esophagectomy with intrathoracic robot-sewn anastomosis. J Thorac Dis 2017;9:E990-3. [Crossref] [PubMed]
- Meredith K, Huston J, Andacoglu O, et al. Safety and feasibility of robotic-assisted Ivor-Lewis esophagectomy. Dis Esophagus 2018;31. [Crossref] [PubMed]
- Hodari A, Park KU, Lace B, et al. Robot-Assisted Minimally Invasive Ivor Lewis Esophagectomy With Real-Time Perfusion Assessment. Ann Thorac Surg 2015;100:947-52. [Crossref] [PubMed]
- Tagkalos E, Goense L, Hoppe-Lotichius M, et al. Robot-assisted minimally invasive esophagectomy (RAMIE) compared to conventional minimally invasive esophagectomy (MIE) for esophageal cancer: a propensity-matched analysis. Dis Esophagus 2019. [Epub ahead of print]. [Crossref] [PubMed]
- Meredith K, Blinn P, Maramara T, et al. Comparative outcomes of minimally invasive and robotic-assisted esophagectomy. Surg Endosc 2019. [Epub ahead of print]. [Crossref] [PubMed]
- Bongiolatti S, Annecchiarico M, Di Marino M, et al. Robot-sewn Ivor-Lewis anastomosis: preliminary experience and technical details. Int J Med Robot 2016;12:421-6. [Crossref] [PubMed]
- Zhang Y, Han Y, Gan Q, et al. Early Outcomes of Robot-Assisted Versus Thoracoscopic-Assisted Ivor Lewis Esophagectomy for Esophageal Cancer: A Propensity Score-Matched Study. Ann Surg Oncol 2019;26:1284-91. [Crossref] [PubMed]
- Zhang Y, Xiang J, Han Y, et al. Initial experience of robot-assisted Ivor-Lewis esophagectomy: 61 consecutive cases from a single Chinese institution. Dis Esophagus 2018;31. [Crossref] [PubMed]
- Okusanya OT, Sarkaria IS, Hess NR, et al. Robotic assisted minimally invasive esophagectomy (RAMIE): the University of Pittsburgh Medical Center initial experience. Ann Cardiothorac Surg 2017;6:179-85. [Crossref] [PubMed]
- Nora I, Shridhar R, Meredith K. Robotic-assisted Ivor Lewis esophagectomy: technique and early outcomes. Robot Surg 2017;4:93-100. [Crossref] [PubMed]
- de la Fuente SG, Weber J, Hoffe SE, et al. Initial experience from a large referral center with robotic-assisted Ivor Lewis esophagogastrectomy for oncologic purposes. Surg Endosc 2013;27:3339-47. [Crossref] [PubMed]
- Meredith KL, Maramara T, Blinn P, et al. Comparative Perioperative Outcomes by Esophagectomy Surgical Technique. J Gastrointest Surg 2019. [Epub ahead of print]. [Crossref] [PubMed]
- Shridhar R, Abbott AM, Doepker M, et al. Perioperative outcomes associated with robotic Ivor Lewis esophagectomy in patient's undergoing neoadjuvant chemoradiotherapy. J Gastrointest Oncol 2016;7:206-12. [PubMed]
- van der Sluis PC, van der Horst S, May AM, et al. Robot-assisted Minimally Invasive Thoracolaparoscopic Esophagectomy Versus Open Transthoracic Esophagectomy for Resectable Esophageal Cancer: A Randomized Controlled Trial. Ann Surg 2019;269:621-30. [Crossref] [PubMed]
- Rostas JW, Graffree BD, Scoggins CR, et al. Long-term outcomes after hand-sewn versus circular-stapled (25 and 29 mm) anastomotic technique after esophagogastrectomy for esophageal cancer. J Surg Oncol 2018;117:469-72. [Crossref] [PubMed]
- Deng XF, Liu QX, Zhou D, et al. Hand-sewn vs. linearly stapled esophagogastric anastomosis for esophageal cancer: a meta-analysis. World J Gastroenterol 2015;21:4757-64. [Crossref] [PubMed]
- Cerfolio RJ, Bryant AS, Hawn MT. Technical aspects and early results of robotic esophagectomy with chest anastomosis. J Thorac Cardiovasc Surg 2013;145:90-6. [Crossref] [PubMed]
- Maas KW, Biere SS, Scheepers JJ, et al. Minimally invasive intrathoracic anastomosis after Ivor Lewis esophagectomy for cancer: a review of transoral or transthoracic use of staplers. Surg Endosc 2012;26:1795-802. [Crossref] [PubMed]
- Price TN, Nichols FC, Harmsen WS, et al. A comprehensive review of anastomotic technique in 432 esophagectomies. Ann Thorac Surg 2013;95:1154-60; discussion 1160-1. [Crossref] [PubMed]
- Harustiak T, Pazdro A, Snajdauf M, et al. Anastomotic leak and stricture after hand-sewn versus linear-stapled intrathoracic oesophagogastric anastomosis: single-centre analysis of 415 oesophagectomies. Eur J Cardiothorac Surg 2016;49:1650-9. [Crossref] [PubMed]
- Sugimura K, Miyata H, Matsunaga T, et al. Comparison of the modified Collard and hand-sewn anastomosis for cervical esophagogastric anastomosis after esophagectomy in esophageal cancer patients: A propensity score-matched analysis. Ann Gastroenterol Surg 2018;3:104-13. [Crossref] [PubMed]
- Chao YK, Li ZG, Wen YW, et al. Robotic-assisted Esophagectomy vs. Video-Assisted Thoracoscopic Esophagectomy (REVATE): study protocol for a randomized controlled trial. Trials 2019;20:346. [Crossref] [PubMed]
- Huang L, Onaitis M. Minimally invasive and robotic Ivor Lewis esophagectomy. J Thorac Dis 2014;6:S314-21. [PubMed]
- van Workum F, Slaman AE, van Berge Henegouwen MI, et al. Propensity Score-Matched Analysis Comparing Minimally Invasive Ivor Lewis Versus Minimally Invasive Mckeown Esophagectomy. Ann Surg 2018. [Epub ahead of print]. [Crossref] [PubMed]
- Luketich JD, Pennathur A, Awais O, et al. Outcomes After Minimally Invasive Esophagectomy. Ann Surg 2012;256:95-103. [Crossref] [PubMed]
- Suda K, Ishida Y, Kawamura Y, et al. Robot-assisted thoracoscopic lymphadenectomy along the left recurrent laryngeal nerve for esophageal squamous cell carcinoma in the prone position: technical report and short-term outcomes. World J Surg 2012;36:1608-16. [Crossref] [PubMed]
- Hagens ERC, van Berge Henegouwen MI, Cuesta MA, et al. The extent of lymphadenectomy in esophageal resection for cancer should be standardized. J Thorac Dis 2017;9:S713-23. [Crossref] [PubMed]
- Visser E, van Rossum PSN, Ruurda JP, et al. Impact of Lymph Node Yield on Overall Survival in Patients Treated With Neoadjuvant Chemoradiotherapy Followed by Esophagectomy for Cancer: A Population-based Cohort Study in the Netherlands. Ann Surg 2017;266:863-9. [Crossref] [PubMed]
- Visser E, Markar SR, Ruurda JP, et al. Prognostic Value of Lymph Node Yield on Overall Survival in Esophageal Cancer Patients: A Systematic Review and Meta-analysis. Ann Surg 2019;269:261-8. [Crossref] [PubMed]
- Miyata H, Sugimura K, Yamasaki M, et al. Clinical Impact of the Location of Lymph Node Metastases After Neoadjuvant Chemotherapy for Middle and Lower Thoracic Esophageal Cancer. Ann Surg Oncol 2019;26:200-8. [Crossref] [PubMed]
- Horgan S, Berger RA, Elli EF, et al. Robotic-assisted minimally invasive transhiatal esophagectomy. Am Surg 2003;69:624-6. [PubMed]
Cite this article as: Ji A, Han Y, Li H. Robotic-assisted Ivor-Lewis esophagectomy. Shanghai Chest 2019;3:52.