Robotic surgery for esophageal cancer: Merits and demerits

Abstract Since the introduction of robotic systems in esophageal surgery in 2000, the number of robotic esophagectomies has been gradually increasing worldwide, although robot‐assisted surgery is not yet regarded as standard treatment for esophageal cancer, because of its high cost and the paucity of high‐level evidence. In 2016, more than 1800 cases were operated with robot assistance. Early results with small series demonstrated feasibility and safety in both robotic transhiatal (THE) and transthoracic esophagectomies (TTE). Some studies report that the learning curve is approximately 20 cases. Following the initial series, operative results of robotic TTE have shown a tendency to improve, and oncological long‐term results are reported to be effective and acceptable: R0 resection approaches 95%, and locoregional recurrence is rare. Several recent studies have demonstrated advantages of robotic esophagectomy in lymphadenectomy compared with the thoracoscopic approach. Such technical innovations as three‐dimensional view, articulated instruments with seven degrees of movement, tremor filter etc. have the potential to outperform any conventional procedures. With the aim of preventing postoperative pulmonary complications without diminishing lymphadenectomy performance, a nontransthoracic radical esophagectomy procedure combining a video‐assisted cervical approach for the upper mediastinum and a robot‐assisted transhiatal approach for the middle and lower mediastinum, transmediastinal esophagectomy, was developed; its short‐term outcomes are promising. Thus, the merits or demerits of robotic surgery in this field remain quite difficult to assess. However, in the near future, the merits will definitely outweigh the demerits because the esophagus is an ideal organ for a robotic approach.

was carried out by Horgan et al. 4 in September 2001 at the University of Illinois, Chicago. Horgan's procedure was a transhiatal esophagectomy (THE). Robotic transthoracic radical esophagolymphadenectomy (a type of TTE) was first done in November 2002 at the University of Iowa Hospital, Iowa City, and reported by Kernstine et al. 5 Initially, the potential advantages of this technological innovation were thought to allow surgeons to carry out more precise and safer, more minimally invasive procedures, compared with conventional laparoscopic procedures. 6 Also, the esophagus was regarded as an ideal organ for a robotic approach, 7 because the esophagus is anatomically located in a limited and narrow space, the mediastinum, behind such vital organs as the heart and the trachea. Figure 1 shows growth in the number of robotic esophagectomy procedures using the da Vinci system around the world. Although the numbers are gradually increasing worldwide, robotic esophagectomy for esophageal cancer is not yet regarded as a standard procedure, or as superior for treatment of urological and gynecological malignancies because of the lack of clear benefits. 8 Robotic surgery's advantages and disadvantages for esophageal cancer thus remain controversial.
We reviewed this problem focusing on robotic surgery for esophageal carcinoma, although high-level evidence is lacking because of the absence of any except currently ongoing randomized controlled trials. 9 2 | EARLY RESULTS WITH SMALL SE RIES
Robotic THE was reported to be safe even after chemoradiotherapy. 12 These reports showed high complication rates, approximately 50%; one patient (1/81, 1.2%) died from pulmonary failure after surgery. Table 1 summarizes the surgical outcomes of these series. One paper reported a high incidence (19.4%, 7/36) of incarcerated hiatal hernia after robotic THE. 13 Indications for robotic THE were mostly adenocarcinomas located in the distal esophagus and gastroesophageal junctions. [10][11][12] 3 | EARLY RESULTS WITH SMALL SERIES

| AFTER THE INITIAL SERIES
To the best of our knowledge, very few or no series of robotic THE have been published following the initial small series; more results of F I G U R E 1 Growth in the number of robotic surgery procedures worldwide. © Intuitive Surgical, Inc. robotic TTE, albeit few, have been published. [29][30][31][32] Surgeons still disagree over the relative merits of THE versus TTE. One paper reported seriously high morbidity in both groups. 33 Another paper reported that TTE achieved a higher rate of R0 resections, a higher lymph node yield, and resulted in longer survival than THE, especially in advanced cases. 34 Therefore, TTE is putatively more radical and therefore a more definitive treatment for esophageal cancer.
Recent papers report that robotic esophagectomy is feasible for patients with a high body mass index, 35 the elderly, 36 and patients undergoing neoadjuvant chemoradiotherapy. 37 Compared with initial periods, operative time and blood loss have been reduced, and the number of harvested lymph nodes has increased. Indications for robotic TTE are similar to those for conventional procedures, and tumor locations were mostly the middle esophagus, the lower esophagus, or the gastroesophageal junctions. 29-32 A potential advantage of real-time perfusion assessment using indocyanine green and software built into the robotic console was recently reported: 38 prevention of anastomotic leakage with allegedly easier detection of poorly perfused tissues at the anastomotic site.

| ONCOLOGICAL LONG-TERM RESULTS
More than 15 years have passed since robotic surgery began to be used in esophageal cancer treatment, and several papers have reported oncological long-term results. The Utrecht group, one of the pioneers in this field, reported that, based on 108 cases, their radical resection (R0) rate was 95%, 5-year overall survival (OS) was 42%, and locoregional recurrence was only 6%. 39 The Yonsei group, another pioneer, also reported R0 and 3-year OS rates of 95.7% and 85%, respectively. 40 In their series, 3-year OS was 77.8% even in stage IIIA disease. Both groups concluded that robotic TTE is oncologically effective and acceptable with a high R0 rate and adequate lymphadenectomy. Galvani et al. 10 18 267  54  10  14  11  33  5 Dunn et al. 11  In comparisons of robotic to thoracoscopic approaches (ie minimally invasive esophagectomy), the first such paper published failed to show any clear advantages. 43  The longer operative time was pointed out as a disadvantage. The most important concern is that high-level evidence of robotic esophagectomy's superiority is lacking, despite technical, oncological, and safety advantages over conventional procedures. One reason is that no randomized controlled trial of sufficient size has been conducted to show any clear benefit. Another problem is cost. Some benefit must be shown to outweigh the higher cost. The combination of fluorescence, overlay, or other advanced diagnostic imaging with robotic procedures has additional potential benefits. To conclude, robotically assisted meticulously executed procedures are expected to reduce the development of complications and improve the radicality of lymphadenectomy, which will translate into good short-and long-term outcomes.

| NOVEL PROCEDURES
With the aim of averting postoperative pulmonary complications without diminishing lymphadenectomy (ie aiming at equivalence to the transthoracic approach), a nontransthoracic radical esophagectomy procedure has been developed which combines a video-assisted cervical approach for the upper mediastinum (Figure 2A) and a robot-assisted transhiatal approach for the middle ( Figure 2B) and lower mediastinum. 48,49 The

| COMMEN TS
No-one denies the technical innovativeness and advantages of robotic surgery, and the anatomical features of the esophagus make it an ideal organ for robotic surgery. Robotic surgery therefore has merits for esophageal cancer, but it is still not regarded as a standard procedure, as a result of the paucity of definite high-level evidence and its unacceptably high cost. We must wait for the results of ongoing randomized controlled trials to be reported 9 and look forward to seeing competition leading to lower costs. Meanwhile, continuous endeavors to identify and develop additional areas of progress in the technology such as epochal imaging systems or TME applying the strong points of robots are crucial for academic surgeons pioneering the use of robotic systems.