Short-term outcomes of robotic- versus laparoscopic-assisted Total Gastrectomy for advanced gastric Cancer: a propensity score matching study

Gastric cancer (GC) is the fifth most common cancer and the third leading cause of cancer-related death worldwide [1]. Its incidence and mortality rates have been steadily declining worldwide since the middle of the 20th century [2, 3]. However, it is notable that the morbidity of esophagogastric junction cancer is increasing in Western and Eastern countries [2‐5]. Total gastrectomy (TG) with adequate regional lymphadenectomy is the most common treatment choice for upper GC and includes cancers located in the proximal third of the stomach and esophagogastric junction (EGJ) (Siewert type II and III) or cancers located at the lower two-thirds of the stomach to ensure a tumour-free surgical margin [6‐8]. Since Kitano [9] reported laparoscopy-assisted distal gastrectomy in 1994 for the first time, laparoscopy-assisted gastrectomy has been widely used for gastric cancer [10‐12]. Despite its technical difficulty, laparoscopy-assisted total gastrectomy (LATG) has been shown to be technically feasible and is superior to open total gastrectomy performed by experienced surgeons in terms of its safety and short-term outcomes [13, 14]. However, the two-dimensional visualization and limited movement of laparoscopic instruments make it difficult to perform lymphadenectomy precisely. Robotic surgical system overcomes those limitations including eliminating the traces of physiologic human tremor and increasing dexterity through its typical internal articulated endoscopic wrist (EndoWrist™ System) for a precise lymphadenectomy with a 3D high-resolution images at the console [15]. In 2002, Hashizume reported robotic-assisted gastrectomy for the first time [16]. Since then, robotic surgery has been demonstrated to obtain similar or even better anatomical and operative conditions compared to the traditional laparoscopic approach during gastric resection [15, 17‐21]. However, most of the reported cases were early gastric cancer (EGC) [22, 23], and few studies have retrospectively compared robotic-assisted total gastrectomy (RATG) with LATG for advanced gastric cancer (AGC) [15, 24]. The aim of this study is to evaluate the feasibility and safety of RATG and LATG for AGC using the propensity score matching (PSM) method.

It is well known that total gastrectomy combined with complete D2 lymphadenectomy and esophagojejunostomy is a technically difficult procedure compared to distal gastrectomy to dissect more lymph nodes [12]. Nonetheless, we described our experience with LATG in the treatment of AGC in 2013, which indicated that LATG was a feasible and safe alternative to standard open gastric resection with similar short-term and long-term results [29]. In regard to RATG, Yoon et al. and Son et al. both reported comparable short-term surgical and oncologic outcomes between RATG and LATG, yet EGC patients accounted for a large percentage of the population in their studies [22, 23]. Ye’s study, which included a total of 205 patients with AGC who underwent RATG or LATG, reported that RATG had a longer operation time, more RLNs, and less operative blood loss and volume of abdominal drainage compared to LATG, and the complication rate was comparable (7.5% vs. 9.1%, p = 0.915, 24]. To the best of our knowledge, our study is the first to report the short-term outcomes of RATG compared with LATG for AGC using the PSM method to reduce bias.

Generally, robotic gastrectomy is known to have some advantages over laparoscopic surgery in reducing perioperative bleeding [17, 24, 30]. In our study, we also concluded that robotic surgery can reduce intraoperative bleeding compared to laparoscopic surgery after PSM (154.37 ± 89.68 vs. 183.77 ± 95.39 ml, p = 0.004). Although the mean difference of approximately 30 mL of blood loss between the two minimally invasive groups may not provide much clinical benefit for every individual patient, this may show that the robot can operate more accurately to reduce bleeding. However, the present study demonstrated that the operative time of RATG was significantly longer than that of LATG after PSM, which was consistent with the findings of previous studies [22‐24]. The docking time of robot arms, the time for arm change during clipping, and the lack of experience of the assistants may explain the longer operative time [22]. The docking time of robotic surgeries was between 20 and 60 min, as reported in a meta-analysis [31]. Since all of our surgeons had performed robotic surgery (RG) for more than 30 cases, the docking time mainly accounted for the prolonged operating time. Hence, the extra time spent in our study (approximately 20 min) for robotic surgery could be acceptable, as docking time was inevitable.

D2 lymphadenectomy is an indispensable process for the application of minimally invasive surgery for AGC [32]. The dissection of the N2 area is the most crucial part of lymphadenectomy. It has been reported that robotic surgery could retrieve more dissected lymph nodes, especially in the technically demanding N2 area, especially in the suprapancreatic area and splenic vessels [33]. In addition, Son et al. found that robotic spleen-preserving total gastrectomy could retrieve more LNs around splenic vessels and the hilum than laparoscopy, and they even compared each group and their metastases [23]. At the same time, the subgroup analysis of a meta-analysis revealed that the number of RLNs of RG was significantly higher than that of LG (p = 0.03, 31]. Our study shown that RATG can retrieve more N2 tier RLNs (p = 0.007 vs. p = 0.016) than LATG both before and after PSM. Nevertheless, the difference in RLNs between the two methods was not clinically significant after PSM. Moreover, the study by Shen et al., which included 23 robotic and 75 laparoscopic total gastrectomy procedures, reported that the RAG and LAG groups had no significant difference in the number of harvested lymph nodes [30]. Li et al. found in their stratified analysis of 92 patients after PSM that the average number of RLNs was not significantly different between robotic and laparoscopic total gastrectomy (30.6 vs. 32.0, p = 0.406, 34]. Therefore, it is still controversial whether robotic total gastrectomy can retrieve more lymph nodes. Thus further studies of robotic total gastrectomy, especially RCTs, should be conducted to focus on this issue.

Postoperative complications are an important factor to evaluate the safety and feasibility of a surgical procedure. We evaluated postoperative complications according to the Clavien-Dindo classification system, which is applicable in most parts of the world [25]. Previous studies have proven that the complication rate of laparoscopic total gastrectomy varies from 9.1 to 34.6% [14, 22‐24, 34, 35]. In the current study, the complication rate of the RATG group was not significantly different from that of the LATG group before PSM (23.8% vs. 29.2%, p = 0.268) and after PSM (23.8% vs. 28.6%, p = 0.390). Not surprisingly, pulmonary complications obviously accounted for most of the complications in our study. Upper abdominal surgery combined with pneumoperitoneum and postoperative pain affect the activity of the diaphragm and lead to micro-atelectasis, which in turn causes pulmonary dysfunction. More importantly, total gastrectomy was an independent risk factor for pulmonary complications [36]. Moreover, anastomosis complications were considered to be one of the most serious complications after TG and result in poorer quality of life, prolonged hospital stay, and increased surgery-related costs and mortality [37]. The Japanese National Clinical Database (NCD) of digestive surgery reported that the incidence of anastomotic leakage after total gastrectomy was 4.4% (881 of 20,011) in 2011 [38]. Of the 383 patients included in the analysis, 6 patients in the RATG group and 10 in the LATG group encountered anastomosis-related complications (4.76% vs. 3.89%, p = 0.689). The ratio of anastomosis-related complications in the present study was similar with that in previous studies.

Since total gastrectomy was the most common treatment choice for upper gastric cancer, which includes tumours in the proximal third of the stomach and EGJ [6‐8], we conducted subgroup analysis according to tumour location. RATG for tumours located at the EGJ showed less intraoperative bleeding and comparable surgical outcomes compared to LATG. As we have mentioned the merits of robot, RG can manage the narrow anatomical fields such as the fundus of the stomach and esophageal hiatus more easily than LG, just as it can overcome the limitations of laparoscopic surgery in the pelvis during rectal surgery [39]. Despite not achieving much statistical significance, RATG have some advantages in dealing with EGJ cancer compared with LATG in our view combined with our limited surgical experience.

However, this study has several limitations. First, the results were based on a retrospective analysis from a single-clinic institution. Second, the present study lacks a detailed comparative analysis of the cost-effectiveness and gastrointestinal function recovery index between robotic and laparoscopic gastric surgery. Third, although the five surgeons who performed the surgeries received robotic surgery certification and were experienced in both minimally invasive surgeries, different surgeons can still cause some bias and further influence the results. Despite this study having some limitations, our findings provide evidence for minimally invasive surgery of total gastrectomy for AGC. Further well-designed studies, especially RCTs or prospective trials, are needed to assess the impact of RATG and LATG.

This retrospective study demonstrates that RATG is comparable to LATG in terms of short-term surgical outcomes. With longer operation time, less estimated blood loss, more N2 tier RLNs and similar complication rate after PSM, RATG is a safe, reliable and promising approach compared with LATG for the treatment of AGC. Well-designed and randomized controlled trials are needed to further compare RATG with LATG.