Current status of laparoscopic total gastrectomy

Abstract In this article, the current state of laparoscopic total gastrectomy (LTG) was reviewed, focusing on lymph node dissection and reconstruction. Lymph node dissection in LTG is technically similar to that in laparoscopic distal gastrectomy for early gastric cancer; however, LTG for advanced gastric cancer requires extended lymph node dissections including splenic hilar lymph nodes. Although a recent randomized controlled trial clearly indicated no survival benefit in prophylactic splenectomy for lymph node dissection at the splenic hilum, some patients may receive prognostic benefit from adequate splenic hilar lymph node dissection. Considering reconstruction, there are two major esophagojejunostomy (EJS) techniques, using a circular stapler (CS) or using a linear stapler (LS). A few studies have shown that the LS method has fewer complications; however, almost all studies have reported that morbidity (such as anastomotic leakage and stricture) is not significantly different for the two methods. As for CS, we grouped various studies addressing complications in LTG into categories according to the insertion procedure of the anvil and the insertion site in the abdominal wall for the CS. We compared the rate of complications, particularly for leakage and stricture. The rate of anastomotic leakage and stricture was the lowest when inserting the CS from the upper left abdomen and was significantly the highest when inserting the CS from the midline umbilical. Scrupulous attention to EJS techniques is required by surgeons with a clear understanding of the advantages and disadvantages of each anastomotic device and approach.

implemented in patients with advanced gastric cancer at high-volume centers, and RCT comparing the feasibility and long-term survival between LDG and ODG are currently ongoing in China (CLASS-01 trial 18 ), Korea (KLASS-02 trial 19 ), and Japan (JLSSG0901 20 ).
In contrast, laparoscopic total gastrectomy (LTG) is not common compared with LDG, which is carried out in only 25% (1556/6183) of total gastrectomy procedures, according to a questionnaire-based survey conducted by the Japan Society of Endoscopic Surgery in 2015, although the proportion of LDG had increased to 54% (6884/ 12 722). 21 In this survey, the conversion rate in LTG was reported as 2.1% which was about three times as compared with 0.6% in LDG. Furthermore, according to the National Clinical Database (NCD), covering 95% of general surgery procedures in all of Japan, LTG is carried out in 18% (5749/32 144) of total gastrectomy procedures. 22 Several reports have already published data on the feasibility and safety of LTG, but these reports were mainly from high-volume centers, and almost all the LTG were carried out by surgeons who were already accustomed to laparoscopic gastrectomy. Many surgeons still hesitate to carry out LTG, and the main reasons are difficulty of lymphadenectomy at the splenic hilum and the high technical demands of esophagojejunostomy (EJS).
Two large-scale reports based on data from the National Clinical Database, one retrospective 22 and the other prospective, 23 have been recently reported as so-called "real-world data" in Japan, with controversial results about the occurrence of anastomosis-related complications.
In this article, the status of LTG was reviewed focusing on lymphadenectomy and reconstruction.

| LYMPHADENECTOMY
Lymphadenectomy, excision of the regional lymph nodes (LN) draining from a tumor, is an essential element in the surgical management of gastric cancer. The extent of systematic lymphadenectomy is defined, respectively, for each type of gastrectomy, according to Japanese gastric cancer treatment guidelines. 24 In principle, D1 and D1 + lymphadenectomy is indicated for early gastric cancer, and D2 lymphadenectomy for advanced gastric cancer and cases with apparent metastasis at the regional lymph nodes, even in early gastric cancers. In D1 + lymph node dissection, differences between LDG and LTG are only left paracardial LN (No. 2), left greater curvature LN along the short gastric arteries (No. 4sa) which is usually easily removed with the stomach in LTG, and proximal splenic artery LN (No. 11p) which is generally removed in LDG for early gastric cancer.
In that sense, technical aspects of lymph node dissection in LTG are like those in LDG for early gastric cancer; therefore, the prognostic evidence based on results of RCT (JCOG 0912), which confirm that LDG is not inferior to ODG in efficacy for early gastric cancer, would be applicable to LTG.
However, LTG for advanced gastric cancer requires precise lymph node dissection. As for LDG, two RCT, JLSSG0901 and KLASS-02, are in progress and the results will soon be available; they compare long-term outcomes of LDG with those of ODG. In contrast, although some retrospective studies have reported that longterm outcome of LTG is equivalent to that of open total gastrectomy (OTG), RCT in LTG for advanced gastric cancer has just been started in Korea (KLASS-06).
Among several LN stations, splenic hilar (No. 10) and along the distal splenic artery (No. 11d), the LN are specific and are the most applicable regions for the procedure of LTG for advanced gastric cancers. Survival benefit of lymphadenectomy for these regions remains controversial not only for laparoscopic surgery, but also for open surgery of advanced gastric cancer.
The difficulty of lymphadenectomy of the region is due to anatomical variation of the splenic hilar vessels and the narrow and deep space, and lymphadenectomy increases the risks of operative morbidities including pancreatic fistula. In recent reports, the incidence of pancreatic fistula in LTG ranged between 0.2% and 2.7% and this rate is equivalent to OTG. 22,23,25,26 Furthermore, some reports 22,25 showed that the incidence of overall complications of LTG was equivalent to that of OTG, and other reports showed that the rate of complications was lower for LTG than for OTG. 23,26,27 One of the reasons for this is the improvement of energy devices, which is described in many reports, 28,29 and some researchers reported that preoperative assessment of splenic vascular anatomy using computed tomography (CT) with 3-D imaging was useful and correlated with shorter operative time, lower blood loss, 30 and a larger number of retrieved lymph nodes. 31 Open total gastrectomy with splenectomy has been standard in Japan for complete removal of lymph nodes at the splenic hilum.
Splenectomy can be done safely even in laparoscopic surgery by experienced surgeons, and the procedure itself is feasible with good short-term outcomes. [32][33][34] Several recent retrospective reports, however, showed that splenectomy in open total gastrectomy could increase postoperative morbidity and mortality 35,36 without survival benefit. 37,38 In 2017, a multi-institutional RCT comparing splenectomy with spleen preservation in proximal gastric cancer was conducted in Japan. 39 Splenectomy was associated with higher morbidity and greater blood loss, but had no survival benefit. The RCT concluded that prophylactic splenectomy, even in open surgery, should be avoided not only for operative safety but also for survival benefit, except for cases with tumors invading the greater curvature and with Borrmann type 4 tumors (linitis plastica).
Conversely, the clinical significance of lymph node dissection for cases with tumors invading the greater curvature and type 4 advanced gastric cancer remains a matter of debate. We reported that patients with tumors localized on the greater curvature and type 4 cancer might obtain relatively high survival benefits from splenic hilar lymph node dissection. 40     In Table 1, literature that compares two anastomosis methods in a single institution is shown. [51][52][53][54][55][56] Five of the studies reported that morbidity such as anastomotic leakage and stricture were not significantly different in CS and LS methods; however, one report showed that the LS method has fewer complications.

| LINEAR STAPLER
Esophagojejunostomy using LS is mainly divided into two types; a functional end-to-end anastomosis (FEEA) and a side-to-side anastomosis (called the "overlap method"). They concluded that when the crus was incised to improve the visual field of the anastomosis, it should have been repaired.

| CIRCULAR STAPLER
As described above, many surgeons are familiar with reconstruction methods using the CS. Therefore, the CS method has been more widespread than the LS method, especially in the introductory period. Since the transorally inserted anvil (OrVil) was developed, it is easier and very convenient to carry out intracorporeal EJS and esophagogastrostomy. Several reports have reported the safety and feasibility of EJS carried out by the CS method in LTG. 63 However, some papers noted a high incidence of postoperative complications in CS methods.
For this paper, a literature retrieval was carried out in PubMed for January 1, 1997 through April 30, 2018. The search terms included "laparoscopic," "total gastrectomy," and "gastric cancer." Reports in languages other than English, reviews, and meta-analyses were excluded, and cases <10 were also excluded.  Figure 1, the visual field differed depending on the approach of the anastomotic device, and the left upper abdomen provided the widest visual field of the anastomotic plane.
Results showed that the occurrence rates of anastomotic leakage and stricture were the lowest in the upper left abdomen approach, and anastomotic complications were significantly higher in a midline umbilical approach. These results suggested that a good visual field may reduce anastomotic complications, and surgeons should be particularly attentive to maintaining a good visual field for the anastomotic plane, even in the umbilical approach, and avoiding unnecessary tension during anastomosis.
The flexible laparoscope should be useful in obtaining a good view where a straightforward view is difficult. However, only a few reports were confirmed to use the flexible laparoscope in each approach; therefore, it is not yet clear whether these complications can be reduced by the use of a flexible scope.

| CONCLUSION
We reviewed several recent reports on lymphadenectomy and reconstruction in LTG. As cancers located at the upper third of the stomach and at the esophagogastric junction have increased in recent years, 100 in the future, safe and secure LTG is important.
According to the Japanese gastric cancer treatment guidelines, LTG for clinical stage I gastric cancer may be carried out; however, it is recommended that the procedure be conducted under the guidance of experienced surgeons. In contrast, LTG has been rated by the guidelines of the Japan Society for Endoscopic Surgery (2014) as recommendation C1 (may be considered for a patient in need of total gastrectomy, but no scientific evidence in support of the procedure is currently available). Those who consider challenging the procedure should plan to do so with sufficient caution as postoperative complications were reported to occur significantly more often in the first year of its introduction. 24 Concerning advanced cancer, a Korean group has launched a large multi-institutional clinical study for prognostic evaluation of lymph node dissection in LTG for advanced gastric cancer (KLASS-06). LTG for advanced gastric cancer should be carried out on a trial basis until the definitive results are available, and surgeons should be particularly attentive to nodes No. 10 and 11d in a lymphadenectomy without lessening the quality of lymph node dissection compared with OTG.
Then again, inappropriate reconstruction sometimes results in postoperative complications, some of which have recently been reported to correlate with poor long-term oncological outcome. 101,102 In that sense, surgeons must give scrupulous attention to leakage and stricture after EJS while understanding the advantages and disadvantages of each anastomotic device and approach.