AIM: To assess the efficacy and safety of intracorporeal esophagojejunostomy in patients undergoing laparoscopic total gastrectomy (LTG) for gastric cancer.

METHODS: A retrospective review of 81 consecutive patients who underwent LTG with the same surgical team between November 2007 and July 2014 was performed. Four types of intracorporeal esophagojejunostomy using staplers or hand-sewn suturing were performed after LTG. Data on clinicopatholgoical characteristics, occurrence of complications, postoperative recovery, anastomotic time, and operation time among the surgical groups were obtained through medical records.

RESULTS: The average operation time was 288.7 min, the average anastomotic time was 54.3 min, and the average estimated blood loss was 82.7 mL. There were no cases of conversion to open surgery. The first flatus was observed around 3.7 d, while the liquid diet was started, on average, from 4.9 d. The average postoperative hospital stay was 10.1 d. Postoperative complications occurred in 14 patients, nearly 17.3%. However, there were no cases of postoperative death.

CONCLUSION: LTG performed with intracorporeal esophagojejunostomy using laparoscopic staplers or hand-sewn suturing is feasible and safe. The surgical results were acceptable from the perspective of minimal invasiveness.

Since the first reported laparoscopy assisted distal gastrectomy (LADG) was performed for gastric disease in 1994[1], for tumors relatively low in the stomach, interest for this surgical approach has continued to grow. For middle or upper gastric adenocarcinoma, laparoscopy assisted total gastrectomy (LATG) has become more popular than laparoscopy assisted proximal gastrectomy (LAPG) due to the relatively lower rate of reflux esophagitis. In addition, LATG is the treatment of choice for middle or upper gastric adenocarcinoma with deeper invasion[2,3].

Because of the narrow operating window, however, technical problems during extracorporeal esophagojejunostomy may necessitate performing an exit via a mini-laparotomy. This relatively small incision has a number of disadvantages, including removal of the possibly challenging specimen, contamination through the incision, and extra pulling over the residual stomach[4].

Based on our extensive laparoscopic experience obtained from performing laparoscopic pancreatic, gastric, and other operations[5-11], we developed totally laparoscopic total gastrectomy (TLTG) for middle or upper gastric cancer. Here, we describe our 7-year experience using this technique and the short-term clinical results obtained using different kinds of intracorporeal esphagojejunostomy using laparoscopic staplers or a hand-sewn suture technique.

The use of laparoscopic gastrectomy (LG) for gastric cancer has been gradually accepted because of its short-term benefit and the comparable oncological results as open gastrectomy. Most available studies on LG have focused on LDG for tumors located in the lower third of the stomach, which is the most common type in East Asia[12,13]. The incidence of tumors located in the upper and middle stomach has been evaluated recently and has resulted in an increased demand for LTG.

The major indications and technical aspects for LTG are similar to those for LDG. Several technical points relevant to the safety and feasibility of this technique should be addressed. The additional requirement set for the lymph nodes over the splenic hilum or any other short gastric artery represents a difficulty that has been encountered in fundamental gastrectomy. This requirement exists because the splenic vessels flow circuitously, with the branches substantially varying from one to another in deep locations. It is well known that hemorrhage or ischemia could occur because of splenic vascular injury during dissembling of lymph nodes neighboring splenic artery branches. Laparoscopy, compared with the laparotomy, permits the operator to finish dissembling the lymph nodes, which are quite clear, and assists in developing surgical safety. Therefore, the most obvious obstacle to LTG is still the difficulty involved in esophagojejunostomy, which can be performed extracorporeally or intracorporeally. Indeed, it is quite difficult in many cases to conduct the anastomosis via a mini-laparotomy, because space is quite restricted and narrow, specifically in obese victims with relatively thick abdominal walls or the specific tumors that exist in an upper location. It is for this reason that we started to conduct extracorporeal anatomosis, hoping to deal with the barricades of cumbersome reconstruction. We first introduced the use of intracorporeal anastomosis after LTG in 2007.

Two approaches for mechanical esophagojejunostomy have been used in LTG, linear stapling and circular stapling. Circular stapling enjoys similar merits as open total gastrectomy (OTG). The esophagojejunostomy can be performed successfully by adopting a circular stapler via a structure technique, which was hand-sewn in the first 18 patients of our series to mend the anvil that was applied in the esophageal stump. Based on our experience, the esophagus was not cut off initially, and the cardia was tightly tied with a band and then stretched down to expose the esophagus. Purse-string sutures were undertaken, and the anterior wall of the esophagus was then cut with a harmonic scalpel to form a half-circle. After placement of the anvil, the suture line was tightened and the esophagus was finally cut off with the harmonic scalpel. However, the circular stapler was inappropriate for placement during laparoscopic surgery due to its larger size and the absence of a matching tube. The pneumoperitoneum was vulnerable to its placement, and vision was unclear. Therefore, it was not an ideal method and may have resulted in a higher rate of postoperative complications[14,15], especially in our early experience. Thus, a novel transorally inserted anvil (OrVil; Covidien, Mansfield, MA, United States) was introduced to address the challenge of anvil placement[16]. OrVil is not only good in terms of operation safety and treatment effects but also in the reduction in operation time. However, due to its high cost, possibility of bacterial contamination in the abdominal cavity, and injury to the esophageal mucosa, this method is adopted only in some specialized medical centers.

A linear stapler was used for side-to-side esophagojejunostomy. This method was first reported by Uyama et al[17] and was modified by Wang et al[18]. Circular stapling was performed to isolate separately the esophagus and jejunum prior to anastomosis. The linear stapler was inserted at the two ends to complete the anastomosis and then closed the collective opening. Benefits of the linear stapling method involved no initial dissection of the jejunum and esophagus to pull down the esophagus. Thus the esophagus did not need to be completely retracted to the chest; and instead, the specimen was removed, and the common opening was closed together after completion of the anastomosis, economizing the staplers. This method was simple to perform, and the anastomotic stoma was bigger, which may have helped avoid postoperative complications, such as anastomotic stenosis. With regard to specific surgical methods, some surgeons advise that the position taken by the esophageal and jejunum stump should be fixed, adopting at least one stitch prior to the endoscopic linear staple that has been applied[19]. However, in our practice, it has been found that the suture angulates and suspends the jejunum, posing great challenges to the endoscopic linear stapler, sacrificing the mobility of the jejunum. According to our experience, it is more favorable to place one arm of the endoscopic linear stapler, which has been applied into the opening of the jejunum, and to clamp the two arms with no stapling. Later, with the assistance of the stapler, attracting the jejunum close to the esophageal stump’s rear and then unveiling the two arms to replace the second one finishes the anastomosis following the apposition, which has been proven to be quite satisfactory. However, even using this approach, possible issues remain, including taking the distortion over the mesenterium and Roux limb as well as the slipping over the esophagojejunal anastonomic site applied in the comparative lower mediastinum. The surgical margin is limited as a longer esophageal stump should be reserved.

The delta-shaped esophagojejunostomy provides a considerable lumen, regardless of the size of the esophageal stump. More importantly, as a long esophageal stump and anastomosed intestine are not required, this technique achieves less flexion in order to provide enough blood supply for the anastomotic site, thus decreasing the risk of anastomotic leakage. However, surgeons of the technique should have proficient laparoscopic suturing skills, or the outcome of the anastomosis will be impacted because of the unfavorable apposition of the average opening. The assistant should maneuver the stay suture efficiently to ensure that the stapler is applied adequately on all layers of the esophagus[20]. Hand-sewn end-to-side esophagojejunostomy overcomes the limitations caused by the mechanical method. The suturing process can be clearly observed under high definition laparoscopy, and the anastomosis is reliable. The operating space is large, and there is no tension in the whole anastomosis procedure, thus avoiding injury. More importantly, this method completes the anastomosis after removal of the specimen, as the anastomosis can be performed after negative margins are confirmed using intraoperative frozen sections. This method does not require a long esophageal stump. In patients with a positive resection margin, the removal length can be expanded appropriately to confirm a negative resection margin. Therefore, the R0 resection can be improved, and the conversion rate to laparotomy is reduced. However, the hand-sewn method requires operators with extensive experience in laparoscopic suturing, which may increase surgery time. In our experience, progressive practice (from practice on the simulator to practice on animal models and simple suture under laparoscopy, and finally to laparoscopic gastrointestinal anastomosis) can effectively shorten the learning curve. At the same time, the application of new laparoscopic instruments can simplify intracorporeal hand-sewn suturing. Knotless barbed sutures (V-Loc^TM; Covidien, Mansfield, MA, United States) can reduce the time of anastomosis and can ensure the safety of anastomosis, with no need for permanent traction during the whole anastomosis procedure.

We recommend that the reconstruction method using a stapler should be selected on the basis of tumor location. In our experience, side-to-side or delta-shaped esophagojejunostomy using a linear stapler can be adopted for patients with lesions in the body and fundus of the stomach as well as the lower cardia. For patients with lesions in the upper and middle cardia, end-to-side esophagojejunostomy using a circular stapler is chosen to ensure a negative surgical margin. In addition, if the surgeon is well experienced with the laparoscopic hand-sewn technique, it can be used after total gastrectomy, regardless of tumor location.

In conclusion, we demonstrated that LTG facilitated with intracorporeal anastomosis is feasible and safe, leading to quite favorable contemporary results. However, the clinical efficacy should be demonstrated further in a perfectly designed randomized controlled clinical trial. The choice of approach for intracorporeal anastomosis depends mainly on the surgeon’s preference and experience.