To evaluate the safety and efficacy of totally laparoscopic total gastrectomy (TLTG) with esophagojejunostomy using a linear stapler compared with laparoscopic-assisted total gastrectomy (LATG) using a circular stapler in gastric cancer patients.

We retrospectively reviewed 687 patients who underwent laparoscopic total gastrectomy for gastric cancer at a single institution from August 2008 to August 2014. The patients were divided into two groups according to the type of operation: 421 patients underwent TLTG and 266 underwent LATG. Clinicopathologic characteristics and surgical outcomes in the two groups were compared and analyzed.

The TLTG group had higher mean ages at the time of operation (57.78 ± 11.20 years and 55.69 ± 11.96 years, P = 0.020) and more histories of abdominal surgery (20.2% and 12.4%, P = 0.008) compared with the LATG group. Surgical outcomes such as intraoperative and postoperative transfusions, combined operations, pain scores and administration of analgesics, and complications were similar between the two groups. However, compared with the LATG group, the TLTG group required a shorter operation time (149 min vs 170 min, P < 0.001), had lower postoperative hematocrit change (3.49% vs 4.04%, P = 0.002), less intraoperative events (3.1% vs 10.2%, P < 0.001), less intraoperative anastomosis events (2.4% vs 7.1%, P = 0.003), faster postoperative recovery such as median time to first flatus (3.30 d vs 3.60 d, P < 0.001), faster median commencement of soft diet (4.30 d vs 4.60 d, P < 0.001) and shorter length of postoperative hospital stay (6.75 d vs 7.02 d, P = 0.005).

The intracorporeal method for reconstruction of esophagojejunostomy using a linear stapler may be considered a feasible procedure comparing with extracorporeal anastomosis using circular stapler because TLTG is simpler and more straightforward than LATG. Therefore, TLTG can be recommended as an appropriate procedure for gastric cancer.

Asian countries, especially South Korea and Japan, have the highest incidences of gastric cancer in the world[1]. Gastric cancer is the second most common cause of cancer-related deaths worldwide[2,3], and surgery is the only curative modality for primary treatment of resectable gastric cancer[4,5]. The proportion of early gastric cancer patients has increased in Korea and Japan as a result of improved nationwide surveillance[6,7], and now accounts for nearly 60% of all cases. The incidence of upper and middle body gastric cancer has also increased. Consequently, the demand for minimally invasive treatments for upper body early gastric cancer has grown, and there is more need for new therapeutic methods and modalities. Laparoscopic gastrectomy has become one of the most popular modalities because of less postoperative pain, rapid postoperative recovery, lower blood loss, better cosmetic outcomes, and fewer complications compared with open gastrectomy[5,8-10]. In addition, the oncologic outcomes of laparoscopic gastrectomy for gastric cancer are acceptable as well[11,12].

Intracorporeal anastomosis has advantages over extracorporeal anastomosis because the former creates a smaller wound, provides a larger workspace and is less invasive[13-19]. Totally laparoscopic total gastrectomy (TLTG) using various types of intracorporeal anastomosis methods has been developed due to improvements in surgical devices and the accumulation of operative experience, but an optimal method for TLTG is yet to be established because of the technical challenges, especially for reconstruction of the esophagojejunostomy (EJ). Since 2008, TLTG using endoscopic linear staplers has been performed in our institute on more than 400 patients by expert surgeons with much experience of laparoscopic surgery, and we have developed a secure and effective technique for reconstructing the EJ[15-17].

In this study, we aimed to evaluate the surgical safety and efficacy of TLTG for treating gastric cancer of the upper third of the stomach by comparing its outcomes with those of laparoscopic-assisted total gastrectomy (LATG) using a circular stapler.

Various modified methods of TLTG have been developed, but no standard method for upper and middle gastric cancer has been established because the reconstruction of intracorporeal EJs requires a high level of technical proficiency and is difficult, even for experienced surgeons[24-28]. We have recently reported a TLTG method developed for intracorporeal EJ using an endoscopic linear stapler, and we believe that it could become a standard method for these patients[16,17]. Although extracorporeal EJ anastomosis using a circular stapler is the generally accepted method for laparoscopic total gastrectomy, the anastomosis is often difficult to complete because of the limited working space formed by the mini-laparotomy[24]. Furthermore, an extended laparotomy incision is sometimes required, but this may reduce the benefits of the laparoscopic approach.

In a study on distal gastrectomy, TLTG without a mini-laparotomy was unaffected by obesity and could, thus, be a safe procedure for avoiding the impact of obesity[18,19]. Similarly, TLTG helps the surgeon easily resect and reconstruct the anastomosis without limiting the surgeon’s view. In a previous study, TLTG produced similar early surgical outcomes to LATG, although the BMI was higher in the TLTG group[29]. In the present retrospective study, the TLTG patients had similar BMIs and tended to be slightly older, with more histories of abdominal surgery compared with LATG patients. Nevertheless, TLTG was superior to LATG in terms of operation time, postoperative hematocrit change, intraoperative events, bowel movements, and postoperative hospital stays. Although TLTG is less invasive than LATG, there was no significant difference in pain score, which was probably due to the use of active pain control, such as patient-controlled analgesia.

Chen et al[5] found in their meta-analysis that the number of lymph nodes harvested in TLTG was marginally higher than in LATG (P = 0.06). In our study, lymphadenectomy seems to have been adequate in both groups, despite the significant difference in the number of retrieved lymph nodes in the LATG and TLTG group (34.91 ± 13.92 and 40.04 ± 15.59, respectively, P < 0.001). The reason for this difference is unclear since the lymphadenectomy procedure is the same in both LATG and TLTG. There was a significant difference between the LATG and TLTG groups with regard to the length of the resection margin (LATG: 3.85 ± 3.11 cm and TLTG: 2.68 ± 2.62 cm, P < 0.001). This could be attributed to the fact that linear staplers are often placed on either side of the resection line, and might hinder accurate histopathologic evaluation of the surgical margin of the resected specimen. Linear staplers generally have four or six rows of staples and form two or three staple lines on a margin of length approximately 4-5 mm as exempted staples on the resection line, in contrast to conventional circular staplers[30]. Moreover, the linear staplers used in TLTG require a substantial length of esophagus for anastomosis. On the other hand, the circular stapler used in LATG allows the esophagus to be transected more proximally and does not need a long esophageal stump. EJ anastomosis using a circular stapler, thus, allows higher anastomosis in patients with tumors at the gastroesophageal junction, or in the upper stomach and invading the esophagus[31,32].

In the current study, the TLTG group was older and had more histories of abdominal surgery. However, the operation time for TLTG was shorter than for LATG. Our TLTG experience suggests several factors that may contribute to this shorter operation time. First, TLTG provides a wider view than LATG. Second, reconstruction in TLTG carried out with a linear stapler is easy, rapid and requires no hand-sewn reinforcement procedure. Finally, opening and closing a mini-laparotomy is not required. Incision for a mini-laparotomy may take especially long additional incision in obese patients. Moreover, our data show that TLTG has superior surgical outcomes in terms of postoperative hematocrit change, intraoperative events, time to first flatus, soft diet and postoperative hospital stay because the intracorporeal method has a wider view and causes less surgical trauma.

Postoperative morbidity after LATG has been reported to range from 17% to 27%[33-38]. In our study, early complication occurring within 30 d following LATG and TLTG classified as Clavien-Dindo classification grade ≥ III were observed in 16 (6.0%) and 35 (8.3%) patients, respectively; late complications developing after 30 d following LATG and TLTG were observed in 11 (4.1%) and 18 (4.3%) patients, respectively. These results show that there were no significant differences between LATG and TLTG in terms of postoperative complications.

Patient characteristics such as age and obesity are risk factors for postoperative complications in laparoscopic gastrectomy. ASA scores may be influenced by age and comorbidity because these factors reinforce each other. Most of all, being overweight is a potent risk factor for poor surgical outcomes[39,40]. Delayed bowel movement, increased postoperative pain, and prolonged hospital stay can occur in obese patients, as we have suggested in a previous report on laparoscopic distal gastrectomy[40]. We found no significant differences in early and late complications between LATG and TLTG, even though the TLTG group patients were much older and had more histories of abdominal surgery. In addition, there was no significant difference between the two groups in complications related to EJ. However, TLTG makes a wide operating space and carries out EJ construction safely, and several investigators have insisted that the anastomotic site should be further secured and have a wider diameter when using a linear stapler than when using a circular stapler[5,16,41].

The procedure of LATG and TLTG differ in many ways. First, TLTG is less invasive, and requires a smaller incision than does LATG. Second, the wider working space in TLTG ensures safe reconstruction of the EJ. Therefore, laparoscopic surgeons are more comfortable with the intracorporeal than the extracorporeal one. Furthermore, using a linear stapler in TLTG has another advantage in that whereas circular staplers have only two staggered rows, endoscopic linear staplers have three staggered rows and provide better staple line security.

We conclude that TLTG requires a shorter operation time and permits faster postoperative recovery than LATG, while having similar surgical outcomes and complications. Therefore, TLTG using a linear stapler may be considered a more appropriate procedure than LATG using a circular stapler, and may be recommended for the treatment of gastric cancer of the upper third of the stomach.

This study has certain limitations. It is a retrospective study from a single institution and the baseline clinical characteristic of the two groups were different. Although the pathologic results for the patients in the LATG and TLTG groups were similar, the LATG and TLTG operations were performed at different periods of time. In addition, cancer recurrence and long-term survival rates were not analyzed because approximately half the patients underwent surgery, and 5 years had not yet passed. Therefore, data on long-term outcomes are still needed in order to compare the oncological adequacy of these two methods.