Abstract
Background: This study was designed to evaluate the surgical outcomes as well as the morbidity and mortality of totally laparoscopic total gastrectomy (TLTG) compared to laparoscopically-assisted total gastrectomy (LATG), and to confirm the feasibility and safety of TLTG. Patients and Methods: Between August 2009 and January 2014, 56 patients underwent laparoscopic total gastrectomy for gastric cancer. Among them, 27 underwent TLTG using a linear stapler and 29 underwent LATG using a circular stapler for esophagojejunostomy. Results: Clinicopathological characteristics did not differ significantly between groups, except for stage and tumor size. Anastomotic time and estimated blood loss did not differ significantly. Differences in the number of retrieved lymph nodes and the proximal cut margin were not found to be significant. Early postoperative complications were observed in five patients in both groups. No mortality occurred in either group. Conclusion: The outcomes of TLTG are not inferior to those of LATG. TLTG for gastric cancer is technically feasible and safe.
Gastric cancer is the third leading cause of cancer-related death for men and the fifth leading cause of death for women, according to data obtained from global cancer statistics. In addition, Eastern Asia, and in particular Korea and Japan, have the highest incidences of gastric cancer in the world (1). Since Kitano et al. introduced laparoscopic distal gastrectomy for early gastric cancer (2), this technique has been rapidly adopted within Korea and Japan. Laparoscopic surgery has become one of the most popular modalities because of its reduced postoperative pain, earlier recovery of bowel function, shorter hospital stays, and better cosmetic outcomes. In addition, surgical outcomes of laparoscopic gastrectomy for patients with early gastric cancer are comparable to those of open gastrectomy (3, 4). Many studies have compared laparoscopically assisted distal gastrectomy (LADG) with totally laparoscopic distal gastrectomy (TLDG) for gastric cancer. In the majority of these studies, TLDG was found to be safe and feasible in comparison to LADG (4, 5). Furthermore, since laparoscopic total gastrectomy was first reported in a technical note in 1999 (6), many surgeons have adopted this method for gastric cancer. In line with this, the majority of studies related to laparoscopic total gastrectomy published within the past 5 years have originated from Korea (7). Various types of esophagojejunostomy following laparoscopic total gastrectomy have been introduced and evaluated (8-11). However, only few studies have compared the outcomes of totally laparoscopic total gastrectomy (TLTG) and laparoscopically-assisted total gastrectomy (LATG) (12, 13). Therefore, the purpose of this study was to evaluate and compare postoperative surgical outcomes and morbidity and mortality at 30 postoperative days between TLTG and LATG, and to confirm the feasibility and safety of TLTG.
Patients and Methods
We reviewed prospectively collected data on 56 patients who underwent laparoscopic total gastrectomy with Roux-en-Y reconstruction for gastric cancer at Bucheon St. Mary's Hospital between August 2009 and January 2014. Approval for this study was obtained from the hospital's Institutional Review Board (HC 15RISI0111). Patients were divided into two groups according to the type of esophagojejunostomy. The TLTG group was defined as those patients who underwent esophagojejunostomy using a linear stapler without the need for additional incision. The LATG group was defined as those patients who underwent surgery using a circular stapler and with an additional mini-laparotomy to provide an anastomosis. Initially, the surgeon's preference was to perform LATG. After learning the laparoscopic total gastrectomy procedure, the surgeon extended the technique from LATG to include TLTG. However, later on, LATG was also performed when the tumor size was too large or splenectomy was required because of difficulty in extracting specimens through the umbilicus in these cases. The number of patients in the TLDG and LATG groups was 27 and 29, respectively.
Surgical techniques. All patients were placed supine and subjected to a 15-20° reverse Trendelenberg position. An initial 10 mm trocar for a 30° rigid electrolaparoscope was inserted through the infraumbilical area using an open technique. After establishing pneumoperitoneum with carbon dioxide, the operator stood on the patient's right side, and maintained the pneumoperitoneum at 12-15 mmHg throughout the operation. The extent of resection was decided based on the location of the primary tumor and lymph node status. Using ultrasonically activated scissors, a partial omentectomy with D1+β lymphadenectomy for early gastric cancer and a total omentectomy with either D1+β or D2 lymphadenectomy for advanced gastric cancer were performed according to treatment guidelines published by the Japanese Gastric Cancer Association. A combined splenectomy was performed, in particular, for cases of advanced gastric cancer located in the greater curvature side (14, 15). Following these procedures, esophagojejunostomy was performed using a linear or circular stapler, as described below.
Esophagojejunostomy reconstruction technique in the TLTG group. If the left crus muscle was interrupted to form the anastomosis after esophageal mobilization, it was partially transected and the esophagus was transected by a 45-mm linear stapler. After extension of the skin incision at the umbilical port site, the specimen was extracted from the abdominal cavity. A small opening was then made in the end of the esophageal stapler line to insert a linear stapler. One full-layer suture was inserted at the edge of the opening for traction and so as not to overlook the mucosa during the anastomosis. A Roux limb of the jejunum was intracorporeally prepared. The 45-mm-sized linear stapler was inserted individually between the esophagus and the prepared Roux limb and fired to form a side-to-side esophagojejunostomy. During the anastomosis, the stapler was introduced through the umbilicus, and the scope was changed to the right lower quadrant port to prevent stretching of the anastomosis. Finally, the entry hole was closed by an intracorporeal hand-sewn continuous suture. To close the entry hole, full_layer sutures were applied at both ends. To ensure that the sutures overlapped in the middle portion, continuous full-layer sutures were applied, with one of the sutures sewn up to down and the other down to up. Several reinforcement sutures were also applied. Side-to-side jejunojejunostomy was also performed intracorporeally using a linear stapler.
Esophagojejunostomy reconstruction technique in the LATG group. After esophageal mobilization, a mini-laparotomy was created in the upper midline or the left subcostal (approximately 7 cm) and a double-ring wound retractor was inserted through the incision to protect the wound from cancer spillage. The stomach was then pulled through the wound. The esophagus was transected 2 cm above the esophagogastric junction and, using an anvil holder, an anvil was inserted into the esophageal stump and a purse-string suture applied. A Roux limb of the jejunum was prepared via the wound. Finally, a 25-mm circular stapler was introduced through the Roux limb and closed to the esophageal stump. The entry hole of the jejunal stump was closed using a linear stapler, and a jejunojejunostomy was performed extracorporeally.
Outcome measurements. Surgical outcomes include operating time, anastomotic time, estimated blood loss, number of retrieved and metastatic lymph nodes, tumor-free margin, time to first flatus and oral intake, postoperative hospital stay, and duration of antibiotic use. In addition, postoperative morbidity, including anastomosis-related complications, and mortality were assessed at 30 postoperative days.
Statistical analysis. The two groups were compared using Student's t-test for continuous variables, and results are expressed as the mean±standard deviation (SD). Categorical variables were analyzed using Chi-square test. Statistical significance was inferred from p-values less than 0.05. All statistical analyses were performed with the IBM SPSS software version 20.0 (IBM Corp., Armonk, NY, USA).
Results
Clinicopathological characteristics. Of the 56 patients, 29 underwent LATG, while 27 underwent TLTG. Overall, 42 (75.0%) were male, and the mean age was 60±11.3 years. The preoperative mean body mass index was 23.8±2.7 kg/m2. Most patients presented with stage I disease (n=37; 66.1%).
In the TLTG group, the number of patients with early-stage disease was significantly higher than in the LATG group (p=0.001). In addition, the tumor size was significantly greater in the LATG group than in the TLTG group (5.1±3.5 cm vs. 2.9±1.4 cm, respectively; p=0.004). The remaining clinicopathological factors did not significantly differ between the groups (Table I).
Surgical outcomes. During surgery, the operating time, anastomotic time, and estimated blood loss were similar for the two groups. In terms of oncological outcomes, the mean number of retrieved lymph nodes was 38.3±14.2 and 45.5±20.2 in the TLTG and LATG groups, respectively, and the difference was not significant (p=0.140). The proximal margin for the TLTG group did not significantly differ from that of the LATG group (p=0.289). Recovery outcomes such as time to first flatus and oral intake, length of postoperative hospital stay, and duration of antibiotic use between the two groups also did not differ significantly (Table I).
30-Day postoperative morbidity and mortality. Postoperative complications within 30 days after surgery were observed in five (18.5%) patients in the TLTG group and five (17.2%) in the LATG group, and the difference was not significant (p=0.901). In the TLTG group, anastomosis-related complications occurred in only one case, while in the LATG group, they occurred in two cases. Anastomotic leakages were successfully treated by stent insertion in the TLTG group. In the LATG group, the condition related to anastomotic stricture was solved by supportive care and the anastomotic bleeding by transfusion. No 30-day postoperative mortality occurred in either group (Table II).
Discussion
Esophagojejunostomy is always considered problematic and technically demanding in laparoscopic total gastrectomy. Thus, various types of esophagojejunostomy have been introduced but none are standard. The most commonly studied question regarding anastomosis after laparoscopic total gastrectomy is to compare a trans-orally inserted anvil with a circular stapler (16-18). All these reports concluded that in its most recently developed form, the trans-orally inserted anvil was faster and more reliable than the circular stapler. In recent years, there have been great technical advances in anastomotic techniques for TLTG. Inaba et al. (9) introduced side-to-side anastomosis using a linear stapler (overlap) for esophagojejunostomy without the need for an extra incision, as used in our study. Besides this technique, functional end-to-end anastomosis (FEEA) using a linear stapler was also adopted in TLTG and shown to be safe compared to other techniques (11, 12). Many studies have demonstrated that the linear stapled method can be performed more safely than other methods of anastomosis, for a variety of reasons. Above all, the linear stapler is simpler and easier to handle than the circular stapler in a limited field of operation. In particular, reconstruction following LATG is difficult in situations where there is a narrow operational field, such as in obese patients. This may lead to a higher rate of anastomosis-related complications after LATG. Moreover, linear stapled anastomosis enables the surgeon to avoid torsion of the jejunal limb, tension during anastomosis, and damage to other organs. Lastly, linear stapling can create a larger anastomosis than circular stapling (19).
Although, as previously described, there have been many studies regarding laparoscopic total gastrectomy, few have compared the efficacy of TLTG and LATG. In addition, most studies regarding laparoscopic total gastrectomy have shown the outcomes of either TLTG or LATG, rather than comparing the various anastomotic methods. Therefore, the main strength of this study is that it is one of few to compare the outcomes of TLTG using a linear stapler with LATG using a circular stapler. Hiyosi et al. concluded that both FEEA with a linear stapler and a double stapling technique using a trans-orally-inserted anvil in esophagojejunostomy after laparoscopic total gastrectomy are safe and practical methods (12). The designs of that study and ours are similar. However, the studies differ in terms of technical details and results for TLTG and LATG. In our study, the direction of the end of the Roux limb in esophagojejunostomy was different from that in FEEA. In addition, the anastomotic device for LATG was a circular stapler, rather than a trans-orally inserted anvil. Moreover, in that study, TLTG had a shorter operative time and significant postoperative hospital stay.
There has been no consensus regarding the definition of LATG and TLTG because they are new procedures. Many surgeons have also confused the technique using a trans-orally inserted anvil with that of TLTG. As in our study, side-to-side anastomosis without additional laparotomy may actually be TLTG because it may not require an extra incision for anastomosis. Therefore, the second strength of this study is that it has corrected and clarified the definition and classification of TLTG and LATG. Thirdly, the present study confirms that our technique for entry-hole closure is both useful and safe. Unlike previous studies, the entry hole was closed in a continuous hand-sewn manner. To close the entry hole, full-layer sutures were applied at both ends. Then, at both ends, a continuous full-layer suture was applied individually to secure the suture line and prevent leakage from the ends of the hole. Originally, Inaba et al. performed an interrupted hand-sewn suture to close the entry hole (9). More recently, Morimoto et al. closed the hole in a similar manner (19). In contrast, Kim et al. in Korea reported the outcomes of TLTG with closure using a linear stapler (20, 21). In this study, the incidence of anastomotic stricture and leakage was between 0.7-2.9%. However, in our case, no strictures were present, even in the long-term outcomes.
Interestingly, our study revealed that the number of patients with advanced-stage disease was higher and the tumor size was significantly greater in the LATG group compared to the TLTG group. This can be attributed to our means of deciding whether to perform LATG or TLTG, as previously described. That is, the surgeon preferred to perform LATG in patients with larger and more advanced cancer because it was easier to retrieve the tumor via a mini-laparotomy. In addition, in our study, one anastomotic leakage occurred in the TLTG group. However, the differences were not statistically significant and that case was treated with intervention or supportive care, rather than re-operation.
Conclusion
The surgical outcomes of TLTG were not inferior to those of LATG. Additionally, TLTG is a technically feasible and safe procedure compared to LATG with respect to short-term surgical outcomes and complications, although there is currently no consensus on the first choice of procedure for esophagojejunostomy. Thus, a large-scale prospective randomized study is required to investigate differences not only in surgical outcomes but also in biological outcomes related to postoperative inflammatory reaction and stress. In future, TLTG should replace LATG in treatment for gastric cancer.
Footnotes
Disclosure
The Authors declare no commercial, financial, or material support for this study.
- Received January 17, 2016.
- Revision received February 23, 2016.
- Accepted February 24, 2016.
- Copyright© 2016 International Institute of Anticancer Research (Dr. John G. Delinassios), All rights reserved