This retrospective study involved 221 consecutive patients with gastric cancer treated in the Department of Minimally Invasive Gastrointestinal Surgery, Peking University Cancer Hospital, between January 2007 and February 2011. The exclusion criteria included: (1) invasion of adjacent structures; (2) conglomeration of lymph nodes and no R0 resection; (3) distant metastases; and (4) absence of consent signing before operation. Blood tests, chest X-rays, enhanced computed tomography scans of the abdomen and pelvis, double-contrast upper gastrointestinal X-ray studies, and gastric endoscopy were performed before operation. All tumors were diagnosed as adenocarcinomas by biopsy. Informed consent was signed prior to surgery from each case. Among the 221 patients, 12 were excluded: 7 could not undergo R0 resection (3 with tumor invasion of adjacent structures, 4 with conglomeration of lymph nodes), 4 had distant metastases, and 1 refused operation. The study population thus included 209 cases that successfully underwent radical gastrectomy with D2 dissection. One hundred and thirty-one cases received LAG (LAG group) and 78 cases received open gastrectomy (OG group). All operations were performed by the same surgical team.

General anesthesia was administered with epidural analgesia to all the patients. The patients were placed in the supine position with legs apart. A 12-mm trocar for laparoscopy was introduced using the open technique below the umbilicus, and pneumoperitoneum at 10-13 mmHg was induced with carbon dioxide. Another 12-mm trocar was inserted at the left preaxillary line, 2 cm below the costal margin, to serve as a major hand port. Then a 5-mm trocar was placed at the left midclavicular line parallel to the umbilicus, and another 5-mm trocar was inserted at the contralateral site as an accessory port. The last 5-mm trocar was then placed at the right preaxillary line, 2 cm below the costal margin, also serving as another accessory port. The operator stood on the left side of the patient. The first assistant stood on the patient’s right. The camera assistant stood between the patient’s legs.

According to the guidelines of the Japanese Gastric Cancer Association (JGCA), the stomach was divided anatomically into three portions: upper, middle, and lower. The three portions were defined by subdividing both the lesser and greater curvatures into three equal lengths[20]. The type of gastrectomy and extent of D2 dissection were determined by tumor location (Figure 1)[20]. The aim of any oncological resection was to achieve en-bloc resection of gastric segment and surrounding lymph nodes, in order to obtain adequate oncological clearance.

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Figure 1 Lymph node stations of the stomach. The groups of lymph node in red, green and blue should be dissected in radical total gastrectomy; the groups of lymph node in red and green should be dissected in radical proximal gastrectomy; the groups of lymph node in red and blue should be dissected in radical distal gastrectomy.

Laparoscopy-assisted radical total gastrectomy with D2 dissection: This procedure was performed for gastric cancer involving more than 2/3 of the stomach. The greater omentum was first dissected, using the ultrasonicactivated scissors (Ultracision-Harmonic Scalpel; Ethicon Endo-Surgery Inc, Cincinnati, OH, United States), along the border of the transverse colon. The left gastroepiploic vessel was vascularized, clamped with double Hem-o-lok clips (Teleflex Medical RTP, NC, United States) and cut at its origin. The gastrosplenic ligament was then divided and resected along the edge of spleen. These processes allowed the removal of No. 4sb, 4sa, and 10 lymph nodes. Then removal of No. 2 lymph nodes was performed. The next step was to resect the superior leaf of the mesocolon and the anterior leaf of the pancreas rightward the pylorus. The superior mesenteric vein, the Henle’s trunk, the right colic vein, and the right gastroepiploic vessel were exposed allowing dissection of No. 14v lymph nodes. Then the right gastroepiploic vessel was clamped at its origin using double Hem-o-lok clips and cut, allowing No. 6 and 4d lymph nodes to be removed. In order to expose the gastropancreatic fold, the stomach was turned headward with the greater omentum folded up on the anterior aspect of the stomach. Along the gastroduodenal artery, the common hepatic artery could be skeletonized easily. The right gastric artery was divided and cut at its origin, using double Hem-o-lok clips, from the proper hepatic artery. Then dissection of No. 8a and 5 lymph nodes was completed. Once No. 8a lymph nodes were dissected, the procedure was continued leftward along the artery in order to remove the lymph nodes located along the celiac trunk (No. 9) and the left gastric artery (No. 7). The left gastric artery was cut from the celiac trunk using triple Hem-o-lok clips. Afterward, the celiac trunk was skeletonized. So, No. 7 and 9 lymph nodes were dissected. Then the splenic artery was skeletonized from its origin to the end in order to remove No. 11 lymph nodes. After returning the stomach and the greater omentum to normal position, the lesser omentum could be resected along the liver edge to the esophagogastric junction, with dissection of No. 1 and 3 lymph nodes. The last step of lymph node dissection was to skeletonize the proper hepatic artery, so No. 12a lymph nodes could be dissected. After standard D2 dissection was completed, an upper midline incision (about 5 cm) was made. The gastrectomy was performed and gastrointestinal continuity was restored in a Roux-en-Y fashion though this incision.

Laparoscopy-assisted radical proximal gastrectomy with D2 dissection: This procedure was performed for lesions located in the upper third of the stomach. The standard D2 dissection, including No. 1, 2, 3, 4, 7, 8a, 9, 10 and 11, was conducted using the same procedure described above. Esophagogastric anastomosis was performed to rebuild gastrointestinal continuity.

Laparoscopy-assisted radical distal gastrectomy with D2 dissection: This procedure was performed for lesions located in the lower third of stomach with or without involving the middle third of the stomach. The standard D2 dissection, including No. 1, 3, 4sb, 4d, 5, 6, 7, 8a, 9, 11p, 12a, and 14v, was conducted using the same procedure described above. Gastroduodenal anastomosis (Billroth I) or gastrojejunal anastomosis (Billroth II) was performed to rebuild gastrointestinal continuity.

Conventional open operation: The premedication and anesthetic techniques used were similar to the LAG group. Patients lay in the supine position, and the operator stood on the right side of the patient. An upper midline incision (about 20 cm) was made, and a standard gastrectomy with D2 dissection and reconstruction were performed in the same manner as in LAG.

Nasogastric tube and nasojejunal tube were inserted routinely in operation. Enteral nutrition started through nasojejunal tube on the first postoperative day (POD). Gastroenterography, with the use of compound meglumine diatrizoate, was performed routinely to observe anastomosis on the 7th POD. If there was no evidence of anastomotic leakage by gastroenterography, the nasogastric tube could be removed and liquid diet was taken on the 8th POD.

During surgery, operative time, blood loss (estimated by the volume of suction and the weight of gauze), and the amount of blood transfusion were recorded. Postoperative complications, categorized as surgical and nonsurgical complications, occurred during the hospital stay, and included fluid or abscesses needing drainage, intra-abdominal or anastomotic bleeding needing transfusion or reoperation, ileus, delayed gastric emptying, lymphatic leakage, and anastomotic leakage. Nonsurgical complications included cardiac, pulmonary, urinary, renal and hepatic complications. Mortality was defined as any death that occurred during hospital stay. The depth of tumor invasion, tumor size, margins, the number of harvested lymph nodes (HLNs), and positive lymph nodes were determined by pathological analysis. Histological staging was classified according to the 7th edition of the American Joint Committee on Cancer Staging Manual.

The data of patient’s age, operation time, blood loss, and the number of lymph nodes were presented as χ± s. Differences were compared in sex, type of resection, stage, and complications between the two groups using Chi-square test. Independent-sample t test was used to estimate differences in age, operation time, blood loss, and the number of HLNs between the two groups. P values less than 0.05 were considered statistically significant. All statistical analyses were performed with SPSS software, version 11.0 (SPSS Inc, Chicago, United States).

Demographic details of the two groups are shown in Table 1. There were 88 males and 43 females in the LAG group, and the mean age of patients was 59.5 (range, 26-80) years. The OG group included 52 males and 26 females, with a mean age of 60.6 (range, 33-79) years. There were no significant differences in sex and age between the two groups (P = 0.940 and 0.523, respectively). Compared with the OG group, the LAG group had a significantly less blood loss (111.1 ± 83.7 mL in LAG vs 230.1 ± 96.8 mL in OG, P < 0.001), and a longer operation time (259.1 ± 58.6 min in LAG vs 213.9 ± 37.6 min in OG, P < 0.001). No blood transfusion was administered during surgery in either group.

Radical proximal gastrectomy with D2 dissection (PG + D2) was performed in 50 cases (33 in LAG and 17 in OG), radical distal gastrectomy with D2 dissection (DG + D2) in 104 cases (64 in LAG and 40 in OG), and radical total gastrectomy with D2 dissection (TG + D2) in 55 cases (34 in LAG and 21 in OG). There were no significant differences in the type of radical resection between the two groups (P = 0.856). Tumor free margins were obtained in all the patients. In the LAG group, there were 29 cases in stage I, 28 cases in stage II, and 74 cases in stage III. In the OG group, there were 12 cases in stage I, 13 cases in stage II, and 53 cases in stage III. There were no significant differences in pathological stages between the two groups (P = 0.253).

Details of the number of HLNs are shown in Tables 2 and 3. In the LAG and OG groups, 127 (96.9%) cases and 76 cases (97.4%) had 15 or more HLNs. The average number of HLNs was 26.1 ± 11.4 in the LAG group and 24.2 ± 9.3 in the OG group (P = 0.233). The number of HLNs was 21.9 ± 8.1 in PG + D2, 24.4 ± 10.0 in DG + D2, and 30.3 ± 12.3 in TG + D2 (P < 0.001) (Table 2). In the same type of resection, there was no significant difference in the number of HLNs between the LAG and OG groups (PG + D2: 21.7 ± 7.5 in LAG vs 22.4 ± 9.3 in OG, DG + D2: 25.7 ± 11.0 in LAG vs 22.3 ± 7.9 in OG, TG + D2: 30.9 ± 13.4 in LAG vs 29.3 ± 10.4 in OG). P value was 0.770, 0.091 and 0.653, respectively (Table 3).

Postoperative complications are listed in Table 4. Delayed gastric emptying (n = 5), lymphatic leakage (n = 3), anastomotic leakage without reoperation (n = 2), large pleural effusion needed drainage (n = 1), anastomotic bleeding needed transfusion (n = 1), and acute myocardial infarction (n = 1) occurred in the LAG group. Postoperative complications in the OG group included delayed gastric emptying (n = 3), lymphatic leakage (n = 2), and anastomotic leakage without reoperation (n = 1). There were no significant differences in the morbidity between the two groups (9.9% vs 7.7%, P = 0.587). Mortality was zero in both groups.

Gastric cancer is one of the leading fatal malignancies worldwide, particularly in China and other Far Eastern countries. Laparoscopic surgery is a minimally invasive operation, which can be performed in colorectal cancer, and has been proved by many randomized control trials (RCTs). However, few studies have evaluated the role of laparoscopy-assisted gastrectomy (LAG) in gastric cancer.

Several RCTs have shown that LAG can be performed in early gastric cancer. However, LAG for the treatment of advanced gastric cancer (AGC) has remained controversial. This is mainly due to a lack of evidence from large-scale studies showing that laparoscopic D2 dissection, the standard lymphadenectomy for AGC, is equivalent in outcome to open surgery.

In recent years, some studies have analyzed D2 dissection in LAG and open surgery for gastric cancer. Although the range of lymph node involvement differs by tumor location, making the extent of D2 dissection differ as well, little effort has been made to distinguish between tumors in various locations, with all simply being regarded as “gastric cancer” or just evaluated as one type of LAG. Thus, this study evaluated the overall radicalness of laparoscopic D2 dissection in gastric cancer, and further compared the difference among distal gastrectomy, proximal gastrectomy, and total gastrectomy.

This paper confirms the equivalent radicalness of D2 dissection between LAG and open surgery, thus providing preliminary evidence of the feasibility of applying LAG in gastric cancer, even in AGC. Long-term outcomes of LAG should be further studied.

D2 dissection is the standard lymphadenectomy for AGC. The regional lymph nodes of the stomach are classified into three groups according to the guidelines of the Japanese Gastric Cancer Association. D2 dissection includes dissection of all Group 1 and Group 2 nodes. The extent of D2 dissection is different due to different tumor locations.

The paper can be accepted for publication. The authors compared the radicalness of gastrectomy by laparoscopic and open approaches.