| Technical requirement | Stratification |
Grade I recommendations * |
Grade II recommendations | Grade III recommendations | ||
|---|---|---|---|---|---|---|
| Lymphadenectomy recommendations a | Non‐EGJ tumors | Distal gastrectomy | D1 | Stations: 1, 3, 4sb, 4d, 5, 6, 7 a , b (Evidence 1A) | ||
| D1+ | Stations: D1 + 8a, 9 a , b (Evidence 1A) | |||||
| D2 | Stations: D1 + 8a, 9, 11p, 12a a , b (Evidence 1A) | D2 stations and station 14v a , b , * (Evidence 2A) | If tumor invaded duodenum: D2 stations + station 13 a , b (Evidence 2B) | |||
| Pylorus‐preserving gastrectomy** | D1 | Stations: 1, 3, 4sb, 4d, 6, 7 a , b (Evidence 1A) | ||||
| D1+ | Stations: D1 + 8a, 9 a , b (Evidence 1A) | |||||
|
Total gastrectomy |
D1 | Stations: 1‐7 a , b (Evidence 1A) | ||||
| D1+ | Stations: D1 + 8a, 9, 11p a , b (Evidence 1A) | |||||
| D2 | Stations: 1‐7, 8a, 9, 11, 12a a , b (Evidence 1A) | D2 stations and station 10 a , b , *** (Evidence 2A) | ||||
| EGJ tumors | Proximal gastrectomy | D1 | Stations: 1, 2, 3a, 4sa, 4sb, 7 a , b (Evidence 1A | |||
| D1+ | Stations: D1 + 8a, 9, 11p, 19 a , b (Evidence 1A) | |||||
| D2 | Stations: D1 + 8a, 9, 11, 19 (If tumor invaded esophagus >2 cm: + station 110; if tumor invaded esophagus >4cm: stations 106recR, 107, 108, 109, 111, 112) a , b (Evidence 2A | |||||
| Total gastrectomy | D1 | Stations: 1‐7 a , b (Evidence 1A) | ||||
| D1+ | Stations: D1 + 8a, 9, 11p a , b (Evidence 1A) | |||||
| D2 | Stations: 1‐7, 8a, 9, 11, 19 (If tumor invaded esophagus >2 cm: station 110; if tumor invaded esophagus >4cm: stations 106recR, 107, 108, 109, 111, 112) a , b (Evidence 2A) | |||||
| Digestive tract reconstruction c | Distal gastrectomy | Roux‐en‐Y anastomosis c (Evidence 2B) | ||||
| Pylorus‐preserving gastrectomy | Remnant gastrogastrostomy c (Evidence 2A) | ‐ | ||||
| Proximal gastrectomy | ||||||
| Digestive tract reconstruction c | Total gastrectomy | Roux‐en‐Y anastomosis c (Evidence 1A) | ||||
Abbreviations: cTNM, clinical tumor‐node‐metastasis; EGJ, esophagogastric junction.
For stage III patients in the middle and lower part of the stomach with positive subpyloric lymph nodes.
For early gastric cancer (clinical stage cT1N0M0) involving the middle 1/3 of the stomach and lesion located >4 cm from the pylorus (tumor distal margin is at least 2 cm from the distal resection margin and at least 2 cm from the pylorus)
For patients preoperatively staged as cT3 or cT4, primary tumor >6 cm, and located along the greater curvature
The lymphadenectomy procedure and extent are selected based on TNM staging and overall treatment strategy
Notes
Resection extent and lymphadenectomy
The extent of gastrectomy is based on the location of the tumor, with the aim to ensure adequate surgical resection margin. For T1 early gastric cancer, the gross margin should be >2 cm. Based on data from recent studies [42, 43], the recommendations for an adequate distance of resection margin for >T2 Borrmann I‐II gastric cancers is ≥3 cm, and for Borrmann III‐IV is ≥5 cm. If the tumor has invaded the esophagus or pylorus, a resection margin of 5 cm is not obligatory as long as R0 resection and negative margins on frozen pathological examinations can be assured.
Based on the findings of the JCOG9502 study [44], for EGJ adenocarcinoma, which has invaded <3 cm into the esophagus or the body of the stomach, abdominal (non‐endoscopic) surgery is recommended. Transthoracic surgery is not recommended. For EGJ tumors, the choice between total gastrectomy and proximal gastrectomy primarily depends on the lesion extent, lymph node metastasis at stations 4, 5 and 6, and the patient's survival outcomes. A prospective study [45] by the Japan Gastric Cancer Association and the Japan Esophageal Society across 42 centers on patients with cT2‐cT4 adenocarcinoma or squamous cell carcinoma of the EGJ for assessing lymph node metastasis rates found that for tumors with a diameter ≤4 cm, the rates of metastasis at station 4d, 5 and 6 were 2.2%, 1.1% and 1.7%, respectively, and for tumors with a diameter ≥6 cm, the rates of metastasis at station 4d, 5 and 6 ranged from 6% to 10.7%. However, no long‐term survival data for these cases were reported [45]. Therefore, the CSCO Expert Committee considered that for EGJ cancer of ≤ 4 cm diameter, with no station 4d, 5 or 6 lymph node metastasis by imaging assessments, proximal gastrectomy may be considered, with the stipulation that at least half of the distal stomach should be preserved.
The resection of perigastric lymph nodes and those alongside accompanying vessels of the celiac trunk should be performed according to the type of gastrectomy [42, 43]. D1 gastrectomy includes the resection of the required part of the stomach (with adequate resection margin), greater and lesser omentum, and the following perigastric lymph nodes: the right and left para‐cardiac lymph nodes, lesser and greater curvature lymph nodes, lymph nodes along the left gastric artery, suprapyloric, and infrapyloric lymph nodes along the right gastric artery. D2 gastrectomy includes the structures resected in D1 gastrectomy and the resection of the lymph nodes along the common hepatic artery, gastroduodenal ligament and splenic artery. Based on the Dutch study [46], for resectable cT2‐4 and cT1N+ cases, D2 lymphadenectomy is recommended as it has been shown to be superior in decreasing the risk of recurrence and gastric‐related death compared to D1 lymphadenectomy. It is recommended that ≥16 lymph nodes should be pathologically examined to ensure accurate staging and prognostication.
Currently, there is still controversy regarding the necessity for splenic hilar lymph node dissection. A phase III clinical study conducted at a single center in China revealed that for tumors located in the proximal stomach without involvement of the greater curvature, the addition of laparoscopic splenic hilar lymphadenectomy to D2 lymphadenectomy does not result in a survival benefit [47]. However, for tumors with advanced TNM stage, size >6 cm, and located at the greater curvature of the stomach, the probability of splenic hilar lymph node metastasis is high [48]. The Expert Committee recommends that splenic hilar lymph node dissection should be performed in the following cases: the primary tumor is >6 cm, the tumor is located at the middle‐upper part of the stomach along the greater curvature and preoperatively staged as cT3‐4 [49, 50]. Splenectomy for lymph node dissection is not recommended.
Whether it is necessary to dissect lymph nodes at the root of the superior mesenteric vein (station 14v) in advanced gastric cancer remains controversial. Although station 14v is not within the routine extent of D2 lymphadenectomy in the 3rd edition of the Japanese Gastric Cancer Treatment Guidelines [51], it has been observed that D2 lymphadenectomy with station 14v lymph node dissection may improve overall survival (OS) in patients with clinically staged III/IV middle‐ and lower‐third gastric cancer. Retrospective studies showed that the rate of metastasis to station 14v in distal gastric cancer was 18.3%‐19.7%, while the metastasis rate of stage I distal gastric cancer patients was 0, and that of stage II distal gastric cancer patients was 1.6% [52, 53]. D2 lymphadenectomy with resection of station 14v lymph nodes may improve the OS of stage cIII/IV middle and lower gastric cancer patients [54]. Therefore, the Expert Committee recommends the following indications for the dissection of station 14v lymph nodes: clinically staged III patients with tumors located at the middle and lower parts of the stomach, especially for those with metastasis to the infra‐pyloric lymph nodes.
Although the station 13 (retro‐pancreatic) lymph nodes are not within the routine extent of D2 dissection, studies have found that for advanced lower gastric cancer, the metastasis rate to station 13 was 2.5%‐9.0%, and if the tumor has invaded the duodenum, the metastasis rate is even higher, at 26.7% [55, 56, 57]. In terms of survival outcome, for patients with stage cI/II disease, the dissection of station 13 does not improve OS, while for stage cIII/IV patients, it can improve OS. For patients with duodenal invasion and stage cIII disease, dissection of station 13 can be considered, but this population is often accompanied by a low R0 resection rate. Therefore, neoadjuvant therapy combined with D2 lymphadenectomy and station 13 dissection can be considered for such patients.
In EGJ tumors, particularly in regard to mediastinal lymphadenectomy, a consensus on the optimal extent of lymphadenectomy remains unclear. A multicenter prospective study in Japan assessing the lymph node metastasis rates of cT2c‐T4 patients with EJC adenocarcinoma and squamous cell carcinoma revealed that different lengths of esophageal infiltration were associated with varying lymph node metastasis rates [45]. When esophageal infiltration was ≤2 cm, mediastinal lymph node metastasis was less frequent. However, for esophageal infiltrations >2 cm but ≤4 cm, lower mediastinal lymph nodes (station 110) exhibited higher metastasis rates, whereas upper and middle mediastinal lymph nodes had lower metastatic rates. Comparatively, in cases where the tumor had esophageal infiltrated >4 cm of the EGJ, upper and middle mediastinal lymph node metastasis rates were increased. Based on these findings, the CSCO Expert Committee recommends dissecting station 110 in lymph nodes when esophageal infiltration exceeds 2 cm. Furthermore, if infiltration exceeds 4 cm, dissection should extend to encompass the 106recR, 107, 108, 109, 111 and 112 stations lymph nodes.
For patients with resectable advanced gastric cancer, it has been reported that preventive para‐aortic lymph node dissection was not associated with improved long‐term survival of these patients [58], and the value of therapeutic para‐aortic lymph node dissection is still controversial. Suitable patients should be encouraged to participate in clinical trials.
Regarding the utility of postoperative abdominal lavage in curative surgery for gastric cancer, findings from the 2021 EXPEL study indicate that postoperative abdominal lavage following standard D2 surgery did not reduce the risk of peritoneal recurrence (7.9% vs. 6.6%, hazard ratio [HR]: 1.33; 95% confidence interval [CI]: 0.73‐2.42; P = 0.347) but instead increased the risks of adverse events (relative risk: 1.58; 95% CI: 1.07‐2.33; P = 0.019) [59]. Consequently, the Expert Committee does not recommend the use of extensive abdominal lavage following radical gastrectomy.
Laparoscopic and robotic surgery
For distal gastrectomy of gastric cancer classified as cT1N0 and cT1N1, large‐scale prospective studies from Japan and Korea, JCOG0912 [60] and KLASS‐01 [61], have shown that laparoscopic surgery was equivalent to open surgery in terms of safety and long‐term prognosis. Therefore, laparoscopic surgery is recommended as a routine surgical technique.
There is no large prospective study for laparoscopy‐assisted total and proximal gastrectomy (LATG and LAPG) of early gastric cancer. Although preliminary evidence from China's CLASS02 [64], South Korea's KLASS‐03 [62] and Japan's JCOG1401 [63] studies confirmed the safety of LATG/LAPG, there is currently no long‐term efficacy data available. Therefore, the Expert Committee recommends further investigations of such cases in experienced medical centers.
For advanced gastric cancer, the CLASS‐01 [65] and KLASS‐02 [66] phase III randomized controlled trials confirmed that LADG combined with D2 lymph node dissection was safe when performed by experienced surgeons in high‐volume medical centers. It was associated with reduced blood loss, faster gastrointestinal recovery, shorter hospital stays, and similar long‐term survival compared to open surgery.
Whether laparoscopic gastrectomy is feasible for patients with advanced gastric cancer after neoadjuvant therapy is still controversial. Currently, there is a lack of large cohort prospective studies. The recent results of a Chinese randomized controlled study comparing the safety of LADG with D2 lymphadenectomy against open distal gastrectomy (ODG) with D2 lymphadenectomy in locally advanced gastric cancer (cT2‐4aN+M0) patients who received neoadjuvant chemotherapy, showed that LADG was associated with better postoperative safety and adjuvant chemotherapy tolerance compared than ODG [67].
Therefore, the Expert Committee suggests that for patients with stage I‐III gastric cancer who are suitable for distal subtotal gastrectomy, laparoscopic surgery can be routinely performed. LATG for early gastric cancer can be performed in experienced medical centers as clinical investigations. However, there is no evidence for the benefit or superiority of proximal and LATG for advanced gastric cancer, and the results of clinical studies are awaited. Further, whether laparoscopic surgery can be performed for advanced gastric cancer after neoadjuvant therapy still urges more prospective clinical confirmations.
Further, robotic gastric cancer surgery has attracted much attention in recent years. Although there is no large prospective study to confirm its efficacy in the treatment of gastric cancer, a retrospective study from Korea that compared robotic gastric cancer surgery (n = 421) with open/laparoscopic surgery (n = 1663) [68] showed that although there was no difference in long‐term survival between the study groups, patients from the robotic group had a lower risk of intra‐operative bleeding. A retrospective analysis from 7 major centers in China showed that robot‐assisted surgery was associated with lower complication rates, lesser bleeding, a more extensive lymph node dissection, and equivalent long‐term survival compared to laparoscopic surgery [69]. Furthermore, two randomized controlled clinical studies in China comparing robot‐assisted distal gastrectomy (RADG) with LADG demonstrated that RADG resulted in fewer postoperative complications and led to more extensive resection of perigastric lymph nodes [70, 71]. Currently, the Expert Committee considers that the advantages and significance of robotic gastric cancer surgery still need further confirmatory evidence before wide clinical application.
According to the Expert Committee, for stage cIII patients, laparoscopic exploration should be performed, and the 3‐incision method should be applied. Peritoneal metastasis should be evaluated. For complete exploration, it is recommended to open the gastrocolic ligament and observe whether there is occult metastasis in the omentum. If peritoneal metastasis is detected, HER2 and MMR status detection in the metastatic lesion should be performed to guide the treatment. If no obvious peritoneal metastasis is found, cytological examination of peritoneal lavage fluid should be performed.
Digestive tract reconstruction
The type of digestive tract reconstruction performed depends on the patient's physical condition and the surgeon's experience as far as it does not affect the radicality of the gastrectomy.
Billroth I and Billroth II reconstructions are mostly adopted for distal gastrectomy. The postoperative complication rates for both reconstructions are similar. However, Billroth I is easier to perform and better suits the normal physiological gastrointestinal pathway. For tumors located in the lower third of the stomach, especially those invading the pylorus and the duodenum, Billroth II reconstruction is recommended because these patients can have a second chance for surgery in case of tumor recurrence [72]. Compared with Billroth type I and II, Roux‐en‐Y anastomosis can effectively reduce bile reflux and prevent the occurrence of remnant gastritis. However, this operation is relatively complex, and the risk of postoperative retention syndrome may be increased [73].
Although proximal gastrectomy preserves some functions of the stomach, it disrupts the cardia's anti‐reflux mechanism and delays gastric emptying. Therefore, digestive tract reconstruction after proximal gastrectomy should aim to minimize the occurrence of reflux esophagitis. While esophagogastrostomy can be considered a simpler and quicker procedure with fewer anastomoses and lower risks of short‐term complication rates, it can be associated with common and severe gastroesophageal reflux [74]. Researchers indicated that the likelihood of severe gastroesophageal reflux after surgery significantly decreases with double‐tract reconstruction, modified tubular stomach‐esophagus anastomosis, and modified esophagogastrostomy [75, 76, 77]. Compared with gastroesophageal anastomosis, the Jejunal interposition procedure can reduce the occurrence of moderate or severe esophageal reflux, but this operation is complex and abdominal discomfort, upper abdominal fullness, and hiccups are commonly observed in these cases [78]. Therefore, its advantages remain to be confirmed, and if required, it is suggested that the Jejunal interposition method is recommended to be performed in large experienced medical centers. Therefore, there is no recognized optimal digestive tract reconstruction, and the Expert Committee recommends large medical centers to conduct randomized controlled trials to explore the optimal digestive tract reconstruction.
Roux‐en‐Y is the preferred reconstruction procedure for total gastrectomy [43]. It has been reported that, in addition to Roux‐en‐Y anastomosis, the reconstruction of the Jejunal pouch digestive tract may improve the patients’ postoperative quality of life, which is mainly reflected in the increase of food intake and the decrease of digestive tract symptoms [79]. However, the Jejunal interposition technique is complicated and may be associated with a high risk of postoperative complications, and controversies concerning its efficacy in improving the patients’ quality of life exist. Therefore, if required, it is suggested that this procedure should be carried out in large experienced medical centers.