Short- and long-term outcomes after laparoscopic versus open total gastrectomy for stage 0–I gastric cancer: a multicenter, retrospective analysis

Introduction

Background

With the mastery of laparoscopic surgery by abdominal surgeons, laparoscopic surgery is increasingly used in gastric cancer surgery. The safety and efficacy of laparoscopic distal gastrectomy have been demonstrated in early gastric cancer (JCOG0912, KLASS01, CLASS02) (1-3) and advanced gastric cancer (CLASS01) (4). Laparoscopic gastric cancer surgery has the advantages of less trauma, faster postoperative recovery, and long-term survival that is comparable to that of open surgery. Due to the increased incidence of adenocarcinoma of the esophagogastric junction (5,6) and the increased proportion of total gastrectomy in gastric cancer (7), the proportion of total gastrectomy in gastric cancer surgery is also relatively increased, and laparoscopic total gastrectomy (LTG) is attracting increasing attention.

The indications for LTG are similar to those of traditional open surgery and are mainly determined by the location and range of the tumor, including adenocarcinoma of the esophagogastric junction and gastric body cancer. Due to its minimal invasiveness, fast postoperative recovery, and reduced postoperative pain, LTG is widely used in gastric cancer surgery. However, open total gastrectomy (OTG) is preferred over LTG in cases of larger tumors, potential infiltration of the tumor into surrounding organs, and patients who are intolerant to pneumoperitoneum. The surgical resection range of LTG for early gastric cancer includes the whole stomach, lower esophagus and duodenal bulb. The supply vessels of the stomach are abundant, the anatomical level and the route of lymph node metastasis are complex, and the technical difficulties of laparoscopic digestive tract reconstruction are difficult; therefore, the safety and efficacy of LTG need to be further evaluated (8). In recent years, there have been some reports comparing LTG to OTG, suggesting that the long-term survival of LTG in the treatment of early and advanced gastric cancer is comparable to that of traditional OTG (9-12). However, the difference between LTG and OTG in the incidence of complications is still controversial (13-16). Because LTG is still in its exploratory phase, the number of cases studied is generally low. Therefore, we designed this multicenter, large-sample study for stage 0–I gastric cancer to compare short-term surgical outcomes and long-term survival between LTG and OTG. We present this article in accordance with the STROBE reporting checklist (available at https://cco.amegroups.com/article/view/10.21037/cco-2025-aw-152/rc).

Methods

Patients

In this study, we retrospectively collected the clinicopathological data of patients with early gastric cancer who underwent radical total gastrectomy in Guangdong Provincial People’s Hospital, Fujian Provincial Cancer Hospital and Guangdong Provincial Hospital of Chinese Medicine from January 2010 to December 2013. These three large research centers have strong research foundations and consistent surgical techniques to minimize surgical variations as much as possible. The inclusion criteria were as follows: (I) pathological diagnosis of gastric cancer; (II) TNM stage 0–I (TNM 8th); (III) LTG or open total gastrectomy (OTG); (IV) complete clinicopathological data; and (V) follow-up data. The exclusion criteria were as follows: (I) gastric adenocarcinoma without pathological diagnosis; (II) other TNM stages; (III) preoperative chemoradiotherapy; (IV) no radical total gastrectomy; and (V) unwillingness or inability to participate in the follow-up.

Operation and complication evaluation

Total gastrectomy and lymph node dissection were performed by surgeons with extensive experience in gastric cancer surgery at each center. According to the Japanese guidelines for gastric cancer treatment, total gastrectomy combined with D1+/D2 lymph node dissection is performed. Intraoperatively, routine frozen section analysis is conducted on the proximal margin to confirm negative margins. In the LTG group, the laparoscopic procedure includes gastric devascularization, lymph node dissection, and vascular ligation. Gastrectomy and gastrointestinal reconstruction can be achieved through a small abdominal incision of no more than 10 centimeters, and the choice of reconstruction method depends on each surgeon’s preference. The surgical procedure in the OTG group is similar to laparoscopic surgery, except that it is performed under direct visualization. Postoperative complications were assessed according to postoperative laboratory examination, imaging examination and other examinations, and the severity of postoperative complications was classified according to the Clavien-Dindo grading system (17). According to previous reports, incision infection, postoperative intestinal obstruction, abdominal hemorrhage and lymphatic fistula have a high incidence in OTG (18-20); therefore, we defined them as OTG-related complications. Similarly, we defined complications with a higher incidence in LTG as LTG-related complications, including anastomotic leakage, anastomotic bleeding and anastomotic stenosis (18,19,21). All patients were informed of the advantages and disadvantages of LTG versus OTG and the possible complications. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Guangdong Provincial People's Hospital (approval No. KY-Q-2021-309-02). and informed consent was obtained from all individual participants. The other hospitals were informed of and agreed on the study.

Follow-up

Patients were followed up regularly by professionals via telephone, communication software and outpatient services once every 3 months in the first 2 years, once every 6 months in the third to fifth years, and once every year after 5 years. All patients were followed up for at least 5 years. Survival time was defined as the time from surgery to death or the last follow-up in January 2019. Patients with incomplete follow-up data have been excluded from this study.

Statistics analysis

The statistical analysis was performed using SPSS software, version 25.0 (SPSS, Chicago, IL, USA) and R, version 3.5.1 (R Core Team 2019, Vienna, Austria). Continuous variables are expressed as the mean ± SD, and categorical variables are reported as frequencies with percentages. Student’s t-test or the Mann-Whitney test was used for intergroup comparisons of continuous variables, whereas the χ² test or Fisher’s test was used to compare categorical data.

To assess the risk of overall complications, LTG-related complications, and OTG-related complications, we conducted a “global” multivariate analysis (22), which is also known as multivariate regression with a generalized estimation equation (GEE). In survival analysis, to reduce selection bias, we adjusted the characteristics of the LTG and OTG groups by using inverse probability of treatment weighting (IPTW). Baseline variable adjustments included age, sex, BMI, tumor location, TNM staging, pathological T stage, pathological N staging, the degree of differentiation, and histology type. The Kaplan-Meier curves before and after IPTW adjustment were used to compare the overall survival rate of the two groups.

All of the analyses were performed with the statistical software package R (http://www.R-project.org, The R Foundation) and EmpowerStats (http://www.empowerstats.com, X&Y Solutions, Inc., Boston, MA). P values less than 0.05 (two-sided) were considered statistically significant.

Results

Baseline characteristics

In this study, we retrospectively collected the clinicopathological data of patients with early gastric cancer who underwent radical total gastrectomy in Guangdong Provincial People’s Hospital, Fujian Provincial Cancer Hospital and Guangdong Provincial Hospital of Chinese Medicine from January 2010 to December 2013. A total of 122 patients were included. As shown in Figure 1, of the 122 patients included in the study, 73 (59.8%) received LTG, and 49 (40.1%) received OTG. The clinicopathological features of the two groups are shown in Table 1. There was a significant difference in tumor differentiation between the two groups (P<0.05), and patients in the LTG group had lower differentiation. There was no significant difference in age, sex, BMI, tumor location, tumor size, TNM stage, pathological T stage, pathological N stage or histological type between the two groups (P>0.05). After IPTW adjustment, there was no significant difference between the two groups (P>0.05).

Figure 1 Study flowchart.

Surgical results

The surgical results of the two groups are shown in Table 2. Compared to the OTG group, LTG had a longer surgical time (262.78±87.45 vs. 190.51±37.11 min; P<0.001), less intraoperative blood loss (112.66±95.75 vs. 178.16±86.09 mL; P<0.001) and a shorter postoperative exhaust time (3.30±0.98 vs. 3.67±0.83 days; P<0.05). There were no statistically significant differences in the number of lymph nodes resected, number of positive lymph nodes, postoperative defecation time, fluid feeding time, semifluid feeding time or postoperative hospital stay between the two groups (P>0.05).

Postoperative complications of the LTG group and the OTG group

The comparison of postoperative complications is shown in Table 3. The incidence of overall postoperative complications was 16.4% in the LTG group and 18.4% in the OTG group, with no statistically significant difference between the two groups (P>0.05) and no statistically significant difference in the CD grade. Compared to the LTG group, the OTG group had a higher incidence of incision infection, postoperative intestinal obstruction, abdominal hemorrhage and lymphatic fistula, but there was no statistically significant difference between the two groups (P>0.05). Compared to the OTG group, the incidence of anastomotic leakage, anastomotic bleeding and anastomotic stenosis was higher in the LTG group, but the difference between the two groups was not statistically significant (P>0.05). In the multivariate regression with a GEE for OTG-related complications as shown in Table 4, in the unadjusted model, the difference between the groups was nearly statistically significant (P=0.06), and the risk of OTG-related complications in the LTG group was 0.131 [95% confidence interval (CI): 0.016–1.10]. After adjustment for age, sex, BMI, pathological T stage and pathological N stage, the difference was statistically significant (P=0.03), and the risk of OTG-related complications in the LTG group was 0.111 (95% CI: 0.016–0.771). In the model for overall complications, in the unadjusted and adjusted models, the risk of complications in the LTG group was 0.802 (95% CI: 0.34–1.91) and 0.703 (95% CI: 0.33–1.49), respectively, compared with the OTG group, but the difference was not statistically significant (P>0.05). In the model for LTG-related complications, the risk of LTG-related complications in the LTG group was 2.73 (95% CI: 0.31–24.28) and 2.78 (95% CI: 0.44–17.68) in the unadjusted and adjusted models, respectively, and the difference was not statistically significant (P>0.05).

Survival analysis

The median follow-up time was 76 months in the LTG group and 81 months in the OTG group. The 3-year and 5-year survival rates were 95.9% and 90.4% in the LTG group and 95.9% and 83.7% in the OTG group, respectively. There was no statistically significant difference between the two groups (P=0.28), as shown in Figure 2. After IPTW adjustment for age, sex, BMI, tumor location, TNM stage, pathological T stage, pathological N stage, differentiation degree and histological type, there was no statistically significant difference in survival between the LTG group and the OTG group (P=0.34).

Figure 2 Unadjusted and IPTW-adjusted K-M analysis of OS between the LTG group and the OTG group. (A) Unadjusted K-M curves for OS. (B) IPTW-adjusted K-M curves for OS. IPTW, inverse probability of treatment weighting; K-M, Kaplan-Meier; LTG, laparoscopic total gastrectomy; OS, overall survival; OTG, open total gastrectomy.

Discussion

In recent years, gastrointestinal surgeons have begun to explore the long-term survival and short-term results of LTG versus OTG (9,10,23,24). Since LTG and studies of its safety and efficacy are still in the exploratory stage, Lombardi et al. have previously conducted an analysis on the survival outcomes of patients with advanced gastric cancer who underwent curative laparoscopic or open gastrectomy. Ultimately, it was found that laparoscopic gastrectomy for advanced gastric cancer provides similar survival rates compared to open gastrectomy (9,10,25,26). But few studies have been reported on its outcomes in stage 0–I gastric cancer. In our study, we compared the short-term outcomes and long-term survival of LTG with traditional OTG for stage 0–I gastric cancer.

In our study, LTG required a longer operative time than OTG (262.78±87.45 vs. 190.51±37.11 min; P<0.001), which was consistent with previous studies (10,27). This may be due to technical reasons, for example, because lymph node resection and digestive tract reconstruction in LTG takes a long time (10). In addition, the intraoperative blood loss of LTG is less than that of OTG, and more operation time may be needed for more adequate hemostasis. In terms of postoperative recovery, postoperative exhaust time was shorter in LTG than in OTG (P<0.05), but postoperative defecation time, fluid and semifluid feeding time, and postoperative hospital stay were not significantly different between the two groups.

Postoperative complications are one of the major concerns of LTG. Postoperative complications are a major concern when comparing LTG with OTG. In this study, complications were classified using the Clavien-Dindo system, and no significant difference was observed in the distribution of complication severity between the two groups, indicating comparable overall safety. However, the characteristics of complications differed between surgical approaches. OTG was more frequently associated with incision-related and procedure-related complications, such as incision infection, postoperative ileus, intra-abdominal hemorrhage, and lymphatic fistula, likely due to greater surgical trauma. In contrast, LTG showed a higher proportion of anastomosis-related complications, reflecting the technical complexity of laparoscopic esophagojejunal reconstruction. Further analysis using a GEE model demonstrated that LTG significantly reduced the risk of OTG-related complications without increasing the risk of LTG-related complications. These findings suggest that LTG alters the pattern rather than the severity of postoperative complications. In our study, the overall complication rate of the OTG group was higher than that of the LTG group (18.4% vs. 16.45%), which was similar to previous studies (15,18). Whether LTG has a lower overall complication rate than OTG remains controversial. Kim et al. considered LTG to have a lower overall complication rate than OTG (14,15), while some studies suggested that there was no significant difference in postoperative complications between LTG and OTG (9,10,16). Because LTG and studies of its safety and efficacy are still in the exploratory stage, the number of cases in the current study is generally less, and the number of cases in the study for stage 0–I gastric cancer is even smaller. There may be no significant difference in the evaluation of complications due to the lack of statistical efficacy. Therefore, our study further used multivariate regression with a GEE to compare the occurrence of complications between the two groups. The LTG group did not show a higher or lower risk than the OTG group in the comparison of postoperative complications in the model (number of observations n=1,098).

Due to the technical differences between LTG and OTG, the incidence of complications may be different for the different surgical methods. Traditional open surgery involves a large incision, which causes more stimulation or damage to the intestines, blood vessels and lymphatic system during the operation, resulting in this method being more prone to postoperative incision infection, postoperative intestinal obstruction, abdominal hemorrhage, lymphatic fistula and other complications (18-20). However, digestive reconstruction is difficult in LTG surgery, especially in esophagojejunal anastomosis; therefore, the incidence of anastomosis-related complications in LTG may be higher than that in OTG (18,19,21). In a national big data study (19), LTG was considered to increase the risk of anastomosis-related complications, but no subgroup analysis of stage 0–I gastric cancer was conducted in the study. Lee et al. (28) also considered that LTG surgery would increase the risk of anastomotic complications in a study comparing OTG with laparoscopic-assisted total gastrectomy for early gastric cancer. However, in other studies on the treatment of LTG in early and advanced gastric cancer, the incidence of anastomosis-related complications between LTG and OTG was similar (9,18,23). In addition, in a meta-analysis in 2019, it was suggested that LTG did not increase the risk of anastomotic leakage or anastomotic stenosis (13,29). In our study, the OTG group had a higher incidence of incision infection, postoperative intestinal obstruction, abdominal bleeding and lymphatic fistula, while the LTG group had a higher incidence of anastomotic leakage, anastomotic bleeding and anastomotic stenosis; these findings are consistent with those of previous reports. In view of the different tendencies of complications between the different surgical methods, we divided the complications into OTG-related complications and LTG-related complications in the analysis and compared them by the GEE model. In the GEE model of OTG-related complications (number of observations n=488), the unadjusted model showed that the risk of OTG-related complications in the LTG group was lower, with a nearly significant difference (OR: 0.131, 95% CI: 0.02–1.10). After adjusting for age, sex, BMI, tumor location, pathological T stage and pathological N stage, we found that LTG had a lower risk of OTG-related complications (OR: 0.111, 95% CI: 0.02–0.77). However, in a comparison of LTG-related complications (number of observations n=366), LTG did not show a higher risk of LTG-related complications than OTG. This suggests that although there is no significant difference between LTG and OTG in the occurrence of overall complications, LTG can reduce the occurrence of OTG-related complications and does not increase the risk of LTG-related complications.

Lu et al. (9) reported that the 3-year overall survival rate of stage I gastric cancer was 92.3% and 91.5% in LTG and OTG, respectively, and the long-term survival rate of LTG was similar to that of OTG (P>0.05). Moisan et al. (30) reported that the 3-year overall survival rate of stage I gastric cancer was 94% and 100% in LTG and OTG, respectively, with no difference in long-term survival between the two groups. In our study, the 3-year survival rates for LTG and OTG were 95.9% and 95.9%, respectively, and the 5-year survival rates were 90.4% and 83.7%, respectively, similar to previous reports. In the K-M survival curve without IPTW adjustment, there was no significant difference in long-term survival between the two groups (P>0.05). After IPTW adjustment, there was also no significant difference in survival between the two groups (P>0.05). In a comparison of long-term survival, LTG showed long-term survival comparable to that of traditional open surgery. Therefore, we consider the application of LTG to be safe and feasible in patients with stage 0–I gastric cancer.

Limitations

The main limitation of this study is that it is retrospective. LTG and OTG are not based on random assignment, so there is selection bias, although we have adopted IPTW to minimize bias. To the best of our knowledge, our study has been one of the largest in terms of the number of LTG cases in early gastric cancer, and we used multivariate regression with a GEE to make up for the shortage of cases, but there may still be a problem of insufficient statistical efficiency.

Conclusions

LTG is safe and feasible in stage 0–I gastric cancer. The overall complication rate and long-term survival of LTG are similar to those of OTG, but LTG can reduce the incidence of OTG-related complications and does not increase the risk of LTG-related complications. However, these results still need to be confirmed in a large clinical trial.

Acknowledgments

We would like to thank the research assistants in Department of Gastrointestinal Surgery, Guangdong Provincial People’s Hospital, for their assistance in the data collection.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://cco.amegroups.com/article/view/10.21037/cco-2025-aw-152/rc

Data Sharing Statement: Available at https://cco.amegroups.com/article/view/10.21037/cco-2025-aw-152/dss

Peer Review File: Available at https://cco.amegroups.com/article/view/10.21037/cco-2025-aw-152/prf

Funding: This work was supported by Beijing Xisike Clinical Oncology Research Foundation (No. Y-HR2022QN-0383), grants of the Science and Technology Plan of Guangzhou, Guangdong Province, China (No. 202102080230), National key Clinical Specialty Construction Project (2021-2024, No. 2022YW030009) and The ‘Outstanding Young Medical Talent of Guangdong Province’ program, Guangdong Provincial People’s Hospital (No. KJ012019439).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://cco.amegroups.com/article/view/10.21037/cco-2025-aw-152/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Guangdong Provincial People's Hospital (approval No. KY-Q-2021-309-02) and informed consent was obtained from all individual participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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