Short- and long-term outcomes of laparoscopy-assisted versus open total gastrectomy for gastric cancer: a propensity score-matched analysis

INTRODUCTION

Since laparoscopy-assisted distal gastrectomy (LADG) for early gastric cancer (EGC) was first reported by Kitano et al. [1] in 1994, the use of laparoscopy-assisted gastrectomy (LAG) has gained popularity as a treatment for EGC. The advantages of minimally invasive laparoscopic gastrectomy include faster recovery, decreased blood loss, fewer postoperative complications and a shorter hospital stay [2–4]. Laparoscopic gastrectomy has been a standard approach for EGC due to its minimal invasiveness and similar long-term outcomes compared with conventional open surgery. Many experienced institutions have already extended the indications of laparoscopic gastrectomy to highly selective patients with advanced gastric cancer (AGC), and the majority of retrospective studies have focused on patients with AGC who underwent laparoscopic distal gastrectomy. Moreover, centers in Japan, Korea and China have been conducting several randomized controlled trials to evaluate the feasibility and safety of LADG for gastric cancer in recent years [5–7]. To the best of our knowledge, few reports have compared the feasibility, safety and long-term outcomes of laparoscopy-assisted total gastrectomy (LATG) to those of open total gastrectomy (OTG), and randomized controlled clinical trials comparing these two modalities have not yet been reported. Therefore, we enrolled a large number of patients and used the propensity score-matching method to reduce bias in our study. We compared the short-term and long-term outcomes achieved by LATG and OTG to investigate the efficacy of the laparoscopic approach for patients with gastric cancer, and the results can provide new evidence to support the application of LATG prior to conducting randomized controlled clinical trials.

RESULTS

Survival after surgery

The median follow-up period was 45 months (range 1–115 months). The 3-year cumulative survival rates of the LATG group and OTG group were 61.5% and 60.7% (P = 0.696) before propensity matching and 59.7% and 54.9% (P = 0.101) after propensity matching, respectively (Figure 1). The 3-year cumulative survival rates of the LATG group and OTG group were 89.9% and 97.7% for patients with stage I disease (P = 0.028), and the 3-year cumulative survival rates did not significantly differ between patients with stage II and stage III disease (P > 0.05). After propensity score matching, the analysis of the cumulative survival curve did not show significant difference for any cancer stage (Figure 2).

Figure 1

Comparison of cumulative survival rates between LATG and OTG before propensity matching (P = 0.696) (A) and cumulative survival rates between LATG and OTG after propensity matching (P = 0.101) (B)

There was no statistically significant difference between the two groups.

Figure 2

Comparison of cumulative survival rates between LATG and OTG according to cancer stage

(C). stage I before matching; (D) stage I after matching; (E) stage II before matching; (F) stage II after matching; (G) stage III before matching; (H) stage III after matching;

DISCUSSION

Laparoscopic gastrectomy is an acceptable alternative to conventional open gastrectomy for patients with ECG not only because the two procedures result in similar survival and recurrence [8, 9] but also because patients tend to experience better early postoperative outcomes than those undergoing open gastrectomy [2–4]. In recent years, several experienced institutions have reported favorable long-term oncological outcomes as well as the improved technical feasibility and safety of LADG for the treatment of advanced gastric cancer compared with conventional open gastrectomy [6, 10, 11]. However, few studies have examined LATG due to extended lymph node detection and complex digestive construction. Moreover, these retrospective studies have primarily examined EGC in small samples [12–17], and randomized controlled clinical trials have not been reported. Therefore, our institution enrolled a large number of patients to evaluate the feasibility, safety and clinical efficacy of LATG before conducting randomized controlled clinical trials that evaluate the efficacy of LATG for the treatment of gastric cancer. Specifically, the propensity score-matching method was used to reduce bias.

In previous studies of LDG and ODG, the main advantages of laparoscopic gastrectomy over conventional open surgery included less blood loss, a smaller skin incision, a shorter time to ambulation, a shorter time to a liquid diet and a shorter postoperative hospital stay [5, 18] as well as the ability to visualize finer structures due to laparoscopic amplification. However, LG is also associated with disadvantages, such as increased cost, the need for a surgeon skilled in laparoscopic techniques and a longer learning curve [19]. However, few studies have examined the minimal invasiveness of laparoscopic total gastrectomy. The results of our study provide new evidence of the minimally invasive nature of laparoscopic total gastrectomy. Specifically, the LATG group in our study exhibited a significantly reduced mean estimated blood loss and shorter times to flatus and liquid diet consumption compared to the OTG group. Some studies [12–14, 20, 21] reported that the operation time was longer for laparoscopic gastrectomy than conventional open gastrectomy. Nevertheless, improvements in laparoscopic techniques, surgical instruments and the accumulation of experience have reduced the operation time for laparoscopic gastrectomy [22]. Specifically, Kunisaki et al. [23] found that the accumulation of experience reduced the operation time; the operation time associated with LAG was significantly shorter in a medical group performing 81 to 100 surgeries than in a group performing 1 to 20 surgeries (221.6 min vs. 351.2 min, P>0.05). Thus, laparoscopic gastrectomy did not require more time than conventional open gastrectomy when performed by an experienced surgeon [13], and the incision required for laparoscopic gastrectomy is preferred to that required for open gastrectomy. Additionally, our institution uses a systematic laparoscopic gastrectomy procedure [24] that simplifies this complex procedure, improves the efficiency of laparoscopic surgery and shortens the operation time of LATG compared to conventional OTG. Our data showed that more lymph nodes were dissected in the LATG group more than in the OTG group, and the average number of lymph nodes harvested exceeded 30 in both groups. The key to lymph node detection is being skilled in laparoscopic techniques and a good anatomical sense under the laparoscope. A laparoscope can help the surgeon dissect lymph nodes under special anatomical structures because the laparoscope can amplify the vasculature, nerves, fascia and other structures. In addition, our center took procedural operative steps [24–26] to dissect the perigastric lymph nodes. Thus, our laparoscopic surgical procedure is preferred over open gastrectomy for AGC lymphadenectomy. This result suggested that the number of retrieved lymph nodes was comparable for LATG and OTG.

Postoperative morbidity and mortality are important objective factors to evaluate technical feasibility. Specifically, the postoperative complications rate of LATG has been reported to range from 8.5% to 32% [12, 14, 16, 20, 21], and these differences may be due to differences in the experience of surgeons as well as differences in the definitions and classifications of postoperative complications. In recent years, many scholars have recommended the Clavien-Dindo classification system has been recommended to define and grade postoperative complications. This system was tested in a large cohort of patients who underwent general surgery, and the acceptability of this classification system was assessed with an international survey, which demonstrated that this system appears to be a reliable tool for quality assessment in surgery [27, 28]. In our study, the postoperative complication rates of the LATG group and OTG group were 14.9% and 21.0% (P = 0.009), respectively, and the mortality rates according to the Clavien-Dindo system did not significantly differ between groups after propensity matching. In our multivariate analysis, operative approach and comorbidities were identified as independent factors related to postoperative complications. Moreover, our study confirmed that comorbidities may increase the postoperative complications rate, which has been reported in a previous study [29]. These results suggested that the safety and feasibility of LATG and OTG were comparable.

Long-term survival rates are important elements for assessing oncological safety. Specifically, laparoscopic gastrectomy can only be accepted as an alternative approach to open gastrectomy if similar long-term outcomes can be achieved. Previous studies showed that the long-term survival rates of patients who underwent LATG were similar to those of patients who underwent OTG, but these reports primarily examined small cohorts of patients who underwent LATG for EGC. A case control study [14] reported that the long-term outcomes of LATG were similar to those of open OTG for patients with AGC. Moreover, Kim et al. [19] found that the long-term oncologic outcomes of laparoscopic gastrectomy for 238 patients with AGC were consistent with those of open gastrectomy in a case-controlled and case-matched study. Although the oncological results of the LATG group were similar to those of the OTG group for the pre-matched patients, the cumulative survival rate of patients with stage I gastric cancer in the LATG group was significantly lower than that in the OTG group. This difference may be due to the heterogeneity of the two groups. Specifically, the proportion of undifferentiated histology was higher in the LATG group than the OTG group, and the cumulative survival rate did not significantly differ between the two groups after the propensity score-matched analysis. These results suggested that the long-term outcomes achieved by LATG and OTG were comparable.

Our study was also subject to several limitations. We conducted the study at a single center in a retrospective manner, and patients who experienced recurrence were not described in detail due to incomplete follow-up results. Nonetheless, to the best of our knowledge, this study examined the largest number of patients with advanced gastric cancer who have undergone LATG at a high-volume center and used the propensity score-matching method to reduce bias.

In conclusion, LATG is a safe and reliable procedure for the treatment of gastric cancer when conducted by experienced surgeons at high-volume institutions. The morbidity and mortality of LATG is acceptable when compared with OTG, and oncologic outcomes are similar in both groups. Additional randomized controlled clinical trials can be conducted to provide valuable evidence of the safety and efficacy of LATG in treating gastric cancer.

MATERIALS AND METHODS