Comparison of the Postoperative Complications Between Robotic Total and Distal Gastrectomies for Gastric Cancer Using Clavien–Dindo Classification: A Propensity Score-matched Retrospective Cohort Study of 726 Patients

Abstract

Background

This study was designed to compare the postoperative complications after Robotic total gastrectomy (RTG) and robotic distal gastrectomy (RDG) and to systematically evaluate the safety and feasibility of RTG for the treatment of gastric cancer (GC).

Methods

Patients with GC who underwent RTG or RDG for curative intent between March 2010 and August 2019 were analyzed. We used propensity score matching (PSM) to reduce selection bias. The morbidity and mortality within 30 days after surgery between the RTG and the RDG groups were compared.

Results

According to Clavien–Dindo (C–D) classification, the morbidity and mortality of the RTG group were comparable to those of the RDG group. Subgroup analyses showed no significant difference between the RTG and RDG groups in all stratified parameters (all P > .05). Multivariate analysis revealed that age ≥70 years (P = .002) and surgeons’ experience ≤25 cases (P = .013) were independent risk factors for overall complication. Surgeons’ experience ≤25 cases (P = .010) was identified as an independent risk factor for severe complication.

Conclusion

RTG is a safe and feasible surgical procedure for the treatment of GC with acceptable morbidity and mortality. More complications were observed for RTG, indicating that RTG is more invasive than RDG.

Keywords

robotic total gastrectomy complication gastric cancer Clavien–Dindo classification

Laparoscopic gastrectomy (LG) has gradually become a globally accepted surgical procedure for patients with gastric cancer (GC).^1-3 The da Vinci surgical system has several technical advantages over laparoscopic instruments, including 3D vision, greater freedom of movement, tremor filtration, and improved ergonomics for the surgeon. Since the robotic gastrectomy (RG) was first reported by Hashizume et al⁴ in 2003, increasing studies have demonstrated that RG is a safe and feasible procedure for the treatment of GC in terms of short- and long-term outcomes.^5-9 However, robotic total gastrectomy (RTG) has not been as popular as RDG because of its technical difficulties, undetermined safety, and postoperative complications. Compared with RDG, RTG requires dissection of lymph nodes at the splenic hilum or along distal splenic vessels, as well as anastomosis of the esophagus to the jejunum. To date, there are a few large-scale studies regarding postoperative complications of RTG.

Thus, we designed this study to compare the complications after RTG and RDG according the Clavien–Dindo (C–D) classification and to systematically evaluate the safety and feasibility of RTG for the treatment of GC.

Materials and Methods

From March 2010 to August 2019, more than 800 cases of patients with GC underwent RG using the da Vinci® Surgical System (Intuitive Surgical, Sunnyvale, CA, USA) at a high-volume center in China. Inclusion criteria of patients were¹ age older than 18 and younger than 80 years²; primary gastric adenocarcinoma confirmed pathologically by endoscopic biopsy³; underwent RTG or RDG for curative intent⁴; pT1 to pT4a, N0 to N+, M0. Patients with the following characteristics were excluded¹: remnant GC²; palliative surgery³; emergency surgery due to a complication (bleeding, obstruction, or perforation) caused by GC⁴; previous neoadjuvant chemotherapy or radiotherapy⁵; missing data. Pathologic evaluations and staging were updated according to the 8th Union for International Cancer Control (UICC)/American Joint Committee on Cancer (AJCC) staging system of GC.¹⁰ The study was approved by the Ethics Committee of our center. One-to-one propensity score matching (PSM) with .02 caliper width was performed using a logistic regression model with the following variables: age, sex, body mass index (BMI), comorbidities, ASA score, histological type, and pathologic TNM stage. Flow diagram of the patient selection process is shown in Figure 1.

Figure 1.

Flow diagram of the patient selection process.

Definition of Postoperative Complication

Postoperative complications were recorded using the C–D classification and divided into local and systemic.^11,12 When complication is associated with surgical technique near the operation field, such as wound or anastomosis, it was considered as local complication. The complication was classified as systemic when it was not associated with the operation field, such as pulmonary or hepatic. We reviewed morbidity and mortality occurred during hospitalization after the surgery. We also reviewed medical records of all patients until postoperative 3 months. Due to operations in general carry an overall risk and some self-limiting complications, here, we considered complications in C–D grade II or over to reflect actual technical maturity and focused our analysis on complications in C–D grade II or over. Grade II complications were considered as minor, and grade IIIa or greater, which required additional interventional or surgical treatment, were considered as severe complications.

Statistical Analysis

All statistical analyses were performed using SPSS, ver.24.0 (SPSS Inc, Chicago IL, USA). The Chi-square test, Fisher’s exact test, and independent sample t test were used for comparisons between the two groups. Categorical variables are presented as counts and percentages. Continuous variables normally distributed are expressed as the mean ± standard deviation (SD). Variables with P values <.10 in univariate analysis were included in the multivariate analysis. Multivariate analysis was conducted with the binary logistic regression model to identify independent risk factors for postoperative complications. P values <.05 were considered significant.

Results

Characteristics of Patients

Table 1 summarizes the patient background in entire (N = 726) and PSM cohort (N = 364). After PSM, 182 matched pairs were selected during the same time period. The baseline characteristics were closely balanced between the matched pairs.

Table 1.

Patient Background in Entire and Propensity Score-Matched Cohorts.

Variables	Entire Cohort			Propensity Score-Matched Cohort
Variables	RTG (n = 207)	RDG (n = 519)	P	RTG (n = 182)	RDG (n = 182)	P
Age (years)	60.5 ± 9.4	55.1 ± 10.2	<.001	59.70 ± 9.58	59.65 ± 9.82	.961
Sex			.001			.132
Male	168 (81.2)	356 (68.6)		155 (85.2)	144 (79.1)
Female	39 (18.8)	163 (31.4)		27 (14.8)	38 (20.9)
BMI (kg/m²)	21.9 ± 2.7	22.1 ± 2.9	.376	22.0 ± 2.7	21.8 ± 2.9	.396
Comorbidities			.346			.903
Present	48 (23.2)	104 (20.0)		45 (24.7)	44 (24.2)
Absent	159 (76.8)	415 (80.0)		137 (75.3)	138 (75.8)
ASA score			.536			.862
1 or 2	186 (89.9)	458 (88.2)		164 (90.1)	163 (89.6)
3	21 (10.1)	61 (11.8)		18 (9.9)	19 (10.4)
Histological type			.820			1.000
Well/moderately	64 (30.9)	156 (30.1)		56 (30.8)	56 (30.8)
Poorly/undifferentiated	143 (69.1)	363 (69.9)		126 (69.2)	126 (69.2)
pTNM			<.001			.222
I	31 (15.0)	214 (41.2)		31 (17.0)	44 (24.2)
II	49 (23.7)	130 (25.0)		49 (26.9)	48 (26.4)
III	127 (61.4)	175 (33.7)		102 (56.0)	90 (49.5)
Tumor size (cm)	4.3 ± 1.9	3.0 ± 1.4	<.001	4.3 ± 2.0	3.3 ± 1.3	<.001
Chronological distribution			.120			.731
2010–2014	67 (67.6)	200 (61.5)		53 (29.1)	56 (30.8)
2015–2019	140 (32.4)	319 (38.5)		129 (70.9)	126 (69.2)

Abbreviations: RTG: robotic total gastrectomy; RDG: robotic distal gastrectomy.

Postoperative Morbidity and Mortality Following Robotic Gastrectomy in PSM Cohort

The postoperative complications of patients in the RTG and RDG groups are shown in Table 2. The overall, severe, local, and systemic complication rates were comparable between RTG and RDG groups (15.4% vs 12.1%, P = .361; 4.4% vs 3.8%, P = .792; 8.2% vs 6.6%, P = .548; and 7.7% vs 6.6%, P = .684, respectively). The details of local and systemic complications following RG are shown in Tables 3 and 4. The specific local and systemic complications were comparable between the two groups.

Table 2.

Morbidity and Mortality in the RTG and RDG Groups.

Grades and Types	Total (n = 364)	RTG (n = 182)	RDG (n = 182)	P
Grade II (%)	36 (9.9)	21 (11.5)	15 (8.2)	.292
Grade IIIa (%)	7 (1.9)	3 (1.6)	5 (2.7)	.721
Grade IIIb (%)	2 (.5)	2 (1.1)	0 (.0)	.499
Grade IVa (%)	2 (.5)	0 (.0)	2 (1.1)	.499
Grade IVb (%)	1 (.3)	1 (.5)	0 (.0)	1.000
Grade V (%)	2 (.5)	2 (1.1)	0 (.0)	.499
Overall complications (%)	50 (13.7)	28 (15.4)	22 (12.1)	.361
Severe complications (%)	14 (3.8)	8 (4.4)	7 (3.8)	.792
Local complications (%)	27 (7.4)	15 (8.2)	12 (6.6)	.548
Systemic complications (%)	26 (7.1)	14 (7.7)	12 (6.6)	.684
Mortality (%)	2 (.5)	2 (1.1)	0 (.0)	.499

Abbreviations: RTG: robotic total gastrectomy; RDG: robotic distal gastrectomy.

Table 3.

Local Complications in the RTG and RDG Groups.

Local Complications	Overall (II-V)			P	Severe (IIIa-V)			P
Local Complications	Total	RTG	RDG	P	Total	RTG	RDG	P
Wound problem	6	2	4	.233	1	0	1	1.000
Intra-abdominal infection	8	6	2	.238	2	2	0	.499
Pancreatitis	1	0	1	.440	1	0	1	1.000
Intra-abdominal bleeding	3	3	0	.113	0	0	0	—
Anastomotic leakage	4	3	1	.425	4	3	1	.315
Lymphatic leakage	0	0	0	—	0	0	0	—
Intraluminal bleeding	2	0	2	.189	1	0	1	1.000
Duodenal stump leakage	1	0	1	.440	1	0	1	1.000
Anastomotic stricture	2	2	0	.497	0	0	0	—
Ileus/motility disorder	3	1	2	.415	1	0	1	1.000

Abbreviations: RTG: robotic total gastrectomy; RDG: robotic distal gastrectomy.

Table 4.

Systemic Complications in the RTG and RDG Groups.

Systemic Complications	Overall (II-V)			P	Severe (IIIa-V)			P
Systemic Complications	Total	RTG	RDG	P	Total	RTG	RDG	P
Pulmonary	12	7	5	.852	2	1	1	1.000
Hepatic	3	1	2	.562	0	0	0	—
Urinary	3	1	2	.562	0	0	0	—
Cardiac	6	2	4	.410	1	1	0	1.000
Renal	0	0	0	—	0	0	0	—
Endocrine	1	0	1	1.000	0	0	0	—
Severe anemia	2	1	1	1.000	0	0	0	—
Neurologic	0	0	0	—	0	0	0	—
Infection	0	0	0	—	0	0	0	—

Abbreviations: RTG: robotic total gastrectomy; RDG: robotic distal gastrectomy.

In the RTG group, the most common local complication was intra-abdominal infection, followed by intra-abdominal bleeding and anastomotic leakage. In the RDG group, the most common local complication was wound problem. Most patients of intra-abdominal infection and wound problem could be cured by antibiotics or parenteral nutrition. Regarding systemic complications, pulmonary was the most common, and the majority of them were cured by antibiotics.

Figure 2 shows the complication rates in different age groups. The overall and systemic complication rates presented a general increased trend along with age, regardless of RTG or RDG groups. Subgroup analyses of postoperative complications showed no significant difference between the RTG and RDG groups in all stratified parameters in the comparison of overall (Figure 3A) and severe complications (Figure 3B).

Figure 2.

Postoperative complication rates in different age groups. (A) Overall complication; (B) severe complication; (C) local complication; (D) systemic complication.

Figure 3.

Subgroup analyses of postoperative complications. (A) Overall complications; (B) severe complications.

Risk Factors for Complications

Multivariate analysis revealed that age ≥70 years (P = .002) and surgeons’ experience ≤25 cases (P = .013) were independent risk factors for overall complication (Supplementary Table 1). As for severe complications, age, BMI, and surgeons’ experience were significantly correlated with severe complication in univariable analysis. Surgeons’ experience ≤25 cases (P = .010) was identified as an independent risk factor for severe complication (Supplementary Table 1).

With respect to local complication, surgeons’ experience ≤25 cases (P = .033) was identified as independent risk factor in multivariate analysis (Supplementary Table 2). In terms of systemic complication, age ≥70 years (P < .001), BMI ≥25 (P = .006), and presence of comorbidity (P = .018) were independent risk factors in multivariate analysis (Supplementary Table 2).

Discussion

In this study, patients underwent RTG showed higher complication rate when compared with those underwent RDG although the difference did not reach statistically significant.

Previous studies reported that the overall complication rate of RG varied from 5.2% to 24.1%.^13-16 In the report of multicenter study evaluating safety and feasibility of RG for stage I/II GC, the severe complication rate was 2.5%.¹⁷ Another multicenter study reported that the overall and major complication rates were 13.5% and 1.3%, respectively.¹⁸ However, patients who underwent RDG account a large part in these studies and they did not perform specific analysis for RTG. Ye et al¹⁴ reported a 7.5% overall complication rate in the RTG group. Wang et al¹⁵ reported that the major complication rate after RTG was 14.3%. In the present study, the overall complication rate in the RTG group was 15.4%, which was slightly higher than that in the RDG group, but without statistically significant difference. The severe complication rate in the RTG group was 3.8%, which was comparable with those in the RDG group.

The major concern following RTG is esophagojejunostomy (EJ)-related complications. As reported by Wang et al,¹⁵ the dominant major complication after RTG was anastomotic leakage. The anastomotic leakage rates following RTG were reported from 1.4% to 5.3%.^14,15 In the current study, we observed three cases of EJ leakage and two cases of anastomotic stricture in the RTG group.

A recent multicenter study reported that 25 cases were needed to overcome complications learning curve of RG.¹⁹ Based on this, we divided the surgeons’ experience into early (first 25 cases) and late phases, aiming at evaluating the relationship between surgeon’s experience and risk of morbidity after RG. In the present study, surgeons’ experience ≤25 cases was found to be an independent risk factor for overall, severe, and local complications. This indicated that even the surgeons proficient at LG should also be alert to the occurrence of postoperative complications during the learning period of RG. In order to minimize the incidence of postoperative complications due to the lack of experiences, we suggest that surgeons should choose patients in good conditions in the learning stage of RG. In clinical practice, surgeons tend to perform more RDG in the learning phase before they transferred toward RTG. To reduce the bias due to effect of learning curve, the patients were divided into two phases. The results of subgroup analyses for patients in different phases were consistent with that for all cases in PSM cohort.

Adequate number of retrieved lymph nodes not only improves the accuracy of staging and prognostic assessment but may also result in improved oncologic outcomes.^20-22 According to the literature, the impact of number of harvested lymph nodes on morbidity following gastrectomy is controversial. Our previous study found that harvested lymph nodes of more than 30 were an independent risk factor for complication after total gastrectomy.²³ We attribute this to adequate lymphadenectomy during operation, which sometimes injures vessels and increases the risk of postoperative intra-abdominal bleeding. However, most patients in our previous study underwent open or laparoscopic surgery rather than RG. In the current study, the number of retrieved lymph nodes was not associated with postoperative complications, indicating that adequate number of retrieved lymph nodes is safe and feasible without increasing the risk of morbidity. Ye et al¹⁴ reported that RTG could retrieve more lymph nodes as compared with laparoscopic total gastrectomy (LTG). This may attribute to the robotic surgical system allow the surgeons to reach deep-seated vessels and some delicate areas more easily. Meanwhile, the stable working platform and 3D views could facilitate lymph node dissection in tough areas. The superiority of RG during the procedure of lymph node dissection was also observed in the study conducted by Kim et al.²⁴ They found that RDG could provide an advantage over LDG in the dissection of technically demanding suprapancreatic area and the splenic vessels. A recent meta-analysis showed that more lymph nodes were harvested during RG than during LG.²⁵ Given these results, we recommend that adequate lymphadenectomy should be performed by surgeons experienced in RG.

According to the current evidence, the impact of age on morbidity following RG has seldom been reported. Okumura et al²⁶ demonstrated that the morbidity after RG in elderly patients with GC was similar with those underwent LG, indicating that RG could be a safe and feasible procedure. In the current study, elderly patients (age ≥70 years) were associated with increased morbidity. Furthermore, the specific analysis for morbidity in different age groups showed that the overall and systemic complication rates presented an increased trend along with age. This indicated that increased age would be a leading risk factor for systemic complication than for local complication. The reason for this may be that elderly patients always have reduced functional reserve and increased comorbidities.^27-29 In the current study, comorbidity was also identified as an independent risk factor for systemic complication. Therefore, for elderly patients, we should pay more attention in preoperative assessment and postoperative management.

There are several limitations to this study. First, all surgeons included in this study had experience with LG prior to initiation of RG, which limited the generalizability of these findings to surgeons with less LG experience. Second, this study is limited in generalizability since BMI of majority of patients was lower than 25 kg/m², which may be lower than what most surgeons would encounter in Western countries. Last, patients who underwent neoadjuvant therapy were excluded from the study. This may limit the generalizability of the study results.

In conclusion, the current study suggests that RTG is a safe and feasible surgical procedure for the treatment of GC with acceptable morbidity and mortality. More complications were observed for RTG, indicating that RTG is more invasive than RDG. We suggest that surgeons should be more careful and choose patients in good conditions in the learning stage of RG.

Supplemental Material

sj-pdf-1-sri-10.1177_15533506211047011 – Supplemental Material for Comparison of the Postoperative Complications Between Robotic Total and Distal Gastrectomies for Gastric Cancer Using Clavien–Dindo Classification: A Propensity Score-matched Retrospective Cohort Study of 726 Patients

Supplemental Material, sj-pdf-1-sri-10.1177_15533506211047011 for Comparison of the Postoperative Complications Between Robotic Total and Distal Gastrectomies for Gastric Cancer Using Clavien–Dindo Classification: A Propensity Score-matched Retrospective Cohort Study of 726 Patients by Zheng-yan Li, Yong-liang Zhao, Feng Qian, Bo Tang, Zi-yan Luo, Yan Wen, Yan Shi and Pei-wu Yu in Surgical Innovation

Footnotes

Acknowledgments

The authors thank Yan Wen for data collection and management.

Author Contribution

Li Zheng-yan, Shi Yan, and Yu Pei-wu designed the study. Qian Feng, Luo Zi-yan, and Wen Yan were responsible for data acquisition. Zhao Yong-liang and Shi Yan were responsible for quality control of data and algorithms. Li Zheng-yan and Tang Bo analyzed and interpreted the data. Li Zheng-yan wrote the article. All authors have seen and approved the final version of the manuscript.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by the Chongqing Postdoctoral Science Special Foundation.

Ethical Approval

This study was approved by the Ethics Committee of the Southwest Hospital, Third Military Medical University. This article does not contain any studies with animals performed by any of the authors.

ORCID iD

Li Zheng-yan

Supplemental Material

Supplemental material for this article is available online.

References

Ying

Huang

, et al. Oncologic outcomes of laparoscopy-assisted gastrectomy for advanced gastric cancer: a large-scale multicenter retrospective cohort study from China. Surg Endosc. 2014;28:2048-2056.

Park

Yoon

Kim

, et al. Laparoscopy-assisted versus open D2 distal gastrectomy for advanced gastric cancer: results from a randomized phase II multicenter clinical trial (COACT 1001). Ann Surg. 2018;267:638-645.

Huang

Sun

, et al. Effect of laparoscopic vs open distal gastrectomy on 3-year disease-free survival in patients with locally advanced gastric cancer: The CLASS-01 randomized clinical trial. JAMA. 2019;321:1983-1992.

Hashizume

Sugimachi

. Robot-assisted gastric surgery. Surg Clin North Am. 2003;83:1429-1444.

Hosoda

Mieno

Ema

, et al. Safety and feasibility of robotic distal gastrectomy for stage IA gastric cancer: A phase II trial. J Surg Res. 2019;238:224-231.

Li ZY

Zhou YB

, et al.

Robotic gastrectomy versus laparoscopic gastrectomy for gastric cancer: A multicenter cohort study of 5402 patients in China [published ahead of print July 2, 2021]

Ann Surg. doi:10.1097/SLA.0000000000005046.

Zhao

Qian

, et al. Long-term oncologic outcomes of robotic versus laparoscopic gastrectomy for locally advanced gastric cancer: A propensity score-matched analysis of 1170 patients [published ahead of print January 4, 2021]. Surg Endosc. doi:10.1007/s00464-020-08198-9

Zheng-Yan

Yong-Liang

Feng

Yan

Pei-Wu

. Morbidity and short-term surgical outcomes of robotic versus laparoscopic distal gastrectomy for gastric cancer: A large cohort study. Surg Endosc. 2020;35(7):3572-3583.

Zheng

, et al. Assessment of robotic versus laparoscopic distal gastrectomy for gastric cancer: A randomized controlled trial. Ann Surg. 2020;273(5):858-867.

10.

Sano

Coit

Kim

, et al. Proposal of a new stage grouping of gastric cancer for TNM classification: International gastric cancer association staging project. Gastric Cancer. 2017;20:217-225.

11.

Dindo

Demartines

Clavien

. Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205-213.

12.

Clavien

Barkun

de Oliveira

, et al. The Clavien-Dindo classification of surgical complications: Five-year experience. Ann Surg. 2009;250:187-196.

13.

Yang

Roh

Kim

, et al. Surgical outcomes after open, laparoscopic, and robotic gastrectomy for gastric cancer. Ann Surg Oncol. 2017;24:1770-1777.

14.

Shi

Liu

, et al. Robotic-assisted versus conventional laparoscopic-assisted total gastrectomy with D2 lymphadenectomy for advanced gastric cancer: short-term outcomes at a mono-institution. BMC Surg. 2019;19:86.

15.

Wang

Guo

, et al. Systematic assessment of complications after robotic-assisted total versus distal gastrectomy for advanced gastric cancer: A retrospective propensity score-matched study using Clavien-Dindo classification. Int J Surg. 2019;71:140-148.

16.

Gao

Qiao

, et al. Comparison of robotic- and laparoscopic-assisted gastrectomy in advanced gastric cancer: Updated short- and long-term results. Surg Endosc. 2019;33:528-534.

17.

Uyama

Suda

Nakauchi

, et al. Clinical advantages of robotic gastrectomy for clinical stage I/II gastric cancer: A multi-institutional prospective single-arm study. Gastric Cancer. 2019;22:377-385.

18.

Kim

Han

Yang

, et al. Multicenter prospective comparative study of robotic versus laparoscopic gastrectomy for gastric adenocarcinoma. Ann Surg. 2016;263:103-109.

19.

Kim

Hyung

, et al. Comprehensive learning curve of robotic surgery: Discovery from a multicenter prospective trial of robotic gastrectomy. Ann Surg. 2019;273(5):949-956.

20.

Shen

Xie

Liang

Jiang

Wang

. Effect of the number of lymph nodes harvested on the long-term survival of gastric cancer patients according to tumor stage and location: A 12-year study of 1,637 cases. Am J Surg. 2015;210:431-440e3.

21.

Liu

Jun

, et al. Impact of total retrieved lymph nodes on staging and survival of patients with gastric cancer invading the subserosa. Surg Oncol. 2009;18:379-384.

22.

Zheng

Feng

Guo

, et al. Harvest of at east 23 lymph nodes is indispensable for stage N3 gastric cancer patients. Ann Surg Oncol. 2017;24:998-1002.

23.

Zhou

Shi

, et al. Evaluation of Clavien-Dindo classification in patients undergoing total gastrectomy for gastric cancer. Med Oncol. 2015;32:120.

24.

Kim

Reim

Park

, et al. Role of robot-assisted distal gastrectomy compared to laparoscopy-assisted distal gastrectomy in suprapancreatic nodal dissection for gastric cancer. Surg Endosc. 2016;30:1547-1552.

25.

Bobo

Xin

Jiang

, et al. Robotic gastrectomy versus laparoscopic gastrectomy for gastric cancer: meta-analysis and trial sequential analysis of prospective observational studies. Surg Endosc. 2019;33:1033-1048.

26.

Okumura

Son

Kim

, et al. Robotic gastrectomy for elderly gastric cancer patients: comparisons with robotic gastrectomy in younger patients and laparoscopic gastrectomy in the elderly. Gastric Cancer. 2016;19:1125-1134.

27.

Mohri

Yasuda

Ohi

, et al. Short- and long-term outcomes of laparoscopic gastrectomy in elderly patients with gastric cancer. Surg Endosc. 2015;29:1627-1635.

28.

Shimada

Sawada

Oae

, et al. Safety and curability of laparoscopic gastrectomy in elderly patients with gastric cancer. Surg Endosc. 2018;32:4277-4283.

29.

Honda

Kumamaru

Etoh

, et al. Surgical risk and benefits of laparoscopic surgery for elderly patients with gastric cancer: a multicenter prospective cohort study. Gastric Cancer. 2018;22:845-852.

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