The Effect of Surgical Approach on Clinical Outcomes in 535 Patients with Remnant Gastric Cancer

Abstract

Purpose:

This study aimed to evaluate the effect of laparoscopic gastrectomy (LG) and open gastrectomy (OG) on clinical outcomes in patients with remnant gastric cancer (RGC).

Materials and Methods:

The databases of PubMed, EMBASE, and Cochrane Library were used to search for eligible studies from inception to April 1st, 2023. Hazard ratios (HRs), mean difference (MD), odds ratios (OR), and 95% confidence intervals (CIs) were pooled up to analyze. The Newcastle-Ottawa Scale (NOS) scores were used to evaluate the quality of the included studies. This study was performed with RevMan 5.3 (The Cochrane Collaboration, London, United Kingdom) software.

Results:

A total of 11 studies involving 535 RGC patients were included in this study. In terms of basic information, we found that the OG group had a higher American Society of Anesthesiologists (ASA) grade (≥2) (OR = 0.24, I² = 54%, 95% CI = 0.08–0.71, P = .01) than the LG group. In terms of postoperative outcomes, we found that the LG group had longer operative time (MD = 33.95, I² = 58%, 95% CI = 15.05–52.85, P < .01), shorter postoperative hospital stay (MD = 5.08, I² = 84%, 95% CI = −9.74 to −0.42, P = .03), shorter length of incision (MD = −7.15, I² = 94%, 95% CI = −10.99 to −3.31, P < .01), earlier food intake (MD = −3.09, I² = 76%, 95% CI = −4.84 to −1.35, P < .01), and earlier time to first flatus (MD = −0.84, I² = 0%, 95% CI = −1.09 to −0.59, P < .01). We found that there was no statistically significant difference in overall survival (HR = 0.96, I² = 0%, 95% CI = 0.48–1.93, P = .92) between the LG group and the OG group.

Conclusion:

LG for RGC patients had longer surgical time, shorter postoperative hospital stay, shorter length of incision, earlier food intake, and earlier time to first flatus.

Introduction

Gastric cancer is the third most common cause of cancer-related deaths in males worldwide and the fifth most common cause in females.¹ Remnant gastric cancer (RGC) is defined as cancer that occurs in the remnant stomach after subtotal gastrectomy due to benign diseases or cancer.^2–4 Compared with gastric cancer, the incidence of RGC is relatively low. According to reports, RGC accounts for 1%–8% of all gastric cancers.^5–7

Due to the improved survival rate after radical gastrectomy for the treatment of peptic ulcers and cancer,⁸ there is an increasing number of RGC being discovered at a resectable stage.^9,10 Although chemotherapy and radiation therapy have rapidly developed in the field of cancer treatment, for resectable RGC, gastrectomy combined with sufficient lymph node (LN) resection is still the preferred treatment option.^8,11,12

With the advancement of endoscopic surgical instruments and the understanding of microsurgery, laparoscopic gastrectomy (LG) has become widespread.^13,14 LG is gradually accepted in clinical practice due to its less invasiveness and shorter recovery time compared to open gastrectomy (OG).^15,16 However, there was no clear conclusion on the clinical outcomes of the surgical approach for RGC. Thus, this study aimed to investigate the effect of the surgical approach on RGC. For this purpose, we compared the clinical outcomes of LG and OG patients with RGC.

Materials and Methods

This study was conducted by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement.¹⁷

Search strategy

PubMed, EMBASE, and Cochrane Library were searched from inception to April 1st, 2023. The following keywords related to RGC were used for the search: “remnant gastric cancer” OR “gastric remnant cancer” OR “gastric stump cancer.” As for laparoscopic, the search strategy was “laparoscopic” OR “laparoscopy.” As for open, the searching strategy was “open” OR “laparotomy.” Then, we combined these items with “AND.” The search was limited to title and abstract. The language available was English. And two authors performed the search independently.

Inclusion and exclusion criteria

The studies were included in this study if they met the following criteria: (1) RGC patients who underwent gastrectomy were included; (2) the comparison between the LG group and the OG group was reported; and (3) clinical outcomes were reported. The exclusion criteria of this study were as follows: (1) Conferences, reviews, letters, comments, or case reports, duplicated publication data; and (2) insufficient data for analysis. All disagreements about inclusion and exclusion were solved by group discussion.

Study selection

Two authors searched the database independently. First, after removing the duplicate records, the titles and abstracts were screened. Second, the full texts were evaluated for eligibility based on the inclusion and exclusion criteria. The final judgment was made after the group discussion.

Definition

Postoperative complications of this study were classified according to the Clavien-Dindo classification and severe postoperative complications were defined as grades ≥III.¹⁸

Data extraction

The data of this study were extracted as follows: (1) Studies' information, including the publication year, the first author's name, country, sample size, and study design; (2) patients' baseline information, including age, sex, body mass index (BMI), American Society of Anesthesiologists (ASA) grade, comorbidity, original disease, previous surgical approach, primary reconstruction, time interval, histologic type, location, Tumor Node Metastasis (TNM) stage, tumor size, and number of retrieved LN and number of metastatic LN; and (3) postoperative clinical outcomes, including operative time, postoperative hospital stay, blood loss, length of incision, food intake, time to first flatus, anastomotic leakage, pancreatic fistula, intra-abdominal infection, surgical site infection, anastomotic stenosis, pneumonia, postoperative bleeding, major complications, overall complications, and overall survival (OS).

Quality assessment

The Newcastle-Ottawa Scale (NOS), which had a score ranging from zero to nine points, was used to assess the quality of enrolled studies.¹⁹ A study with a score of nine points was considered high quality, a study with a score of seven to eight points was considered medium quality, and a study with six or fewer was considered low quality.

Statistical analysis

Mean differences (MDs) and 95% confidence intervals (CIs) were calculated for continuous variables. Odds ratios (ORs) and 95% CIs were calculated for the postoperative complications. Hazard ratios (HRs) and 95% CIs were calculated for the OS of RGC patients. Statistical heterogeneity was assessed by using the value of I² and the result of the chi-squared test. If I² > 50%, it was considered high heterogeneity, the random effect model was used, and P < .1 was considered statistically significant.²⁰ Funnel plots and Egger tests were also used to observe the heterogeneity of studies and publication bias. This study was performed with RevMan 5.3 (The Cochrane Collaboration, London, United Kingdom).

Results

Study selection

A total of 50 studies were identified in the database, including 30 studies in PubMed, 17 studies in Embase, and 3 studies in the Cochrane Library. After removing duplicate studies and unqualified study type, 28 were left for record screening. After browsing the titles and abstracts, 13 studies were left for full-text scanning. Finally, 11 studies^21–31 were included in this study (Fig. 1).

FIG. 1.

Flowchart of study selection.

Characteristics of the included studies

A total of 11 studies involving 535 patients were included in this study. These studies were published from 2014 to 2022 and the study period was from 1996 to 2021, including 11 retrospective studies. More specific information and the NOS scores are shown in Table 1.

Table 1.

Baseline Characteristics of Included Studies

Author	Year	Country	Study date	Study type	Sample size		NOS
Author	Year	Country	Study date	Study type	Laparoscopic open		NOS
Wu et al.³¹	2022	China	2016–2021	Retrospective	36	48	8
Ota et al.²⁸	2020	Japan	2005–2018	Retrospective	7	15	7
Kitadani et al.²³	2021	Japan	2008–2018	Retrospective	23	15	9
Choi et al.²²	2019	Korea	2008–2016	Retrospective	21	139	9
Nakaji et al.²⁷	2019	Korea	2004–2014	Retrospective	4	18	8
Booka et al.²¹	2019	Japan	2007–2017	Retrospective	8	23	9
Otsuka et al.²⁹	2018	Japan	2008–2017	Retrospective	7	21	8
Luo et al.²⁵	2015	China	2017–2014	Retrospective	9	9	7
Kwon et al.²⁴	2014	Korea	2005–2012	Retrospective	18	58	9
Nagai et al.²⁶	2014	Japan	1996–2012	Retrospective	12	10	8
Son et al.³⁰	2015	Japan	2003–2012	Retrospective	17	17	9

NOS, Newcastle-Ottawa Scales.

Baseline information between the LG group and the OG group

By comparing the baseline information, we found that there was no significant difference in age (MD = −0.12, I² = 0%, 95% CI = −2.51 to 2.27, P = .92), sex (OR = 0.94, I² = 0%, 95% CI = 0.57–1.56, P = .82), BMI (MD = −0.24, I² = 0%, 95% CI = −1.00 to 0.52, P = .54), comorbidity (OR = 0.53, I² = 8%, 95% CI = 0.23–1.24, P = .15), original disease (OR = 0.91, I² = 4%, 95% CI = 0.59–1.40, P = .66), primary reconstruction (P > .05), time interval (MD = 8.53, I² = 0%, 95% CI = −0.64 to 17.69, P = .07), histologic type (OR = 0.75, I² = 0%, 95% CI = 0.40–1.40, P = .36), location (OR = 0.75, I² = 0%, 95% CI = 0.41–1.35, P = .33), TNM stage (P > .05), tumor size (MD = −7.80, I² = 0%, 95% CI = −16.46 to 0.87, P = .08), number of retrieved LN (MD = 1.35, I² = 72%, 95% CI = −1.99 to 4.68, P = .43), or number of metastatic LN (MD = −0.47, I² = 0%, 95% CI = −1.01 to 0.07, P = .09).

We found that the OG group had higher ASA grade (≥2) (OR = 0.24, I² = 54%, 95% CI = 0.08–0.71, P = .01) than the LG group (Table 2).

Table 2.

Summary of Characteristics Between the Laparoscopic Gastrectomy Group and the Open Gastrectomy Group

Characteristics	Studies	Participants (LG/OG)	OR/MD [95% CI]	Model	Heterogeneity
Age (year)	7	119/2315	−0.12 [−2.51 to 2.27]; P = .92	FE	I² = 0%; P = .66
Sex, male	11	162/372	0.94 [0.57 to 1.56]; P = .82	FE	I² = 0%; P = .76
BMI (kg/m²)	5	84/240	−0.24 [−1.00 to 0.52]; P = .54	FE	I² = 0%; P = .78
ASA ≥2	2	57/187	0.24 [0.08 to 0.71]; P = .01	RE	I² = 54%; P = .14
Comorbidity	3	39/77	0.53 [0.23 to 1.24]; P = .15	FE	I² = 8%; P = .34
Original disease
Benign	10	Reference	Reference	Reference	Reference
Malignant	10	157/354	0.91 [0.59 to 1.40]; P = .66	FE	I² = 4%; P = .40
Previous surgical approach
Open	6	Reference	Reference	Reference	Reference
Laparoscopic	6	77/272	3.54 [1.08 to 11.54]; P = .04	RE	I² = 58%; P = .03
Primary reconstruction
Billroth I	7	Reference	Reference		Reference
Billroth II	7	107/166	0.85 [0.50 to 1.46]; P = .56	FE	I² = 0%; P = .85
Roux-en-Y	5	50/69	0.67 [0.22 to 2.02]; P = .47	FE	I² = 0%; P = .78
Other	4	46/45	1.03 [0.37 to 2.90]; P = .95	FE	I² = 0%; P = .81
Time interval (years)	3	27/53	8.53 [−0.64 to 17.69]; P = .07	FE	I² = 0%; P = .77
Histologic type
Differentiated	5	Reference	Reference	Reference	Reference
Undifferentiated	5	88/154	0.75 [0.40 to 1.40]; P = .36	FE	I² = 0%; P = .56
Location
Anastomosis involved	4	Reference	Reference	Reference	Reference
Nonanastomosis	4	88/163	0.75 [0.41 to 1.35]; P = .33	FE	I² = 0%; P = .81
TNM stage
II	10	Reference	Reference	Reference	Reference
I	9	115/142	1.75 [0.70 to 4.36]; P = .23	RE	I² = 57%; P = .02
III	10	57/163	1.25 [0.64 to 2.44]; P = .51	FE	I² = 0%; P = .80
IV	7	19/96	0.88 [0.09 to 8.85]; P = .91	RE	I² = 0%; P = .10
Tumor size (mm)	4	77/220	−7.80 [−16.46 to 0.87]; P = .08	FE	I² = 0%; P = .85
No. of retrieved LN	7	110/266	1.35 [−1.99 to 4.68]; P = .43	RE	I² = 72%; P < .01
No. of metastatic LN	2	57/187	−0.47 [−1.01 to 0.07]; P = .09	FE	I² = 0%; P = .71

ASA, American Society of Anesthesiologists; BMI, body mass index; CI, confidence intervals; FE, fix effect; LG, laparoscopic gastrectomy; LN, lymph node; MD, mean difference; OG, open gastrectomy; OR, odds ratio; RE, random effect; TNM, Tumor Node Metastasis.

Operative and postoperative complications between the LG group and the OG group

We found that the LG group had shorter length of incision (MD = −7.15, I² = 94%, 95% CI = −10.99 to −3.31, P < .01) than OG group.

However, was were no significant difference in blood loss (MD = −77.23, I² = 75%, 95% CI = −167.15 to 12.69, P = .09), anastomotic leakage (OR = 1.39, I² = 0%, 95% CI = 0.40–4.88, P = .61), pancreatic fistula (OR = 0.76, I² = 69%, 95% CI = 0.03–22.86, P = .88), intra-abdominal infection (OR = 3.38, I² = 0%, 95% CI = 0.71–16.03, P = .13), surgical site infection (OR = 0.60, I² = 0%, 95% CI = 0.06–5.66, P = .66), anastomotic stenosis (OR = 1.01, I² = 0%, 95% CI = 0.16–6.44, P = .99), pneumonia (OR = 1.07, I² = 16%, 95% CI = 0.28–4.13, P = .93), postoperative bleeding (OR = 0.71, I² = 0%, 95% CI = 0.18–2.73, P = .62), major complications (OR = 0.45, I² = 0%, 95% CI = 0.19–1.06, P = .07), or overall complications (OR = 0.72, I² = 0%, 95% CI = 0.43–1.23, P = .24) (Table 3).

Table 3.

Operative and Postoperative Complications Between the Laparoscopic Gastrectomy Group and the Open Gastrectomy Group

Characteristics	Studies	Participants (LG/OG)	OR/MD [95% CI]	Heterogeneity
Operative time (minutes)	7	116/314	33.95 [15.05 to 52.85]; P < .01	I² = 58%; P = .03
Postoperative hospital stay	4	73/98	−5.08 [−9.74 to −0.42]; P = .03	I² = 84%; P < .01
Blood loss (mL)	5	88/155	−77.23 [−167.15 to 12.69]; P = .09	I² = 75%; P < .01
Length of incision (cm)	2	45/57	−7.15 [−10.99 to −3.31]; P < .01	I² = 94%; P < .01
Food intake (days)	3	56/81	−3.09 [−4.84 to −1.35]; P < .01	I² = 76%; P = .02
Time to first flatus (days)	3	74/204	−0.84 [−1.09 to −0.59]; P < .01	I² = 0%; P = .67
Anastomotic leakage	5	78/157	1.39 [0.40 to 4.88]; P = .61	I² = −0%; P = .48
Pancreatic fistula	3	43/48	0.76 [0.03 to 22.86]; P = .88	I² = 69%; P = .07
Intra-abdominal infection	2	26/81	3.38 [0.71 to 16.03]; P = .13	I² = 0%; P = .47
Surgical site infection	2	12/41	0.60 [0.06 to 5.66]; P = .66	I² = 0%; P = .87
Anastomotic stenosis	2	59/63	1.01 [0.16 to 6.44]; P = .99	I² = 0%; P = .58
Pneumonia	3	77/121	1.07 [0.28 to 4.13]; P = .93	I² = 16%; P = .30
Postoperative bleeding	4	70/134	0.71 [0.18 to 2.73]; P = .62	I² = 0%; P = .41
Major complications	5	114/277	0.45 [0.19 to 1.06]; P = .07	I² = 0%, P = .74
Overall complications	9	143/342	0.72 [0.43 to 1.23]; P = .24	I² = 0%, P = .71

CI, confidence intervals; LG, laparoscopic gastrectomy; OG, open gastrectomy.

Comparing OS between the LG group and the OG group

There were four studies^22,23,26,31 reporting the OS. No statistically significant difference was found in OS between the LG and OG groups (HR = 0.96, I² = 0%, 95% CI = 0.48–1.93, P = .92) (Fig. 2).

FIG. 2.

Comparing OS between the LG group and the OG group. LG, laparoscopic gastrectomy; OG, open gastrectomy; OS, overall survival.

Comparing clinical outcomes between the LG group and the OG group

Seven studies^{21,22,24,25,29–31} reported operative time and four studies^21,26,30,31 reported postoperative hospital stay. We found that the LG group had longer operative time (MD = 33.95, I² = 58%, 95% CI = 15.05–52.85, P < .01) (Fig. 3a) and shorter postoperative hospital stay (MD = 5.08, I² = 84%, 95% CI = −9.74 to −0.42, P = .03) (Fig. 3b). Three studies^21,26,31 reported food intake and three studies^22,30,31 reported time to first flatus. We found that LG group had earlier food intake (MD = −3.09, I² = 76%, 95% CI = −4.84 to −1.35, P < .01) (Fig. 4a) and earlier time to first flatus (MD = −0.84, I² = 0%, 95% CI = −1.09 to −0.59, P < .01) (Fig. 4a).

FIG. 3.

Comparing operative time (a) and postoperative hospital stay (b) between the LG group and the OG group. LG, laparoscopic gastrectomy; OG, open gastrectomy.

FIG. 4.

Comparing food intake (a) and time to first flatus (b) between the LG group and the OG group. LG, laparoscopic gastrectomy; OG, open gastrectomy.

Publication bias

Publication bias for the included studies was based on a visual inspection of the symmetrical funnel plot. We developed a funnel plot to reflect the heterogeneity of overall complications for the included studies (Fig. 5).

FIG. 5.

Funnel plot of overall complications.

Discussion

A total of 11 studies involving 535 RGC patients who underwent surgery were included in this study. By comparing clinical outcomes between the LG group and the OG group, we found that the LG group had longer operative time, shorter postoperative hospital stay, shorter length of incision, earlier food intake, and earlier time to first flatus. We did not find a statistically significant difference in OS between the LG group and the OG group.

The safety and feasibility of LG in treating gastric cancer have been proven to be noninferior compared with OG.³² Therefore, LG treatment for residual gastric cancer was a technically feasible method, and LG could recover earlier compared to open surgery.²⁴ However, LG for RGC was more difficult than primary cancer due to the technical challenges posed by abdominal adhesions, anatomic displacements, and concerns for radical resection in patients with previous gastrectomy.²⁶ Yamada et al.³³ reported the first case of LG for the treatment of RGC in 2005. Since then, there was an increasing researcher reporting the effect of LG and OG on the clinical outcomes of RGC treatment.

However, for some clinical outcomes, researchers did not reach a consensus. Booka et al.²¹ reported that no statistically significant difference was found in operative time, hospital stay, and food intake between LG and OG. Choi et al.²² reported that LG had longer operative time than OG, and LG has an earlier time to first flatus. However, there was no difference in postoperative hospital stay between LG and OG. Kwon et al.²⁴ found that there was no difference in the time to first flatus between LG and OG, and LG had longer operative time, shorter hospital stay, and earlier feeding than OG. Thus, this study aimed to investigate the specific effect of surgical approach on clinical outcomes in patients with RGC.

In our study, we summarized and compared the clinical outcomes of LG and OG patients with RGC. For clinical outcomes that have not reached consensus, we found that the LG group had longer operative time, shorter postoperative hospital stay, earlier food intake, and earlier time to first flatus. The main reason might be due to the difficult operation of LG, which might take longer time than open surgery. However, LG had minimal trauma and low stress response compared to OG. Thus, LG was more conducive to the recovery of gastrointestinal function, early feeding of patients, and accelerating recovery process.³¹

To the best of our knowledge, this study was the first pooling up analysis to assess the effect of LG and OG on clinical outcomes in patients with RGC. However, some limitations existed in this study. First, only 11 articles were included in the study, which was relatively small. Second, some of these articles had relatively few cases, and all articles were retrospective studies. Third, all studies came from Asia; thus, these results applied to restricted regions. Therefore, comprehensive, prospective, large sample size, and high-quality randomized controlled trials should be conducted to further confirm our results in the future.

In conclusion, we found that the LG group had longer operative time, shorter postoperative hospital stay, shorter length of incision, earlier food intake, and earlier time to first flatus. Due to the difficulty in treating RGC with LG, we suggested that the surgery should be performed by an experienced laparoscopic surgeon.

Footnotes

Acknowledgments

We acknowledge all the authors whose publications are referred to in our article.

Authors' Contributions

Data extraction, Y.-Y.Q. and F.L.; quality assessments, X.-R.L. and W.Z.; data analysis, Z.-W.L. and Y.-Y.Q.; writing-origin draft, Z.-W.L.; and writing-review and editing, Z.-W.L., Y.-Y.Q., and D.P. All authors read and approved the final article.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

References

Tao

, Liu

, Cheng

, et al. Does extended intraoperative peritoneal lavage really bring benefit on patients with gastric cancer? A meta-analysis of Published Clinical Trials. Front Oncol, 2021; 11:715040; doi: 10.3389/fonc.2021.715040

Tanigawa

, Nomura

, Niki

, et al. Clinical study to identify specific characteristics of cancer newly developed in the remnant stomach. Gastric Cancer, 2002; 5(1):23–28; doi: 10.1007/s101200200003

Liao

, Wen

, Xie

, et al. Laparoscopic gastrectomy for remnant gastric cancer: Risk factors associated with conversion and a systematic analysis of literature. Int J Surg, 2016; 34:17–22; doi: 10.1016/j.ijsu.2016.08.013

Komatsu

, Ichikawa

, Okamoto

, et al. Progression of remnant gastric cancer is associated with duration of follow-up following distal gastrectomy. World J Gastroenterol, 2012; 18(22):2832–2836; doi: 10.3748/wjg.v18.i22.2832

Tao

, Cheng

, Zou

, et al. Aorta calcification increases the risk of anastomotic leakage after gastrectomy in gastric cancer patients. Cancer Manag Res, 2021; 13:3857–3865; doi: 10.2147/CMAR.S306942

Mezhir

, Gonen

, Ammori

, et al. Treatment and outcome of patients with gastric remnant cancer after resection for peptic ulcer disease. Ann Surg Oncol, 2011; 18(3):670–676; doi: 10.1245/s10434-010-1425-1

Welvaart

, Warnsinck

. The incidence of carcinoma of the gastric remnant. J Surg Oncol, 1982; 21(2):104–106; doi: 10.1002/jso.2930210208

Cheng

, Tao

, Liu

, et al. The outcome of young vs. old gastric cancer patients following gastrectomy: A propensity score matching analysis. BMC Surg, 2021; 21(1):399; doi: 10.1186/s12893-021-01401-1

Pointner

, Schwab

, Königsrainer

, et al. Early cancer of the gastric remnant. Gut, 1988; 29(3):298–301; doi: 10.1136/gut.29.3.298

10.

Sinning

, Schaefer

, Standop

, et al. Gastric stump carcinoma—Epidemiology and current concepts in pathogenesis and treatment. Eur J Surg Oncol, 2007; 33(2):133–139; doi: 10.1016/j.ejso.2006.09.006

11.

Sasako

. Principles of surgical treatment for curable gastric cancer. J Clin Oncol, 2003; 21(23 Suppl):274s–275s; doi: 10.1200/JCO.2003.09.172

12.

Tsunoda

, Okabe

, Tanaka

, et al. Laparoscopic gastrectomy for remnant gastric cancer: A comprehensive review and case series. Gastric Cancer, 2016; 19(1):287–292; doi: 10.1007/s10120-014-0451-2

13.

Kanaya

, Kawamura

, Kawada

, et al. The delta-shaped anastomosis in laparoscopic distal gastrectomy: Analysis of the initial 100 consecutive procedures of intracorporeal gastroduodenostomy. Gastric Cancer, 2011; 14(4):365–371; doi: 10.1007/s10120-011-0054-0

14.

Shinohara

, Kurahashi

, Kanaya

, et al. Topographic anatomy and laparoscopic technique for dissection of no. 6 infrapyloric lymph nodes in gastric cancer surgery. Gastric Cancer, 2013; 16(4):615–620; doi: 10.1007/s10120-012-0229-3

15.

Lee

, Son

, Lee

, et al. Morbidity and mortality after laparoscopic gastrectomy for advanced gastric cancer: Results of a phase II clinical trial. Surg Endosc, 2013; 27(8):2877–2885; doi: 10.1007/s00464-013-2848-0

16.

Tokunaga

, Hiki

, Fukunaga

, et al. Laparoscopy-assisted gastrectomy for patients with earlier upper abdominal open surgery. Surg Laparosc Endosc Percutan Tech, 2010; 20(1):16–19; doi: 10.1097/SLE.0b013e3181cdebdd

17.

Moher

, Liberati

, Tetzlaff

, et al. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med, 2009; 6(7):e1000097; doi: 10.1371/journal.pmed.1000097

18.

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(2):205–213; doi: 10.1097/01.sla.0000133083.54934.ae

19.

Stang

. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010; 25(9):603–605; doi: 10.1007/s10654-010-9491-z

20.

Ioannidis

. Interpretation of tests of heterogeneity and bias in meta-analysis. J Eval Clin Pract, 2008; 14(5):951–957; doi: 10.1111/j.1365-2753.2008.00986.x

21.

Booka

, Kaihara

, Mihara

, et al. Laparoscopic total gastrectomy for remnant gastric cancer: A single-institution experience. Asian J Endosc Surg, 2019; 12(1):58–63; doi: 10.1111/ases.12495

22.

Choi

, Gong

, Kim

, et al. Clinical outcomes of totally laparoscopic total gastrectomy versus open total gastrectomy for remnant gastric cancer. J Minim Invasive Surg, 2019; 22(1):29–38; doi: 10.7602/jmis.2019.22.1.29

23.

Kitadani

, Ojima

, Nakamura

, et al. Safety and feasibility of laparoscopic gastrectomy for remnant gastric cancer compared with open gastrectomy: Single-center experience. Medicine (Baltimore), 2021; 100(4):e23932; doi: 10.1097/MD.0000000000023932

24.

Kwon

, Cho

, Guner

, et al. Minimally invasive surgery for remnant gastric cancer: A comparison with open surgery. Surg Endosc, 2014; 28(8):2452–2458; doi: 10.1007/s00464-014-3496-8

25.

Luo

, Chen

, Cao

, et al. Hand-assisted laparoscopic versus open radical resection of gastric remnant cancer: A clinical comparison. Int J Clin Exp Med, 2015; 8,(11):21152–21158.

26.

Nagai

, Nakata

, Ohuchida

, et al. Laparoscopic total gastrectomy for remnant gastric cancer: Feasibility study. Surg Endosc, 2014; 28(1):289–296; doi: 10.1007/s00464-013-3186-y

27.

Nakaji

, Saeki

, Kudou

, et al. Short- and long-term outcomes of surgical treatment for remnant gastric cancer after distal gastrectomy. Anticancer Res, 2019; 39(3):1411–1415; doi: 10.21873/anticanres.13256

28.

Ota

, Ikebe

, Shin

, et al. Laparoscopic total gastrectomy for remnant gastric cancer: A Single-institution Experience and Systematic Literature Review. In Vivo, 2020; 34(4):1987–1992; doi: 10.21873/invivo.11996

29.

Otsuka

, Hayashi

, Sakata

, et al. Short-term clinical outcomes of laparoscopic gastrectomy for remnant gastric cancer: A single-institution experience and systematic review of the literature. Ann Gastroenterol Surg, 2018; 3(2):181–186; doi: 10.1002/ags3.12221

30.

Son

, Lee

, Jung

, et al. Laparoscopic completion total gastrectomy for remnant gastric cancer: A single-institution experience. Gastric Cancer, 2015; 18(1):177–182; doi: 10.1007/s10120-014-0339-1

31.

, Song

, Li

, et al. 3D laparoscopic-assisted vs open gastrectomy for carcinoma in the remnant stomach: A retrospective cohort study. World J Gastrointest Surg, 2022; 14(8):754–764; doi: 10.4240/wjgs.v14.i8.754

32.

Kim

, Han

, Kim

, et al. Korean Laparoendoscopic Gastrointestinal Surgery Study (KLASS) Group. Effect of laparoscopic distal gastrectomy vs open distal gastrectomy on long-term survival among patients with Stage I Gastric Cancer: The KLASS-01 Randomized Clinical Trial. JAMA Oncol, 2019; 5(4):506–513; doi: 10.1001/jamaoncol.2018.6727

33.

Yamada

, Kojima

, Yamashita

, et al. Laparoscopy-assisted resection of gastric remnant cancer. Surg Laparosc Endosc Percutan Tech, 2005; 15(4):226–229; doi: 10.1097/01.sle.0000174546.41307.02