Short‐term clinical outcomes of laparoscopic gastrectomy for remnant gastric cancer: A single‐institution experience and systematic review of the literature

Abstract Aim Application of laparoscopic approaches for the treatment of remnant gastric cancers (RGC) is still controversial. Therefore, in the present study, the safety and effectiveness of laparoscopic gastrectomy (LG) for RGC was investigated. Methods A total of 27 patients who underwent gastrectomy for RGC from June 2008 to September 2017 were enrolled in this study. A comprehensive review of the literature on LG for RGC published before December 2017 using the PubMed database was carried out. Results Laparoscopic gastrectomy was carried out in seven patients, and open gastrectomy (OG) was done in the remaining 20 patients. LG was associated with significantly less intraoperative blood loss (70 ± 71 vs. 1066 ± 1428 g; P < 0.001), significantly more retrieved lymph nodes (22 ± 13 vs. 12 ± 9; P = 0.03), a relatively lower postoperative complication rate, and a relatively shorter postoperative hospital stay than OG. A comprehensive review of the literature showed that LG for RGC was more likely to correlate with longer operative time, less blood loss, lower postoperative complication rate, shorter postoperative hospital stay, and more retrieved lymph nodes than OG. Conclusion The clinical outcome of our patients with RGC and the literature indicated that a laparoscopic approach contributed to faster recovery after surgery than an open approach without sacrificing its radicality and was a safe and secure treatment option for RGC.


| INTRODUC TI ON
Remnant gastric cancers (RGC) were initially defined as gastric cancer that occurs after gastrectomy for benign disease. 1 It now represents all cancers developed in the remnant stomach, regardless of the malignancy of the initial disease. [2][3][4] Although chemotherapy and radiotherapy have been developed in the field of treatment for gastric cancer, gastrectomy with adequate lymphadenectomy remains the first treatment option for resectable gastric cancers. 5,6 With the expansive application of laparoscopic surgeries for gastric cancer, the first case of laparoscopic gastrectomy (LG) for RGC was reported by Yamada et al in 2005. 7 Several other reports with similar LG for RGC have followed since then. However, the number of cases reported has remained small due to the rarity of RGC, 8 and the usability of laparoscopic approaches for the treatment of RGC is still unclear.
Therefore, the purpose of the current study was to investigate the safety and effectiveness of LG for RGC. To that end, we com-

| Patients
A total of 27 patients who underwent gastrectomy for RGC at Chiba University Hospital from June 2008 to September 2017 were enrolled in this study.
LG was carried out in seven patients, and OG was done in the remaining 20 patients. Stage of the disease was determined according to the TNM classification (UICC 8th edition), 9 and the severity of the postoperative complications was estimated according to the Clavien-Dindo classification. 10 This study was in agreement with the guidelines of the institutional ethics committee and was conducted in accordance with the Declaration of Helsinki.

| Surgical procedures
Indication for a laparoscopic procedure for primary gastric cancer at our institution is a preoperative diagnosis of stage 1A to stage 2A disease. As such, the same criterion was applied to the patients with RGC.
Under general anesthesia, the patient was placed in the supine position with the legs apart. Then, a 12-mm camera port was placed in either the umbilical or left subcostal area by the open method. CO 2 insufflation was maintained at 10 mm Hg, and four working ports were placed, as described previously. 11,12 Adhesiolysis was carried out with one or two working ports if needed for insertion of the other trocar. Dissection around the previous anastomosis was carried out, and the duodenum was divided at the immediate anal side of the anastomosis. Additional lymphadenectomy was done according to the recommendations of the guidelines, 6 with the corresponding tumor location of the original stomach, if necessary. After the resected specimen was removed, continuity of the alimentary tract was resumed intracorporeally with Roux-en-Y reconstruction.

| Literature review
We explored the PubMed database for English language case reports, case series, and case comparative studies of LG for RGC published before December 2017 using the following key words: "remnant gastric cancer" OR "gastric remnant cancer" OR "gastric stump cancer" AND "gastrectomy" AND "laparoscopy." Related citations of all relevant articles were assessed to identify other related reports.

| Statistical analyses
All statistical analyses were carried out using the IBM SPSS Statistical significance was defined as a P value < 0.05.

| Patient characteristics
Clinicopathological features of the patients are summarized in

| Clinical outcomes of our series
Basic characteristics, such as age, gender, body mass index (BMI), previous disease type, previous surgical approach, and time interval of operations, were compared between the LG and OG groups, with no statistically significant differences noted (Table 2). Regarding the surgical outcome, we compared operative time, blood loss, and number of retrieved lymph nodes between the groups (

| Review of the literature
Six case-control studies, seven case series and three case reports on LG for RGC were retrieved by our literature search (Table 4). 2-4,7,13-24 One institution reported a case-control study 2 after the publication of a case series. 25 Therefore, the latter case series was excluded from the analysis to avoid double inclusion of the cases.
In the 17 total studies, including our own, 128 patients under- Seven studies, including our own, conducted comparative analyses between LG and OG for RGC. Although all studies showed a longer operative time for LG than for OG, a lower postoperative complication rate with LG was observed in six studies. Furthermore, blood loss was lower and postoperative hospital stay was shorter in five of the six studies, and more lymph nodes were retrieved with LG than with OG in four of the six studies.

| D ISCUSS I ON
The aim of the present study was to examine the safety and effectiveness of LG for RGC. A comparative study of RGC in our institution indicated that LG was associated with significantly less intraoperative blood loss, significantly more retrieved lymph In our study, a benign previous disease type was significantly associated with a longer interval between operations and more retrieved lymph nodes but not with operative time or blood loss ( In summary, our analyses indicated that laparoscopic gastrectomy was associated with significantly less intraoperative blood loss, significantly more retrieved lymph nodes, a relatively lower postoperative complication rate, and a relatively shorter postoperative hos- pital stay than open gastrectomy. Therefore, a laparoscopic approach may be a safe and secure treatment option for remnant gastric cancer as well as for primary gastric cancers.

D I SCLOS U R E
This study was in agreement with the guidelines of the institutional ethics committee and was conducted in accordance with the Declaration of Helsinki.
Conflicts of interest: Authors declare no conflicts of interests for the present article.