Abstract
Background/Aim: The optimal reconstruction method for laparoscopic proximal gastrectomy (LPG) remains controversial. The present study aimed to compare short-term outcomes, including assessment of nutritional parameters and skeletal muscle, between two different methods, double-tract reconstruction (DTR) versus esophagogastrostomy (EG). Patients and Methods: Data from patients who underwent LPG for gastric tumor(s) between 2018 and 2021, were retrospectively analyzed. Patients were divided into two group: DTR (n=11) and EG (n=17). Since 2020, the authors have applied the modified side overlap with fundoplication by Yamashita (mSOFY) method as the EG technique. Results: Compared with DTR, EG was associated with a shorter reconstruction time (p=0.003). Complications of grade ≥3 occurred only in the EG group [n=4 (23.5%)] and the incidence of abnormal endoscopic findings after surgery was numerically higher in the EG group (n=2 vs. n=9; p=0.047). Across virtually all data points on the line graph, the EG group exhibited greater changes in post-discharge nutritional parameters, with Skeletal Muscle Index also demonstrating significant superiority (0.83 vs. 0.89; p=0.045). Conclusion: Among reconstruction methods for LPG, EG demonstrated superiority over DTR in preserving nutritional parameters and skeletal muscle mass. However, further research, including larger cohorts and longer-term follow-up, is necessary to validate this finding.
- Laparoscopic proximal gastrectomy
- esophagogastrostomy
- mSOFY
- double tract reconstruction
- Skeletal Muscle Index
Gastric cancer is a major disease worldwide, ranking as the fifth most common cancer and the third most common cause of cancer-related deaths (1). Surgical resection with lymph node dissection remains the only curative treatment, with distal or total gastrectomy being the standard procedure(s). However, a paradigm shift toward proximal gastrectomy has occurred, and the indications for early-stage upper gastric cancer have expanded substantially (2-5). Previous studies have reported advantages in nutritional aspects and non-inferiority in oncological aspects of proximal compared with total gastrectomy (6-8). Furthermore, the incidence of proximal gastric cancers has steadily increased (9). Laparoscopic proximal gastrectomy (LPG) is a standard approach, and several reconstruction methods, including jejunal interposition (10), double-tract reconstruction (DTR) (11), and esophagogastrostomy (EG) (3, 12-16), have been used. Up to 2019, we performed DTR and, in 2020, we introduced one of the EG techniques, a modified side overlap with fundoplication by Yamashita (mSOFY) (12). Most recently, EG has been highlighted due to its simplicity; however, there is diversity, even among EG techniques, resulting in ongoing controversy regarding the optimal reconstruction method(s).
Sarcopenia and low skeletal muscle mass have emerged as poor prognostic factors in oncology and transplant research (17-19). For patients with gastric cancers, malnutrition, and body weight loss after surgery have deleterious impacts and their prevention remains a pivotal issue for adjuvant therapy for advanced cancer (20). A previous study reported that total and proximal gastrectomy were involved in the occurrence of weight loss (2); however, the association between the skeletal muscle mass and each reconstruction method for LPG remains poorly documented. The present study aimed to investigate short-term outcomes, including the estimation of nutrition and skeletal muscle mass, for two different reconstruction methods (i.e., EG versus DTR).
Patients and Methods
Patients. The protocol for this single-center, retrospective study was approved by the Ethics Committee of Tenri Hospital (approval code 1301), and the requirement for written informed consent was waived. Prospectively collected data from patients who underwent LPG for gastric tumor(s) at Tenri Hospital between 2018 and 2021 were retrieved. Follow-up data for these patients were updated in December 2022. LPG was indicated for patients with clinically diagnosed early gastric cancer and other tumors (e.g., gastrointestinal stromal and neuroendocrine tumors) in the upper stomach.
Surgical procedure. For LPG, 5 working ports were inserted into the umbilicus (12 mm), right upper quadrant (5 mm), right lower quadrant (12 mm), left upper quadrant (5 mm), and left lower quadrant (12 mm). For all patients with adenocarcinoma, D1+ lymphadenectomy was performed according to the Japanese Gastric Cancer treatment guidelines (21) and was omitted for other tumors. After securing the margin from tumor with endoscopy, the stomach and abdominal esophagus were transected intracorporeally using linear staplers and the dissected stomach was extracted through a supraumbilical incision. Subsequently, reconstruction was performed after confirming R0 status. For all patients, DTR was performed up to 2019, and the mSOFY method, which is one of the EG techniques, since 2020.
For DTR, esophagojejunostomy and gastrojejunostomy were performed intracorporeally, and jejunojejunostomy was performed extracorporeally via mini-laparotomy using a linear stapler. The distances between the gastrojejunostomy, and both the esophagojejunostomy and the jejunojejunostomy, were estimated to be 15-20 cm, respectively.
In the mSOFY method, the bilateral diaphragmatic crus were dissected to enhance gastric elevation and it was confirmed that the esophagus overlapped ≥5 cm at the center of the remnant stomach before EG (Yamashita et al. call it SOFY check). A 45 mm linear stapler was inserted into the esophagus and stomach, and the right-side wall of the esophagus and the anterior wall of the remnant stomach were anastomosed. The left side of esophagus and remnant stomach were sutured at 3 points so that the esophagus was adhered flat to the gastric wall. The staple line of the esophageal stump was buried sutured to complete the reconstruction. Other detailed procedures were performed according to the original studies (12).
Data collection. Clinicopathological characteristics included age, sex, height/weight, body mass index (BMI), hemoglobin, cholinesterase, albumin, total protein, and indication(s) for surgery. Operative variables included duration, reconstruction duration, blood loss, length of dissected abdominal esophagus and postoperative hospital stay, complications (per Clavien-Dindo classification version 2.0) (22), and receipt of adjuvant chemotherapy. All patients underwent laboratory investigations and assessment of clinical symptoms every 3 months, computed tomography (CT) at 6-month intervals, and upper gastrointestinal endoscopy at 1 year after surgery unless there was a confirmed relapse.
Outcomes. Patients were classified into 1 of 2 groups according to surgical procedure: EG and DTR. The primary outcome was skeletal muscle index (SMI), which was measured and compared at the time before surgery and six months after surgery. The axial and transversal psoas muscle at the level of the L3 vertebra were measured in all patients based on abdominal CT at both time points (18). SMI was calculated using a simplified version of the following equation:
The secondary endpoints were other short-term outcomes, including the following: surgical characteristics (operative duration, reconstruction duration, blood loss, length of postoperative hospital stay); postoperative complications; body weight, changes in nutritional parameters after discharge; and abnormal endoscopic findings (e.g., reflux esophagitis and anastomotic stenosis) 1 year after surgery. Nutritional parameters, including hemoglobin, serum cholinesterase, albumin, and total protein, were evaluated every 3 months. The presence of reflux esophagitis was defined based on grades B-D of the Los Angeles classification (23), and the presence of anastomotic stenosis was defined as requiring endoscopic dilatation.
Statistical analyses. Continuous variables are expressed as median (range) and were compared using the Mann-Whitney U-test. Categorical variables were compared using the chi-squared test or Fisher’s exact test. All tests were two-tailed, and differences with p<0.05 were considered to be statistically significant. Statistical analysis was performed using JMP version 16.0 (SAS Institute, Inc., Cary, NC, USA).
Results
Patients. A flow-diagram illustrating patient inclusion in presented in Figure 1. A total of 257 consecutive patients, who underwent gastrectomy during the study period, were identified. Twenty-eight patients who underwent LPG were included as per the eligibility criteria for the study. Among the patients, 11 (39.3%) underwent DTR and 17 (60.7%) underwent EG.
Flow-diagram illustrating patient inclusion.
Patient characteristics and surgical outcomes. Clinical characteristics and surgical outcomes are summarized in Table I. There were no significant intergroup differences in basic patient characteristics. Regarding surgical outcomes, the EG group had a shorter reconstruction time (p=0.003), with no differences observed in other surgical outcomes. Complications of grade ≥3 occurred exclusively in the EG group [n=4 (23.5%)], characterized as the following anastomotic problems: leakage (n=2); ulcer (n=1); and stenosis (n=1).
Clinicopathological characteristics and surgical outcomes of patients undergoing laparoscopic proximal gastrectomy.
Postoperative outcomes after discharge. Postoperative outcomes after discharge in the DTR and EG groups are summarized in Table II. The incidence of abnormal endoscopic findings after surgery was significantly greater in the EG group [n=2 (18.1%) vs. n=9 (56.2%); p=0.047], comprising reflux esophagitis (n=1 and 4, respectively) and anastomotic stenosis (n=1 and 5, respectively). All patients who experienced reflux esophagitis in the EG group exhibited esophageal invasion, and all those with stenosis had undergone surgery during the introduction period. The endoscopic favorable observation of remnant stomach was significantly more prevalent in the EG group. The SMI in the 2 groups was 6.71 and 6.80 (p=0.906), and the post/preoperative ratio of SMI in the EG group was significantly higher than that in the DTR group (0.83 vs. 0.89, respectively; p=0.045) (Figure 2A).
Postoperative outcomes after discharge in the double tract reconstruction (DTR) and esophagogastrostomy (EG) groups.
Post/Pre-operative ratio of Skeletal Muscle Index (SMI) (A) in the double tract reconstruction (DTR) and esophagogastrostomy (EG) groups and (B) in the length of resected abdominal esophagus <2 cm and ≥2 cm in the EG group.
Assessment of changes in nutritional parameters. Changes in the ratio of each nutritional parameter, from 1-month preoperatively to 1-, 6-, and 12-months after surgery, are summarized in Figure 3. For three parameters (hemoglobin, cholinesterase, albumin), the line graphs for the EG group exceeded those of the DTR group. Furthermore, in the EG group, cholinesterase level ratio was significantly higher at 1 month (0.85 vs. 0.75; p=0.029), and albumin level ratio tended to be higher at 6 months after surgery (0.98 vs. 0.88; p=0.081).
Changes in nutritional parameters after surgery in the double tract reconstruction (DTR) and esophagogastrostomy (EG) groups. Hb: Hemoglobin; ChE: cholinesterase; Alb: albumin; TP: total protein.
Association between abdominal esophageal resection distance and SMI. Additionally, postoperative outcomes in the EG group were divided based on the length of resected abdominal esophagus (≥2 cm and <2 cm) (Table III). Reflux esophagitis occurred only in patients with length ≥2 cm (n=4 and 0; p=0.019), and the SMI tended to be associated with the distance (0.86 vs. 0.93; p=0.079 (Figure 2B).
Postoperative outcomes after discharge in length of resected abdominal esophagus ≥2 cm and <2 cm in the esophagogastrostomy (EG) group.
Discussion
The present study aimed to investigate the short-term outcomes of LPG using two different reconstruction methods—DTR and EG—focusing on the evaluation of skeletal muscle and nutritional parameters. The EG method resulted in a high incidence of short-term complications during the early introduction period and a high frequency of long-term complications, such as reflux esophagitis, in cases involving esophageal invasion. However, in terms of postoperative nutritional status and reduction in skeletal muscle mass, the EG method yielded superior outcomes compared to DTR. Our findings shed light on the potential benefits and challenges associated with these reconstruction methods, providing valuable insights for clinical practice and further research.
In LPG, various reconstruction methods, including DTR, jejunal interposition, and EG (11), have been used; however, a unified consensus regarding the optimal method remains elusive. DTR and jejunal interposition, which require three anastomoses, are complex and time-consuming, while EG presents issues with reflux esophagitis. Although previous studies have explored the association between reconstruction methods and nutritional status or weight loss (14, 24), few have investigated changes in skeletal muscle mass. Given the emerging importance of sarcopenia as a prognostic factor, addressing postoperative weight loss remains a crucial challenge in gastrectomy.
Sarcopenia is considered a poor prognostic factor in patients receiving adjuvant chemotherapy for gastric cancer (25). Although proximal gastrectomy was initially intended for early-stage cancer(s), its indications have expanded to include advanced cancers, with adjuvant chemotherapy administered after surgery. Prioritizing reconstruction methods that focus on nutrition and skeletal muscle is essential for long-term prognosis, leading to the novel insight that EG may be superior based on the results of the present study.
A shorter reconstruction time was associated with EG; however, complications of grade ≥3, including anastomotic problems, were exclusively observed in this group, emphasizing the need to carefully consider risks and benefits when choosing between reconstruction methods. However, the EG group demonstrated a significant difference in the post/preoperative ratio of skeletal muscle index (SMI), suggesting its positive impact on preserving skeletal muscle mass compared with DTR. Because sarcopenia and low SMI are associated with poor prognosis in cancer (25), the potential of EG in maintaining skeletal muscle is crucial for clinical outcomes and quality of life.
Furthermore, in this study, we demonstrated an association between the resected length of abdominal esophagus and reflux esophagitis in the EG group. The inventors of the SOFY method, Yamashita et al., also emphasized the importance of overlapping the remnant stomach and abdominal esophagus by at least 5 cm from the perspective of preventing reflux (12). Hence, other methods may be more suitable for patients requiring extensive resection of the abdominal esophagus, such as those with esophagogastric junction cancer, or those with esophageal invasion.
This study has several limitations, the first of which were the relatively small sample size and single-center, retrospective design. The most significant concern was the presence of surgeon bias. The lack of standardization among surgeons and potential lack of technical proficiency in the early introduction of the mSOFY method may have influenced the outcomes. However, it should be noted that, despite these challenging conditions, favorable results were achieved in the EG group. Second, only one type of EG— the mSOFY method—was performed. Evaluating the outcomes based on a small number of cases may have led to an overestimation of the results. A multicenter trial, including various types of EG (26, 27), is needed for further validation.
Conclusion
Among reconstruction methods for LPG, EG demonstrated superiority over DTR in the preservation of nutritional parameters and skeletal muscle mass. Further research including larger cohorts and longer-term outcomes is necessary to validate these findings and provide more comprehensive evidence to support clinical practice.
Acknowledgements
The Authors thank Editage (www.editage.com) for English language editing.
Footnotes
Authors’ Contributions
Koshiro Morino mainly acquired and analyzed the data, and wrote the original draft. Koshiro Morino, Taku Kitano, and Yoshio Kadokawa designed the research. Koshiro Morino and Taku Kitano interpreted the data, and contributed to writing and editing the manuscript. Koshiro Morino, Taku Kitano, Yoshio Kadokawa, Nozomu Nakanishi, and Takafumi Machimoto participated in the data acquisition. Yoshio Kadokawa supervised the research design, interpretation of the data, and contributed to editing the manuscript. All Authors participated in critical revision of the manuscript for important intellectual content.
Conflicts of Interest
There are no conflicts of interest or funding sources to declare in relation to this study.
- Received December 20, 2023.
- Revision received January 22, 2024.
- Accepted January 23, 2024.
- Copyright © 2024, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved
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