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ORIGINAL ARTICLE
Year :   |  Volume :   |  Issue :   |  Page :
 

Feasibility of laparoscopic proximal gastrectomy with piggyback jejunal interposition double-tract reconstruction for proximal gastric cancer: A propensity score-matching analysis


 Department of Minimal Invasive Digestive Surgery, Shanxi Cancer Hospital, Affiliated To Shanxi Medical University, Taiyuan, Shanxi, PR China

Date of Submission29-Jan-2022
Date of Decision30-Mar-2022
Date of Acceptance20-Apr-2022
Date of Web Publication02-Jun-2022

Correspondence Address:
JianHong Dong,
Department of Minimal Invasive Digestive Surgery, Shanxi Cancer Hospital, Affiliated to Shanxi Medical University, Taiyuan, Shanxi
PR China
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jmas.jmas_46_22

  Abstract 


Background: The feasibility of using laparoscopic proximal gastrectomy (LPG) for the treatment of proximal early gastric cancer (EGC) has not been addressed. This study aimed to comparatively evaluate the effects on LPG with piggyback jejunal interposition double-tract reconstruction (PJIDTR) versus laparoscopic total gastrectomy (LTG) with Roux-en-Y reconstruction (overlap method) using propensity score matching for proximal EGC.
Materials and Methods: We examined the clinical outcomes of LPG with PJIDTR for proximal EGC. We retrospectively collected data from patients with proximal EGC who were treated at Shanxi Cancer Hospital between January 2012 and December 2015. The complication rate, nutritional indicators, reflux oesophagitis incidence and overall survival were compared between LTG and LPG with PJIDTR.
Results: Of the 424 patients, 200 were excluded, and 50 of the remaining patients received LPG with PJIDTR. Fifty matched LTG patients were screened. The incidence of early complications was 14% in the LPG group and 16% in the LTG group (P > 0.05). At 1 year after surgery, nutrition indices in the LPG group were significantly better than those in the LTG group (P < 0.05). One year after surgery, the Visick score II rate was 2% and 4%, and the endoscopic oesophagitis rate was 4% and 6% in the LPG and LTG groups, respectively. No tumour recurrence was observed in either group. The 5-year overall survival rates of the two groups were 98% and 90% (P = 0.08).
Conclusions: LPG with PJIDTR may be suitable for proximal EGC.


Keywords: Double-tract, laparoscopic, piggyback jejunal interposition, proximal gastrectomy, proximal gastric cancer, total gastrectomy



How to cite this URL:
Li Z, Dong J, Huang Q. Feasibility of laparoscopic proximal gastrectomy with piggyback jejunal interposition double-tract reconstruction for proximal gastric cancer: A propensity score-matching analysis. J Min Access Surg [Epub ahead of print] [cited 2022 Jul 3]. Available from: https://www.journalofmas.com/preprintarticle.asp?id=346497





  Introduction Top


In recent years, the incidence of proximal gastric cancer has increased. GLOBOCAN data show that there were 952,000 new cases of gastric cancer worldwide in 2012, including 260,000 cases of cardiac cancer, and 52% (135,000 cases) were in China.[1] Among 7887 patients with gastric cancer admitted to Shanxi Cancer Hospital from 2011 to 2016, proximal gastric cancer accounted for 40.4% of cases. In Korea, the incidence of proximal gastric cancer increased from 11.2% in 1995 to 16.0% in 2014.[2]

Proximal gastrectomy (PG) for proximal early gastric cancer (EGC) has been widely accepted in Japan and South Korea. This procedure provides the same overall survival as total gastrectomy (TG)[3] but provides the patient with a better ability to eat and a better quality of life.[4],[5],[6] In contrast, TG is routinely performed for proximal EGC and advanced oesophagogastric junction carcinoma in western countries.[3] PG is recommended when greater than half of the stomach is preserved, as many studies have shown better nutritional status after PG than after TG.[7],[8],[9],[10] Given the lack of a difference in survival between PG and TG, patients who underwent extensive lymphadenectomy do not benefit from this procedure.[11] A 2019 retrospective analysis of 202 upper one-third gastric cancer patients with pT2/T3 staging in Japan showed that the rate of lymph node (LN) metastasis was very low in No. 4d and No. 12a. However, the rate of LN metastasis was zero in No. 5 and No. 6. These results suggest that PG is a safe option for upper one-third gastric cancer with T2/T3 stage disease.

The development of laparoscopic technology has led to the gradual application of laparoscopic gastrectomy in the clinic.[12],[13],[14],[15] The wide application of laparoscopic PG (LPG) in the clinic has not been accepted.[16],[17] According to a nationwide survey conducted by the Japan Endoscopic Surgery Society, approximately 2800 gastric cancer patients underwent LPG surgery from 1994 to 2013. The proportion of LPG surgery has increased gradually. In 2013, the number of LPG surgeries was not only higher than that of open PG surgeries but also accounted for 4.6% of the total laparoscopic gastric cancer surgeries in Japan.[18] Although there is not sufficient evidence to demonstrate that laparoscopic surgery is superior to open surgery in the treatment of proximal EGC, Japan has made some progress in LPG.

Our previous study reported the short-term efficacy of open PG with piggyback jejunal interposition double-tract reconstruction (PJIDTR).[19] In particular, the efficacy of LPG with PJIDTR remains unclear due to the lack of short- and long-term studies.

The purpose of this retrospective cohort study was to compare LPG with PJIDTR versus laparoscopic TG (LTG) with Roux-en-Y reconstruction (overlap method) in terms of oncological safety, functional benefit, complications and reflux oesophagitis in patients with proximal EGC.


  Materials and Methods Top


Ethics statement

This study was a retrospective cohort study. This study was approved by the Ethics Committee of Shanxi Cancer Hospital (approval no. 202028). All participants signed a written informed consent form, and all methods were performed in accordance with the Declaration of Helsinki.

Patients

The clinical data of patients who underwent laparoscopic upper gastric tumour resection in Shanxi Cancer Hospital from January 2012 to December 2015 were collected retrospectively. In this study, upper gastric cancer refers to a tumour located in the upper one-third of the stomach after the tripartite division of the greater curvature and lesser curvature. The inclusion criteria included the following: (1) pre-operative endoscopic and pathological diagnosis was confirmed as gastric cancer, and all were early cancers; (2) age ≥18 years; (3) all operations were performed under a microscope, and the post-operative pathological diagnosis was R0 resection; (4) tumour size <4 cm and (5) no history of abdominal surgery. The exclusion criteria included the following: (1) lack of clinical data; (2) emergency surgery or switch to open surgery; (3) clinical advanced stage >cT2; (4) age <18 years and (5) oesophageal invasion.

Patients were divided into two groups: the LPG group and the LTG group. Patients with R1 resection were excluded from this study due to a lack of statistical significance. Propensity score-matching analysis was performed according to age, sex, body mass index (BMI), American Society of Anesthesiologists (ASA) score, degree of differentiation and pathological stage [Table 1]. In total, 100 patients were included based on 1:1 propensity matching [Figure 1].
Table 1: Patient characteristics

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Figure 1: Flowchart of patient selection and propensity score matching. 50 patients who underwent LPG were matched to 50 patients who underwent LTG in terms of age, sex, body mass index, differentiation, pathological stage and ASA score. LPG: Laparoscopic proximal gastrectomy, LTG: Laparoscopic total gastrectomy, ASA: American Society of Anesthesiologists

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Surgical procedure

All surgeries were performed by the same team of surgeons with extensive laparoscopic experience.

Laparoscopic proximal gastrectomy with piggyback jejunal interposition double-tract reconstruction

The LPG procedures were performed by the 5-port technique under general anaesthesia. The patient was supine with legs divided, and the cephalic side was slightly higher (approximately 15°). After thoroughly examining the internal organs, dissection of D1+ LNs for proximal gastric cancer was performed, and the Nos. 1, 2, 3a, 4sa, 4sb, 7, 8a, 9 and 11p LNs were included in the proximal stomach (approximately 2/3). The digestive tract reconstruction process is as follows. The gastric wall was cut off in a region of the greater curvature of the stomach that lacks vasculature with a laparoscopic linear cutting and closure device (EC60A, ECR60B, Ethicon Endo-Surgery, Inc., Ltd., Guaynabo, Puerto Rico, USA), and greater than half of the residual stomach was preserved. A ligature band was used 1 cm above the cardia and led caudally. An incision of 1 cm was made in the left anterior wall of the oesophagus and the jejunum wall 20 cm from Treitz. The laparoscopic linear cutting and closing device (EC60A, ECR60B, Ethicon Endo-Surgery, Inc., Guaynabo, Puerto Rico, USA) was extended into the oesophageal cavity and the jejunum cavity, and oesophagojejunal anastomosis was performed side to side. The laparoscopic linear cutting and closing device (EC60A, ECR60B, Ethicon Endo-Surgery, Inc., Guaynabo, Puerto Rico, USA) closes the common opening while the PG specimen is resected. A 1-cm incision was made in the jejunum wall and the posterior wall of the greater curvature of the remnant stomach at a distance of 12–15 cm from the oesophagojejunostomy. A laparoscopic linear cutting closure device (EC60A, ECR60B, Ethicon Endo-Surgery, Inc., Guaynabo, Puerto Rico, USA) was inserted into the two incisions to perform the side-to-side gastrojejunostomy. Then, the common opening was closed. A 1-cm incision was made near the broken end of the jejunum and the jejunum wall 30 cm away from the distal end of the gastrojejunal anastomosis, and a laparoscopic linear cutting closure device (EC60A, ECR60B, Ethicon Endo-Surgery, Inc., Ltd., Guaynabo, Puerto Rico, USA) was inserted to perform the jejunum–jejunum side-to-side anastomosis. Satisfactory anastomosis was assessed, and the common opening was subsequently closed [Figure 2]. The specimen was subsequently removed through the umbilical port site by extending the incision.
Figure 2: Laparoscopic proximal gastrectomy with PJIDTR. There are three anastomosis: oesophagojejunostomy, gastrojejunostomy and jejunojejunostomy, respectively. PJIDTR: Piggyback jejunal interposition double-tract reconstruction

Click here to view


Laparoscopic total gastrectomy with Roux-en-Y reconstruction (overlap method)

The patient's anaesthesia, body position and working port position should be the same as those of LPG. After thoroughly examining the internal organs, dissection of D1 + LNs for total gastric cancer was performed, and the range of No. 1, 2, 3, 4sa, 4sb, 4d, 5, 6, 7, 8a, 9 and 11p LNs was included in the total stomach. Roux-en-Y oesophagojejunostomy (overlap method) was performed after the gastrectomy. After the abdominal oesophagus was completed, exposed and dissociated, it was rotated 90° clockwise. The oesophagus was severed using a laparoscopic linear cutting closure device (EC60A, ECR60B, Ethicon Endo-Surgery, Inc., Guaynabo, Puerto Rico, USA) with a sagittal tangent. The oesophageal stump is located in the middle (it can also be on one side). Two barbed wires were sutured and suspended 0.5–1 cm apart. The oesophageal stump between the barbed wires is cut, and the gastric tube is guided for confirmation. A linear cutting and closing device (EC60A, ECR60B, Ethicon Endo-Surgery, Inc., Guaynabo, Puerto Rico, USA) was inserted into the jejunum 25 cm from the Treitz ligament in the peristaltic direction of the mesangial margin, and the upper jejunum was prepared for anastomosis. The surgeon and assistant pulled the stump of the oesophagus with the barbed wire and placed the narrow arm of the linear cutting closure device into the oesophageal cavity under the guidance of the gastric tube, paying attention to avoid accidentally clamping the diaphragm and gastric tube. After stimulation, the anastomosis was assessed, and a double suture of the barbed wire closed the common opening. The input loop jejunum was severed 2–3 cm away from the anastomosis, and Y anastomosis was completed with a linear cutting and closure device 50 cm away from the oesophageal jejunum anastomosis. Satisfactory anastomosis was assessed, and the common opening was subsequently closed. The specimen was subsequently removed through the umbilical port site by extending the incision.

Clinical analysis and surgical outcomes

The patients were followed up 5 years after surgery. The patients were followed up by telephone and returned to the hospital regularly for review. The following data were recorded and analysed: age, sex, BMI, ASA score, tumour differentiation, pathological stage based on the American Joint Committee on Cancer/Union for International Cancer Control 8th Edition,[20] operation time, blood loss and the number of retrieved LNs. The post-operative evaluation indices included the first anal exhaust time, post-operative hospital stay and early complications. Follow-up outcomes included nutrition indices, including BMI, haemoglobin, total serum protein and serum albumin. The Visick score[21] was used to evaluate gastro-oesophageal reflux symptoms 1 year after surgery: Visick Grade I, asymptomatic; Visick Grade II, occasional symptoms; Visick Grade III, apparent but tolerable symptoms and Visick Grade IV, apparent and intolerable symptoms. All patients underwent post-operative endoscopy to evaluate gastro-oesophageal reflux according to the Los Angeles Classification System.[22] Death and cause of death were determined through follow-up, and the cause of disease was assessed.

Statistical analysis

All statistical analyses were performed with SPSS software version 26.0 for Windows (SPSS, Chicago, IL, USA). Continuous variables were compared between the LPG and LTG groups using Student's t-test, and categorical variables were compared using the Chi-squared test or Fisher's exact test. The Kaplan–Meier method was used to calculate the survival rate. The difference between the curves was assessed using the log-rank test. P < 0.05 was considered statistically significant.


  Results Top


A total of 424 patients with proximal gastric cancer who received surgical treatment were included in the study. In total, 200 of these patients were excluded based on the exclusion criteria as follows: 80 patients with clinical advanced stage > cT2, 90 patients who lacked clinical data, 20 patients who had oesophageal invasion, seven patients who were switched to open surgery or emergency surgery and three patients aged <18 years. The remaining 224 patients with proximal EGC were screened by admittance criteria: 163 patients underwent LTG with Roux-en-Y reconstruction, and 50 patients underwent LPG with PJIDTR [Figure 1].

The baseline characteristics of the two groups were well balanced (P > 0.05). Comparison of intraoperative indicators, operative time, blood loss and the number of retrieved LNs between the two groups showed no statistical significance (P > 0.05) [Table 1].

Post-operative recovery indices, including the first anal exhaust time, post-operative hospital stay and early complications (within 1 month after operation), were not significantly different (P > 0.05) [Table 1].

As shown in [Table 2], significant differences in BMI, haemoglobin, total serum protein and serum albumin were noted between the two groups 1 year after the operation (P < 0.05). Visick scoring of the reflux symptoms 1 year after surgery showed that one patient in the LPG group and two patients in the LTG group had Grade II reflux. These patients did not report any further reflux symptoms at the time of the next follow-up.
Table 2: Post-operative outcomes and nutrition indices

Click here to view


As shown in [Table 3], endoscopy was performed on all patients 1 year after surgery. The pre-operative and post-operative endoscopic scores of all patients were determined according to the Los Angeles Classification of reflux oesophagitis. In the LPG group, five cases of Grade A and one case of Grade B reflux oesophagitis developed preoperatively. Two cases of Grade A reflux oesophagitis developed postoperatively in the LPG group. In the LTG group, four Grade A and one Grade B reflux oesophagitis cases developed preoperatively. Three Grade A and one Grade B reflux oesophagitis cases developed postoperatively in the LTG group.
Table 3: Pre- and post-operative reflux oesophagitis scores

Click here to view


One patient in the LPG group died from cerebral infarction. In the LTG group, two died of respiratory failure and three died of heart disease. None of the above deaths were directly related to gastric cancer. During follow-up, no tumour recurrence was found in either group. As shown in [Figure 3], the log-rank test result of the overall comparison of the survival curves of the two groups was P = 0.08. No significant difference in survival was noted between the two groups.
Figure 3: Comparison of the propensity score-matched LPG and LTG groups in terms of overall survival rate. There was no significant difference in overall survival between the two groups (P = 0.08), as determined using the log-rank test. LPG: Laparoscopic proximal gastrectomy, LTG: Laparoscopic total gastrectomy

Click here to view



  Discussion Top


The incidence of proximal gastric cancer has increased significantly worldwide in the past 20 years.[23],[24] The choice and safety of excision methods for upper gastric carcinoma have become hot topics in research. TG with D2 lymphadenectomy has become the standard surgical procedure for patients with advanced proximal gastric cancer. Patients with EGC usually have long post-operative survival and a low recurrence rate.[25] Therefore, this procedure is very important for EGC patients to ensure the quality of life postoperatively.[26] Multiple studies have shown that patients who undergo radical PG have a better quality of life after surgery than those who undergo TG.[27],[28],[29] The Japanese Gastric Cancer Treatment Guidelines suggest that PG should be used in patients with proximal EGC, and at least 50% of the residual stomach should be retained.[7] Usually, 12 cm or more along the lesser curvature of the residual stomach and 25 cm or more along the greater curvature of the residual stomach from the pyloric ring are preserved.

With the development of laparoscopic instruments and technologies, the application of laparoscopy in proximal gastric cancer is likely to represent one of the key directions in the future. The application of PG to proximal EGC has been limited due to the following four main concerns: oncologic safety, nutrition benefits, gastro-oesophageal reflux and anastomotic stenosis. The results showed no significant differences in operation time, bleeding volume, first anal exhaust time or post-operative hospital stay between the two groups. Although LPG with PJIDTR requires three anastomoses and the procedures seem to be more complicated, no significant difference in anastomotic complications was noted between the two surgical methods (6% vs. 4%) [Table 2]. Stricture of the residual gastrojejunal anastomosis after LPG with DTR will allow the flow of food without passing through the residual stomach. Ahn et al.[30] performed a routine gastric emptying scan 3 months after the operation. The relative ratio of food flow from the stomach to the small intestine after DTR was 3:2. Yamashita et al.[31] evaluated the actual food flow 1 year after DTR by digestive tract radiography for the first time, and food directly entered the small intestine without passing through the residual stomach in 17.5% of the patients. Presumably, there are several reasons why food does not pass through the residual stomach. First, the retained residual stomach volume is too small, resulting in the residual stomach pressure being greater than that of the jejunal route. Second, the direction and size of the residual gastrojejunal anastomosis lead to easier food flow into the jejunum. Third, gastrojejunal anastomotic stenosis prevents food from entering the residual stomach. No relevant anastomotic stenosis was found in our study given the large side-to-side anastomosis and the presence of greater than half of the gastric remnant.

When greater than half of the stomach can be preserved, PG is chosen because the nutritional status after PG has been shown to be better than after TG in many studies.[8],[9],[10] According to PGSAS, PG was superior to TG in weight loss, dietary supplementation, diarrhoea and dumping syndrome.[32] The reason is that the presence of gastric remnant reduces the incidence of gastric anaemia due to Vitamin B12 and iron absorption disorders. The presence of the pylorus reduces the incidence of bile reflux and dumping syndrome. As this study shows [Table 2], the nutrition indices at 1 year after surgery in the LPG group were significantly better than those in the LTG group (P < 0.05). LPG was superior to LTG in controlling skeletal muscle loss, maintaining stable body weight, reducing anaemia and improving quality of life.

In this study, we analysed the surgical outcomes of LPG with PJIDTR in 50 patients with proximal EGC. To our knowledge, this is the first report to describe the application of LPG with PJIDTR for proximal EGC, which shows good post-operative effects, especially for the reduction of reflux symptoms. Only one patient had Grade II reflux symptoms in the LPG group. This good result reflects the fact that PJIDTR in LPG is associated with fewer reflux symptoms than LPG based on other reconstruction methods. Several previous studies have applied direct oesophagogastric anastomosis as the reconstruction method, probably because it is simple and requires only one anastomosis. Many antireflux procedures are used to prevent reflux oesophagitis, such as gastric tube formation, fundoplication, oesophagopexy with crural repair and pyloroplasty. However, all these methods involved oesophagogastrostomy, and the results were disappointing because the rate of reflux oesophoagitis remained high.[33],[34],[35] A good alternative to oesophagogastrostomy reconstruction after PG is PJIDTR, which is a very effective antireflux reconstruction. At our institution, LPG with PJIDTR has also been performed since February 2010 and has shown a low rate of early post-operative complications, especially antireflux effects and nutritional recovery.

We found that the oncological safety of LPG with PJIDTR was satisfactory, and no tumour recurrence was observed. It should be noted that most of the five LTG patients who died were elderly individuals with underlying cardiopulmonary disease. No significant difference in the survival rate was noted between the two groups. The results are consistent with relevant studies.[3],[11] A systematic meta-analysis compared TG and PG and concluded that TG and PG had similar overall survival outcomes for proximal gastric cancer.[3]

Limitations

This retrospective cohort study had the following three limitations. First, retrospective studies have a lower level of evidence than prospective studies. Second, we did not assess the quality of life of the patients because this information was not completely captured using a validated questionnaire. Third, the sample size of this study can be further expanded. However, to our knowledge, this is the first retrospective study of LPG with PJIDTR. These encouraging data led us to plan a Phase III multicentre prospective randomised clinical trial of LPG with PJIDTR.


  Conclusions Top


Overall, this study showed that in proximal EGC, LPG with PJIDTR was better than LTG with Roux-en-Y reconstruction in terms of nutrition outcomes. This finding suggests that LPG with PJIDTR may be a suitable surgical option for proximal EGC.

Financial support and sponsorship

This work was supported by the 'Four Batches' Science and Technology to revitalise medical innovation projects (no. 2020XM48).

Conflicts of interest

There are no conflicts of interest.



 
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Ahn SH, Lee JH, Park DJ, Kim HH. Comparative study of clinical outcomes between laparoscopy-assisted proximal gastrectomy (LAPG) and laparoscopy-assisted total gastrectomy (LATG) for proximal gastric cancer. Gastric Cancer 2013;16:282-9.  Back to cited text no. 34
    
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Ronellenfitsch U, Najmeh S, Andalib A, Perera RM, Rousseau MC, Mulder DS, et al. Functional outcomes and quality of life after proximal gastrectomy with esophagogastrostomy using a narrow gastric conduit. Ann Surg Oncol 2015;22:772-9.  Back to cited text no. 35
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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2004 Journal of Minimal Access Surgery
Published by Wolters Kluwer - Medknow
Online since 15th August '04