Long-term efficacy and safety of piggyback jejunal interposition reconstruction single-tract reconstruction after proximal gastrectomy for Siewert II/III adenocarcinoma of the esophagogastric junction: A retrospective case series study

DOI: https://doi.org/10.21203/rs.3.rs-2458202/v1

Abstract

Introduction

The aim of this study is to introduce the protocol of piggyback jejunal interposition reconstruction single-tract reconstruction (PJIRSTR) for Siewert II/III adenocarcinoma of the esophagogastric junction (AEG) in detail, and assess its feasibility and safety, moreover, evaluate the efficacy of preventing postoperative reflux symptoms as well as the clinical outcome of surgical treatment in long term.

Methods

Between July 2013 and October 2017, Patients with Siewert II/III AEG who underwent PJIRSTR in Shanxi Cancer Hospital were enrolled according to the inclusion and exclusion criterias. The retrospectively collected data including clinical characters, intraoperative and postoperative outcomes, and follow-up were collected. Clinical indicators were determined by the paired-samples t-test. Overall survival was analyzed by the Kaplan-Meier curve.

Results

A total of 33 patients with SiewertII/III AEG were enrolled according to inclusion and exclusion, including 29 male and 4 female patients, with a mean age of 60.9 years. 23 patients were Siewert II AEG and 10 were Siewert III. All of 33 patients underwent open surgery via the abdominal approach and no intraoperative death. The mean operation and reconstruction times were 136.7 and 46.9 min, respectively. The mean estimated blood loss was 87.6 mL; the mean number of dissected lymph nodes was 14.7, and the mean duration of postoperative hospitalization was 13.9 days. The early complication rate was 9.1% (n = 3), including one case each of anastomotic bleeding, incision infection, and ileus. The late complication rate also was 9.1% (n = 3): 1 patient had gastrojejunal anastomosis stenosis, which was successfully treated under the fluoroscopic balloon dilatations. 2 had Visick grade II reflux symptoms, no manifestations of reflux esophagitis was found in all patients by postoperative gastroscopy. The mean follow-up time was 73 months, with the median follow-up of 82 months. The 3- and 5-year cumulative overall survival rates were 90.9% and 78.8%, respectively.

Conclusion

PJIRSTR is a safe and feasible, and innovative reconstruction method after proximal gastrectomy (PG) for patients with Siewert II/III AEG. Furthermore, it has excellent efficiency in terms of preventing postoperative reflux symptoms.

Introduction

In the past few decades, the incidence of proximal gastric cancer has significantly increased worldwide[13]; accordingly, extensive research on adenocarcinoma of the esophagogastric junction (AEG) is also being carried out. For AEG treatment, total gastrectomy (TG) is usually preferred considering the oncological safety and the high incidence of complications such as reflux esophagitis and anastomotic strictures after proximal gastrectomy (PG). However, some studies have shown that PG and TG have similar 3-year survival rates in early AEG[46], and PG has been reported to be oncologically safe for patients with T2/T3 proximal gastric cancer[7]. In addition, PG has significant advantages over TG concerning postoperative nutritional status [56]. However, postoperative reflux after PG has plagued surgeons for many years. Although there are various reconstruction methods after PG to solve this problem, no ideal method has found wide application so far owing to the inefficient reflux prevention or the technique not gaining adequate popularity for varied reasons.

A novel method, PJIRSTR was proposed firstly by our group in 2016 and has been showed that PJIRSTR can prevent postoperative reflux effectively. In this study, we will introduce the protocol of PJIRSTR in detail, and analyze the clinical relevance of the pathological data, espacially evaluate the status of gastroesophageal reflux as well as the clinical outcome of surgical treatment in long term.

Methods

Patients

From July 2013 to October 2017, 33 patients with Siewert II/III AEG who underwent PJIRSTR at Shanxi Cancer Hospital were selected. The inclusion criteria were defined as follows: (1) age range between 45 and 75 years; (2) Siewert II/III AEG confirmed by postoperative pathological findings; (3) tumor diameter ≤ 4 cm without distant metastasis, and invasion of the lower esophagus < 1 cm; (4) no vital organ dysfunction and no surgical contraindications, and (5) The patients had complete follow-up records, including postoperative gastroscopy, nutritional index results, and postoperative reflux symptoms. Results of postoperative endoscopic reflux esophagitis were classified by means of the Los Angeles classification. Furthermore, the Visick score was applied for for all patients to evaluate gastroesophageal reflux symptoms. Patients with incomplete follow-up records were excluded. The last follow-up period was November, 2022.This study was approved by the ethics committee of Shanxi Cancer Hospital.

Operative Procedures

PG + esophagojejunal Roux-en-Y anastomosis

For PJIRSTR, the esophagojejunal Roux-en-Y anastomosis was firstly performed, and the jejunal loop was about 30 cm. On this basis, an anastomosis of the remnant stomach and jejunum was performed at a suitable position of the jejunal loop, which resembled the jejunum carrying the remnant stomach on its back.

After induction of general anesthesia, the patients were placed in the supine position. The entire procedure was carried out via a transabdominal approach, with a midline incision made to the upper abdomen. According to the Third and Fourth edition Japanese gastric cancer treatment guidelines, D1 + or D2 lymph node dissection was performed based on the size, location, and degree of esophageal invasion of the tumor. The digestive tract was reconstructed after PG, and at least half of the stomach was preserved. The jejunum and its mesangial blood vessels were cut at about 20–25 cm from the Treitz ligament, and the distal jejunum was raised to the end of the esophagus in front or behind the colon. The circular stapler was used to perform an end-to-side anastomosis between the esophagus and distal jejunum. The stump of the jejunum was closed with a linear closure device and the length of the blind end < 3 cm. Lateral anastomosis between the proximal and distal jejunum was performed about 30 cm away from the distal end of the esophageal jejunum anastomosis. The residual end was closed with a linear cutting closure device, and the length of the blind end was ≤ 3 cm.

Pjirstr Was Performed After Pg

The key of PJIRSTR: (i) The side-to-side anastomosis was performed between the anterior wall of the remnant stomach and the jejunum while keeping the anastomosis 3–5 cm away from the stump of the remnant stomach, which formed a structure of "artificial gastric fundus" and anastomosis size was about 4-5cm. (ii) After anastomosis was completed, the angle formed by the remnant stomach and the jejunum should be < 75°. (iii) The length of the interposition jejunum remains 12–15 cm. (iv) The jejunum was closed with a linear closure device at < 3 cm below the anastomosis of the residual stomach jejunum to completely block the jejunum content channel and complete the PJIRSTR (Fig. 1).

Collection of the required clinical indicators

The data in this study were collected from patients' medical history and the follow-up records of researchers and follow-up room. Surgical outcomes, postoperative complications, and patients' surgical parameters were collected. Early complications (< 30 days) including anastomotic bleeding, anastomosis leakage, incision infection, ileus, and organ dysfunction and late complications (> 30days), containing reflux esophagitis, reflux symptoms, recannulation of intestinal tract, and anastomotic stenosis also were recorded. In addition, changes in nutritional indicators were also collected. The presence and severity of postoperative reflux esophagitis were assessed by gastroscopic report. The presence or absence of postoperative reflux symptoms was known by follow-up records.

Statistical Methods

Statistical analyses were performed using SPSS software (IBM SPSS 26.0 (IBM Corp. New York, USA)). The quantitative data with normal distribution were expressed as mean ± SD, and the quantitative data with non-normal distribution were expressed as median. Nutritional indicators were analyzed by the paired-samples t-test. The survival rate was analyzed by Kaplan-Meier curve.

Result

Patient characteristics

The baseline characteristics of patients are summarized in Table 1. The study population comprised 29 (87.9%) male and 4 (12.1%) female patients (mean age: 60.9 [range, 46–71] years and mean BMI: 24.1 ± 2.6 [range, 18.3–28.3] kg/m2). A total of 33 patients had no severe comorbidities. No patients had reflux esophagitis in accordance with preoperative endoscopic reports.

Table 1

Patient demographics

     

PJIRSTR (n = 33)

Range

 

Age (years, mean ± SD)

60.9 (± 6.8)

46–71

 

< 60

12(36.3%)

   

≥60

21(63.6%)

   

Gender (male : female)

29:4

     

Smoking

   

11(33.3%)

     

Drinking

   

4(12.1%)

     

Body mass index (BMI, kg/m2)

24.1(± 2.6)

18.3–28.3

 

Previous abdominal surgery

0(0%)

   

Comorbidity

           

1.High blood pressure

5(15.2%)

   

2.Diabetes mellitus

3(9.1%)

   

3.Cardiovascular disease

1(3%)

   

ASA score

           

I

   

5(15.2%)

   

II

   

27(81.8%)

   

III

   

1(3%)

   

Siewert type

           

II

   

23(69.7%)

   

III

   

10(30.3%)

   

reflux esophagitis (based on thepreoperative evaluation of

endoscopy)

0(0%)

Surgical Outcomes And Pathological Findings

All surgeries were open surgery via the abdominal transhiatal (TH) approach. Four patients underwent D1 + lymphadenectomy, and all others underwent D2 lymphadenectomy. The surgical outcomes of 33 patients are presented in Table 2. The mean operative time was 136.7 (range: 110–180) min. The mean blood loss was 87.6 (range: 60–120) mL. The mean tumor size was 3.1 (range: 1–4) cm, and R0 resection was performed in all patients. There were no deaths or serious complications during the operation. The mean and median duration of postoperative hospitalization were 13.9 and 14 days.

Table 2

Surgical outcomes and complications

         

Values

 

Range

Operative time (minutes)

 

136.7 ± 22.7

110–180

Digestive tract reconstruction time (min)

46.9 ± 5.5

40–57

Lymph node dissection(n,%)

     

D1+

 

4 (12.1%)

 

D2

 

29 (87.9%)

 

R0 resection (n, %)

 

33 (100%)

 

Intraoperative blood loss (ml)

87.6 ± 18.4

50–120

Combined resection (n)

   

Gall bladder

3

 

Spleen

1

 

First anal exhaust time (days)

2.7 ± 1.2

2–5

Postoperative hospital stays (days)

13.9 ± 1.9

12–21

Median follow-up time (months)

82

24–111

Early complications (n)

   

Anastomotic bleeding

1 (3.0%)

 

Incision infection

1 (3.0%)

 

Ileus

1 (3.0%)

 

Leakage of anastomosis

0 (0%)

 

Late complications

   

Reflux esophagitis(n, %)

0 (0%)

 

Anastomotic stenosis

1 (3.0%)

 

Reflux symptom(n, %)

2 (6.1%)

 

Recannulation of intestinal tract

0 (0%)

 

Pathological findings are shown in Table 3. According to the TNM staging (8th edition AJCC), three, three, five, two, one, eight, and 12 cases were staged IA, IB, IC, IIB, IIIA, IIIB, and IVA, respectively. Histologic types comprised 21 moderately well-differentiated cases and 12 poorly differentiated cases. The upper and lower resection margins of all patients were negative at postoperative pathological examination. The average number of LNs dissected was 14.7 ± 5.1 (range: 9–27) and the mean number of metastatic LNs was 2.6 ± 3.4 (range: 0–12).

Table 3

Pathologic findings

       

PJIRSTR(n = 33)

Range

Lymph nodes dissection number (n)

14.7 ± 5.1

9–27

Number of metastatic lymph nodes

2.6 ± 3.4

0–12

Tumor size (cm)

3.1 ± 0.8

1–4

Differentiation

   

High-middle

21(63.6%)

 

Low

12(36.3%)

 

T stage

   

T1a

3

 

T1b

3

 

T2

7

 

T3

4

 

T4a

16

 

N stage

   

N0

14

 

N1

6

 

N2

8

 

N3

5

 

Stage

   

IA

3

 

IB

2

 

IC

5

 

IIB

2

 

IIIA

1

 

IIIB

8

 

IVA

12

 

Adjuvant chemotherapy(n,%)

23(69.7%)

 

Early Complications And Late Complications

The overall early complication rate was 9.1% (n = 3), including one each of anastomotic bleeding (on postoperative day 1), incision infection(on postoperative day 6), and ileus(on postoperative day 9), which improved after conservative management without the need for reoperation. Among all 33 patients, no anastomotic stenosis or serious complications was discovered.

The late complication rate was 9.1% (n = 3), including one gastrojejunal anastomosis stenosis and 2 Visick grade II gastroesophageal reflux. Discharged patients are followed by telephone once a year through the hospital's follow-up room and the last follow-up time was in November 2022. Only 2 patients (6.1%) experienced symptoms of acid reflux and heartburn after surgery (Visick grade II ) according to follow-up records, which successfully treated with medication. In addition, postoperative reflux esophagitis were diagnosed by gastroscopy. With time dividing point of one year, a total of 33 patients had two or more gastroscopy reports. Furthermore, about 15 patients underwent gastroscopy every year after surgery. No evidence of reflux esophagitis was found among these reports.

The results of gastroscopy are shown in Fig. 2. Patients showed promising imaging results upon upper gastrointestinal angiography after operation with no recanalization of intestinal tract was observed during the follow-up period. Figure 3 shows the post PG upper gastrointestinal radiography findings, using PJIRSTR.

Nutritional Indices

We collected patients' nutritional indicators, including body weight, serum albumin, hemoglobin, and total serum protein (preoperative and postoperative 3, 6, and 12 months). The results of nutritional indices are shown in Fig. 4. All indicators decreased significantly 3 month after surgery compared with those before the operation (A: 95% confidence interval [CI] 1.690–3.970, p = 0.000; B: 95% CI 3.080–4.617, p = 0.000; C: 95% CI 12.575–20.819, p = 0.000; D: 95% CI 7.546–10.454, p = 0.000). However, serum albumin and total serum protein returned to preoperative ranges at postoperative 18 months (95% CI 1.170–1.685,p = 0.716 and 95% CI 0.651–2.851, p = 0.210). The average weight loss was 13.5%, 11.8%, and 10% at postoperative 3, 6, and 12 months, respectively.

Recurrence And Survival Data

The median follow-up period was 82 (range: 24–111) months. One patient with pIVA was diagnosed with gastric stump cancer at postoperative 25 months and underwent re-surgery. The patient subsequently died 16 months after the second operation. peritoneal seeding. In addition, one patient with pIIB developed liver metastases at two years after surgery. The 3- and 5-year cumulative overall survival rates were 90.9% and 78.8%, respectively. The survival curve is shown in Fig. 5.

Discussion

In this study, we analyzed the results of the surgical outcomes of 33 patients who had Siewert II/III AEG underwent PJIRSTR. The PJIRSTR technique was first proposed by our research team in 2016[8]. To our knowledge, this is the first detailed description of the PJIRSTR technique. Based on the results of our analysis, PJIRSTR effectively solves the problem of reflux after PG. It is an acceptable treatment method for the Siewert II/ III AEG.

According to the Japanese gastric cancer treatment guidelines (Fifth edition), for early AEG, if more than half of the stomach after R0 resection can be preserved, PG can be selected as the surgical method[9]. However, it is still unclear whether PG can be performed for advanced AEG. Sugoor et al.[10] reported that as long as sufficient surgical resection margins are ensured and enough remnant stomach is preserved, PG can be selected even for advanced proximal-third gastric cancer. Haruta et al.[11] believed that patients with advanced AEG whose tumor length is < 4 cm could undergo PG.

As a functional preservation surgery, PG has some irreplaceable advantages compared with TG. First, PG ensures that food stays in the residual stomach for preliminary digestion, and then further digestion through the duodenum, which is conducive to full absorption in the jejunum and the nutritional status of patients after surgery. Second, PG provides a better pathway for further endoscopic treatment such as endoscopic retrograde cholangiopancreatography (ERCP) than TG. A recently conducted multi-center, prospective study reported that in terms of long-term efficacy, the 3-year survival rates of PG and TG were similar (96% and 92%, respectively), but the incidence of reflux esophagitis was significantly higher in the TG than PG group (14.5% vs. 5.4%; P = 0.02)[12]. Thus, after ensuring oncological safety, if we improve the PG approach to reduce the incidence of postoperative complications such as reflux esophagitis and anastomotic stenosis to a level similar to or even lower than that of TG, PG has the potential to become the standard surgical method for AEG.

Yamashita[13] found that double-tract reconstruction (DTR), which allows food to pass through the residual stomach into the duodenum, can effectively maintain postoperative nutritional status. However, some studies indicated that dietary bolus after DTR cannot enter the duodenum through the residual stomach as scheduled, rather escape through the jejunum route, which ultimately results in nutritional results similar to TG with Roux-en-Y reconstruction (TGRY)[14, 15]. In addition, a retrospective study have recently demonstrated DTR and esophagogastrostomy has similar nutritional outcomes and QOL[16]. PJIRSTR completely blocked the passage of the proximal jejunum and avoided food escaping through the jejunum. Futhermore, When food passes through the duodenum, it is fully mixed with bile and pancreatic juice, and stimulates the secretion and release of hormones such as pancreatic secretin and cholecystokinin in the gastrointestinal tract, which is conducive to the digestion and absorption of food. Compared to jejunal interposition (JI), PJIRSTR, a technique similar to RY, is relatively easy to perform. In addition, when cancer of the remnant stomach is found, PJIRSTR can deal better with the remnant stomach than JI. In terms of the length of the interposed jejunum, Tokunaga suggested that it should be < 10 cm[17]. Some scholars have suggested that the ideal length is 10–15 cm[1820], otherwise, it may cause intestinal food stasis and inconvenience during postoperative endoscopy. However, according to our clinical experience, when the length of the interposed jejunum is 12–15 cm, the above problems can be solved.

In this context, we speculated that if PJIRSTR could effectively solve long-term complications of postoperative reflux and anastomotic stenosis, it may become an attractive treatment method for Siewert II/III AEG. In our study, only 2 of the 33 patients (3.1%) had Visick grade II reflux symptoms from the follow-up results. In addition, no signs of reflux esophagitis were reported by gastroscopy in all patients after surgery. The postoperative anti-reflux effect of this method is completely comparable with some anti-reflux surgery methods that have been reported so far. For example, the incidence of reflux esophagitis after side-overlap esophagogastrostomy (SOFY) was 10%. However, the procedure requires an experienced surgeon to perform it under a laparoscope[21]. The incidence of reflux esophagitis after the double-flap technique (DFT) was 0%, and the incidence of reflux symptoms was 10%[22]. This technology has a good effect in preventing reflux esophagitis, but technical difficulties and the risk of anastomotic stenosis is relatively high. Our analysis showed that PJIRSTR has better anti-reflux effect than other techniques and may be related to the following two mechanisms that have a dual anti-reflux effect. First, side-to-side anastomosis was performed between the jejunum and the anterior wall of the remnant stomach, while keeping the anastomosis 3–5 cm away from the stump of the remnant stomach. This method of anastomosis formed an “artificial stomach fundus” structure, effectively blocking the food or digestive fluid from flowing into the esophagus. Second, is the anti-reflux effect of jejunum interposition; PJIRSTR completely blocked the passage of the proximal jejunum, making alkaline reflux esophagitis almost impossible.

In this study, we performed adjuvant chemotherapy for all patients whose postoperative pathology was not staged I at that time. Therefore, 23 of 33 patients underwent chemotherapy. The 3-5-year cumulative overall survival rates were 90.9% and 78.8%, respectively, indicating that the technique was feasible in terms of oncology safety.

In our study, we performed PJIRSTR, which achieved satisfactory surgical and postoperative results. No death during operation or severe perioperative complications were recorded in any of the 33 patients. Both early postoperative complications(9.1%) and late complications(9.1%) were low compared to DTR[23]. For the postoperative nutritional status of the patients, the weight and hemoglobin of the patients did not return to the preoperative level at postoperative 18 months, which may be related to the status of advanced tumors in some patients. In our study, the average weight loss was 13.5%, 11.8%, and 10% at postoperative 3, 6, and 12 months, respectively. Difficulty maintaining weight is a typical feature after gastrectomy, which is connected with reduced stomach volume[23]. However, all the nutritional indicators have been rising after surgery.

There are several limitations to this study. First, this was a retrospective study prone to inherent bias. second, all cases had performed laparotomy, we should also apply this technique to laparoscopic or robotic surgery to evaluate its feasibility. Third, the sample size of the study is relatively small, and more multi-center, prospective clinical data support is needed to validate the findings.

In conclusion, we report here our novel reconstruction method after PG—PJIRSTR—that shows satisfactory outcomes after the operation. Most importantly, PJIRSTR effectively addressed the problems of postoperative reflux and reflux esophagitis and improved the postoperative quality of life of patients. However, multi-center and prospective randomized trials are needed to verify its clinical application value.

Declarations

Acknowledgements

None.

Authors’ contributions

All authors contributed to the study conception and design. Wanhong Zhang and Yuchao Ma have equally contributed to this work and should be considered as co-first authors.

Material preparation, data collection and analysis were performed by Baoqing Ren ,Liqiang Lei, Jianhong Dong and Linjie Li. Supervision: Wanhong Zhang. The first draft of the manuscript was written by Yuchao Ma and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Funding 

This study was not externally funded. There was no sponsor for this study.

Availability of data and materials

Data can be provided upon reasonable request from the corresponding author.

Ethics approval 

This study was approved by the ethics committee of Shanxi Tumor Hospital.

Consent for publication 

Informed written consent for publication was obtained from the individuals to publish their data (including individual details, images, videos and presentations of case reports).

Competing interests

The authors declare that they have no competing interests.

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