Reducing anastomotic complications with endoscopy in laparoscopic total gastrectomy

Abstract

BACKGROUND

Early postoperative anastomosis-related complications are frequently associated with technical defects during the anastomotic procedure. Few studies focused on intraoperative anastomotic complications in esophagojejunostomy with circular stapler.

AIM

To explore whether endoscopic examination could reduce the occurrence of early postoperative anastomotic complications.

METHODS

Clinical data from 160 patients with gastric cancer who underwent laparoscopic total gastrectomy with esophagojejunostomy using a circular stapler at Nanchong Central Hospital from January 2020 to December 2023 were retrospectively analyzed. Based on whether intraoperative endoscopic examination (IEE) was performed, patients were divided into the IEE group and the non-IEE (NIEE) group.

RESULTS

All patients successfully underwent laparoscopic total gastrectomy with esophagojejunostomy using a circular stapler. In the IEE group, 7 (8.8%) patients were found to have anastomotic defects: 3 (3.8%) air leaks, 2 (2.5%) bleeding, 1 (1.3%) stricture and 1 (1.3%) full-thickness tearing. Three patients with anastomotic discontinuities were subsequently treated with additional suturing. One anastomotic bleeding was managed with laparoscopic suturing, and another was treated with endoscopic clips. One patient had anastomotic stricture, which was corrected intraoperatively. One patient experienced full-thickness tearing caused by the circular stapler, necessitating a redo anastomosis. These anastomotic defects were repaired intraoperatively, and no postoperative anastomotic complications occurred. 6 (7.5%) patients with postoperative anastomotic complications were observed in the NIEE group. The NIEE group had a significantly higher incidence of postoperative anastomosis-related complications compared to the IEE group (7.5% vs 0%; P = 0.029).

CONCLUSION

Routine IEE significantly reduces early anastomotic complications by enabling immediate detection and repair of technical defects in esophagojejunostomy with circular stapler.

Key Words: Gastric cancer; Laparoscopic total gastrectomy; Esophagojejunostomy; Anastomosis-related complications; Endoscopy

Core Tip: This study demonstrates that routine intraoperative endoscopic examination (IEE) during circular stapler esophagojejunostomy significantly reduces early anastomotic complications by enabling immediate detection and repair of technical defects such as leaks, bleeding, strictures, and full-thickness tears. In a retrospective analysis of 160 patients undergoing laparoscopic total gastrectomy, the IEE group had no postoperative anastomotic complications compared to 7.5% in the non-IEE group, despite a modest increase in operative time. These findings support the integration of IEE as a standard practice to enhance surgical safety and outcomes in gastric cancer surgery.

INTRODUCTION

The safety and efficacy of laparoscopic radical gastrectomy for early and advanced gastric cancer, particularly distal gastric cancer, have been well established[1-4]. In recent years, with an increase in cases of upper gastric cancer and esophagogastric junction cancer, the number of patients undergoing laparoscopic total gastrectomy (LTG) has risen significantly[5]. Roux-en-Y reconstruction remains the most commonly employed technique following LTG. Esophagojejunostomy, a key component of this procedure, can be performed using various methods, including circular stapler anastomosis, linear stapler anastomosis, and suture anastomosis[6].

Intraoperative anastomosis-associated complications, including bleeding, discontinuities, strictures, and full-thickness tears, present substantial risks. If not addressed in a timely manner, these complications can lead to severe postoperative outcomes, including life-threatening conditions[7]. Intraoperative endoscopic examination (IEE) has become a valuable means for the real-time evaluation of anastomotic integrity[8]. Techniques such as the methylene blue test, air insufflation test, and the combined gastroscopic-assisted monitoring (GAM) procedure facilitate the immediate detection of defects, enabling prompt repair and potentially reducing the risk of severe postoperative complications[9,10]. However, the effectiveness of routine IEE in preventing anastomotic complications after LTG remains a subject of controversy, as different studies have reported varying outcomes[11]. Recent progress in endoscopic imaging, such as high-definition white light endoscopy, narrow-band imaging, and blue laser imaging, has further improved the detection sensitivity of mucosal abnormalities and microvascular irregularities[12]. Additionally, the incorporation of indocyanine green fluorescence angiography in some centers offers supplementary intraoperative assessment of tissue perfusion, a crucial factor in anastomotic healing[13].

This study highlights the integration of IEE with the management of complications associated with circular stapler based esophagojejunostomy. Special emphasis is placed on the real-time identification, prevention, and treatment of such complications during LTG. The objective is to explore effective strategies for reducing esophagojejunal anastomosis-related complications and to provide a practical reference for clinical practice.

MATERIALS AND METHODS

Participants

The clinical data of 160 patients with gastric cancer who underwent LTG with esophagojejunostomy using circular stapler reconstruction at Nanchong Central Hospital from January 2020 to December 2023 were retrospectively analyzed. Based on whether IEE was performed, patients were divided into IEE group and non-IEE (NIEE) group. The study was approved by the Ethics Committee of Nanchong Central Hospital and conducted in accordance with the Declaration of Helsinki.

The inclusion criteria were: (1) Preoperative diagnosis of gastric cancer confirmed by gastroscopy and pathological examination; (2) LTG was performed; and (3) Reconstruction of esophagojejunal anastomosis using a circular stapler. The exclusion criteria were: (1) Prior systemic radiotherapy for gastric cancer; (2) Peritoneal metastasis confirmed by intraoperative exploration; (3) T4b tumors (invasion into adjacent organs such as pancreas, colon, or spleen) requiring combined organ resection; (4) Previous major upper abdominal surgery (e.g., gastrectomy, pancreaticoduodenectomy); and (5) Conversion to open surgery.

Surgical procedure

LTG was performed using five trocars. Lymph node dissection was conducted following the Japanese Gastric Cancer Treatment Guidelines (5^th edition)[14]. The duodenum was transected using a linear stapler (Echelon 60, Ethicon Endo-Surgery), and the duodenal stump was subsequently reinforced with a purse-string suture. Roux-en-Y reconstruction was employed for esophagojejunostomy. Esophagojejunostomy was performed using the hemidouble stapling technique with circular stapler (ECS 25, Ethicon Endo-Surgery)[15] (Figure 1A-F).

Figure 1 Esophagojejunostomy with a circular stapler and leak test using the gastroscopic-assisted monitoring procedure. A: Under the guidance of a nasogastric tube, the right esophageal wall was opened using an ultrasonic scalpel; B: The anvil head was inserted; C: The esophagus was transected at the predetermined site using a linear stapler; D: The anvil head was extracted; E: Esophagojejunostomy was completed by connecting the anvil head to the anvil rod; F: The distal jejunum stump was closed with a linear stapler; G: Intraoperative endoscopic examination were performed to assess anastomotic integrity.

IEE technique

After completion of the anastomosis, the GAM procedure was utilized[16]. An Olympus 170 gastroscope (Olympus, Japan) was used to perform anastomotic testing. The endoscopic examination procedure was conducted as follows: (1) Anastomotic integrity was directly observed under gastroscopy; (2) The anastomosis was immersed in 500-1000 mL of warm saline solution; the distal bowel was temporarily clamped, and the jejunum was inflated with air; and (3) Gas was aspirated from the anastomosis, followed by injection of 60 mL of 1% methylene blue through the gastroscope (Figure 1G). If bubble formation or methylene blue leakage was observed at the anastomotic site, intraoperative anastomotic leakage was diagnosed and repaired by suturing.

Postoperative outcomes

Anastomotic leakage was defined as the leakage of contents from the lumen of the digestive tract into the extra-luminal space due to a defect in the tissue wall at the anastomotic site. The diagnosis is confirmed if blue fluid is drained after oral administration of methylene blue, or if extravasation of contrast medium is observed on upper gastrointestinal contrast radiography using diatrizoate meglumine or lipiodol. Anastomotic bleeding was defined as the presence of bloody drainage through the nasogastric tube, hematemesis, or hematochezia, which may be accompanied by alterations in vital signs (such as changes in heart rate and blood pressure) and a decrease in hemoglobin concentration. Emergency endoscopy was performed when necessary to confirm the diagnosis and treatment. Anastomotic stenosis is characterized by a narrowing of the lumen due to excessive scar tissue hyperplasia, fibrosis, or other causes, leading to obstructive symptoms. Patients often present with postoperative dysphagia. The condition was diagnosed and evaluated regarding the location and severity of the stenosis through imaging studies such as contrast radiography or gastroscopy[17]. These postoperative complications were classified according to the Clavien-Dindo classification[18]. All patients underwent a minimum postoperative follow-up of 6 months to monitor clinical outcomes.

Statistical analysis

All statistical analyses were conducted using SPSS software (version 25.0; IBM Corp., Armonk, NY, United States). Continuous variables conforming to a normal distribution were presented as the mean ± SD and compared via the independent samples t-test. Continuous variables with non-normal distribution were presented as the median (interquartile range) and analyzed using the Mann-Whitney U test. Categorical variables were summarized as frequencies (percentages) and evaluated by the χ² test or Fisher’s exact test. Multivariate logistic regression analysis was utilized to identify independent risk factors associated with postoperative anastomotic complications. Variables incorporated into the model were selected based on their clinical relevance or a univariate association with a P value < 0.1. The goodness-of-fit of the logistic regression model was evaluated using the Hosmer-Lemeshow goodness-of-fit test, which demonstrated a satisfactory fit (P > 0.05). The results were presented as adjusted odds ratios along with their corresponding 95% confidence intervals. Statistical significance was defined as a two-tailed P value < 0.05.

RESULTS

Patient clinical characteristics

From January 2020 to December 2023, a total of 160 patients who underwent laparoscopic radical total gastrectomy with esophagojejunostomy using circular stapler reconstruction were retrospectively analyzed. The clinical characteristics of patients in the IEE and NIEE groups were summarized in Table 1.

Table 1 Patient clinicopathological characteristics.

Variables	IEE (n = 77)	NIEE (n = 83)	P value
Demographics
Sex (male/female)	56/21	66/17	0.278
Age (years)	61.3 ± 9.21	63.2 ± 8.85	0.463
BMI (kg/m2)	22.75 ± 3.01	23.35 ± 2.78	0.478
Comorbidities
COPD (yes/no)	11/66	17/66	0.691
Hypertension (yes/no)	15/62	14/69	0.821
Diabetes (yes/no)	9/68	13/70	0.530
Degree of tumor differentiation			0.356
High	17	14
Medium	29	33
Low	31	36
Pathological stage			0.782
IA/IB	11	9
II	25	29
IIIA/IIIB	41	45

IEE: Intraoperative endoscopic examination; NIEE: Non-intraoperative endoscopic examination; BMI: Body mass index; COPD: Chronic obstructive pulmonary disease.

Intraoperative characteristics

In the IEE group, 7 (8.8%) patients were found to have anastomotic defects: 3 (3.8%) air leaks, 2 (2.5%) bleeding, 1 (1.3%) stricture, and 1 (1.3%) full-thickness tearing. Table 2 details the surgical characteristics of patients with positive IEE. Three patients with anastomotic discontinuities were subsequently treated with additional suturing. One anastomotic bleeding was managed with laparoscopic suturing, and another was treated with endoscopic clips due to intrathoracic anastomosis. One patient had anastomotic stricture, which was corrected intraoperatively by Esophagus-Sparing Anastomotic Narrowing Revision procedure[12]. Briefly: (1) Making a 2-cm incision along the jejunal anterior wall at the anastomotic line; (2) Excising contralateral mucosa entrapped within the anastomosis; (3) Inserting a gastric tube distal to the anastomosis; and (4) The anterior wall was then closed with interrupted sutures (Figure 2). One patient experienced full-thickness tearing caused by the circular stapler, necessitating redo anastomosis via: (1) Laparoscopic removal of the original anastomosis; (2) Anvil head insertion into the esophageal stump secured with a purse-string suture; and (3) Jejunal pouch creation to enlarge the lumen (Figure 3). The mean operative time was 27 minutes longer in the IEE group than in the NIEE group (P = 0.032) (Table 3).

Figure 2 Management of esophagojejunal anastomotic stricture. A: An incision was made along the jejunal anterior wall of the anastomosis; B: The stapled contralateral mucosa was completely incised; C: A gastric tube was placed passing through the distal of the anastomosis; D: Suturing was performed with the guidance of gastric tube as a stent; E: The gastroscope successfully passed through the anastomosis.

Figure 3 Management of esophagojejunal anastomotic full-thickness tearing. A: Side-to-side small intestinal anastomosis for jejunal pouch creation was performed extracorporeally; B: The circular stapler’s center rod emerged from the pouch apex extracorporeally; C: Esophagojejunostomy was completed laparoscopically; D: The common entry hole was closed with continuous sutures; E: Laparoscopic reinforcement of the suture line was performed with a continuous seromuscular suture.

Table 2 Intraoperative management of positive leak tests in esophagojejunal anastomosis.

Patient No.	Defect type	Management	Postoperative anastomotic complications	Postoperative hospital stay (days)
1	Anastomotic discontinuity	Suturing	No	10
2	Anastomotic discontinuity	Suturing	No	11
3	Anastomotic discontinuity	Suturing	No	10
4	Anastomotic bleeding	Endoscopic clamping	No	9
5	Anastomotic bleeding	Suturing	No	12
6	Anastomotic stricture	ESANR[16]	No	11
7	Full-thickness tearing	Redo anastomosis	No	13

ESANR: Esophagus-Sparing Anastomotic Narrowing Revision.

Table 3 Patient Intraoperative and postoperative characteristics, mean ± SD.

Variables	IEE (n = 77)	NIEE (n = 83)	P value
Mean operation time (minutes)	308.5 ± 81.3	281 ± 75.6	0.037
Mean blood loss (mL)	105.7 ± 52.8	110.4 ± 65.2	0.745
Number of retrieved lymph nodes	28.5 ± 12.2	32.7 ± 10.8	0.178
Maximum tumor diameter (cm)	4.35 ± 2.16	4.05 ± 2.56	0.563
Proximal margin length (cm)	3.15 ± 2.05	3.26 ± 2.28	0.925
Distal margin length (cm)	7.38 ± 3.78	7.53 ± 3.21	0.672
Length of hospital stay (days)	12.94 ± 2.12	11.73 ± 1.78	0.452
Anastomosis-related complications			0.029
Anastomotic leakage	0	5
Anastomotic bleeding	0	0
Anastomotic stricture	0	1

IEE: Intraoperative endoscopic examination; NIEE: Non-intraoperative endoscopic examination.

Postoperative clinical characteristics

In the NIEE group, 6 cases (7.5%) of postoperative anastomotic complications were observed (Table 3). The incidence of postoperative anastomosis-related complications in the NIEE group was significantly higher than that in the IEE group (7.5% vs 0%; P = 0.029). Nevertheless, there was no significant inter-group difference in the length of hospital stay (P > 0.05). Postoperatively, anastomotic leakage occurred in 5 patients. According to the Clavien-Dindo classification, 3 patients were classified as grade I, and 2 as grade II; all cases were resolved through conservative management. One patient developed anastomotic stricture one month after the operation, and complete resolution was achieved after endoscopic dilation therapy.

Multivariate logistic regression analysis of risk factors for anastomotic complications

Multivariate logistic regression analysis was conducted to determine the independent risk factors for postoperative anastomotic complications (Table 4). The utilization of IEE was recognized as a significant protective factor (odds ratio = 0.12, 95% confidence interval: 0.04-0.41, P = 0.001). Other factors, such as tumor stage, chronic obstructive pulmonary disease, hypertension, diabetes, and operative duration, were not significantly correlated with anastomotic complications in the multivariate model.

Table 4 Multivariate logistic regression analysis of risk factors for anastomotic complications after laparoscopic total gastrectomy (n = 160).

Variable	β	SE	OR (95%CI)	P value
IEE (yes vs no)	-2.12	0.62	0.12 (0.04-0.41)	0.001
Tumor stage (III vs I/II)	0.61	0.32	1.84 (0.98-3.45)	0.058
COPD (yes vs no)	0.49	0.41	1.63 (0.73-3.64)	0.233
Hypertension (yes vs no)	0.25	0.38	1.28 (0.61-2.71)	0.512
Diabetes (yes vs no)	0.37	0.39	1.45 (0.68-3.10)	0.341
Operative time (extend per 30 minutes)	0.18	0.10	1.20 (0.98-1.46)	0.072

IEE: Intraoperative endoscopic examination; COPD: Chronic obstructive pulmonary disease; β: Regression coefficient; SE: Standard error; OR: Odds ratio; CI: Confidence interval.

DISCUSSION

In 2009, Omori et al[15] first introduced the hemidouble stapling technique, which addressed the issue of anvil placement and significantly expanded the use of circular staplers in esophagojejunostomy reconstruction. This anastomotic approach offers several advantages, including achieving a higher esophageal resection margin and eliminating the need for manual closure of a common entry hole. Low-quality anastomosis in esophagojejunostomy can lead to severe postoperative complications, including anastomotic bleeding, leakage, and stricture. These complications may result in prolonged hospital stays, increased medical costs, and even mortality[19,20]. Previous literature has reported various intraoperative methods for preventing esophagojejunostomy leakage, such as the methylene blue test or a comprehensive leak detection approach combining gastroscopy, air insufflation, and methylene blue (GAM)[16]. At our institution, some researchers advocated the use of intraoperative gastroscopic leak detection, which has been shown to effectively prevent anastomotic complications in esophagojejunostomy for gastric cancer surgery[9,10]. However, there is controversy over whether IEE can effectively prevent anastomotic leakage after total gastrectomy[21-24]. Our study revealed a significantly lower incidence of postoperative anastomotic complications in the IEE group vs the NIEE group, although the mean operative time was prolonged by 28 minutes in the IEE group.

In the IEE group, 7 (8.8%) patients were found to have anastomotic defects: 3 (3.8%) air leaks, 2 (2.5%) bleeding, 1 (1.3%) stricture and 1 (1.3%) full-thickness tearing. Kanaji et al[22] reported a 3.2% intraoperative leakage rate in patients undergoing open total gastrectomy. In comparison, Park et al[24] utilized intraoperative endoscopy for anastomotic evaluation, revealing a 9.71% positive rate in the leak detection group among gastric cancer patients. In this study, 3 patients (3.8%) were identified with anastomotic discontinuity in the IEE group. After reinforced suturing was performed intraoperatively, no anastomotic leakage occurred postoperatively.

Anastomotic bleeding is an early complication after esophagojejunostomy, with an incidence of approximately 2%[25]. The causes of postoperative anastomotic bleeding were as follows: (1) Improper selection of staple height resulted in poor staple formation and inadequate compressive hemostasis; (2) The stapler was not fully fired in one attempt, leading to incomplete anastomosis and poor vascular closure; (3) Surrounding tissues were embedded in the anastomosis, resulting in insufficient closure of small vessels; (4) The tube stapler was either too loosely or too tightly rotated, causing incomplete vascular clamping or tissue cutting, respectively; and (5) The staples were precisely placed on the surrounding vessels, causing vascular damage. In this study, the intraoperative anastomotic bleeding rate was 2.5%. After intraoperative intervention, no anastomotic bleeding was observed postoperatively.

Although early stricture of the esophagojejunal anastomosis is a concern for surgeons, it has rarely been reported in the literature. Lee[26] described a case in which a pseudolumen was created during linear stapler anastomosis, resulting in early anastomotic stricture. This was successfully managed with endoscopic release of the covering mucosa postoperatively[21]. Nishikawa et al[27] reported two cases of jejunal obstructions that occurred because of a full-thickness jejunal trap in the jejunal limb caused by the circular stapler during the anastomosis. For the two cases, re-anastomosis was performed[22]. In this study, the IEE group reported one case of intraoperative anastomotic stricture, which occurred because the jejunal mucosa on the mesenteric side of the efferent limb was inadvertently incorporated into staple line. Detaching the jejunal mucosa which stapled in the anastomosis prevented re-anastomosis. After successful intraoperative correction, no postoperative stricture or anastomotic leakage occurred.

Full-thickness tearing at the esophagojejunal anastomosis is a severe intraoperative complication during circular stapler esophagojejunostomy. In cases of complete anastomotic tear, surgical takedown and re-anastomosis should be considered. However, limited guidance exists in the literature for managing such scenarios clinically. Understanding the etiology of anastomotic tears is crucial for prevention. Contributing factors include: (1) Using an oversized circular stapler in a narrow jejunal lumen can cause damage; and (2) Excessive force during insertion may injure the tissue. Re-anastomosis poses technical challenges, particularly for supra-diaphragmatic anastomoses. In IEE group, one case of full-thickness anastomotic mucosal tear was identified. Postoperative leakage or obstruction was absent following re-anastomosis.

Multivariate logistic regression analysis further verified that IEE served as an independent protective factor against anastomotic complications (odds ratio = 0.12, P = 0.001), highlighting its crucial role in alleviating technical deficiencies during esophagojejunostomy. Although tumor stage, comorbidities, and operative duration have been previously associated with anastomotic outcomes, our analysis did not identify them as significant predictors within this cohort. This implies that the immediate intraoperative detection and rectification of defects, facilitated by endoscopy, may supersede other patient - or surgery - related factors in preventing early anastomotic complications. These findings strengthen the recommendation for the routine incorporation of IEE in LTG to improve surgical safety and outcomes.

This research exhibits several limitations. Firstly, its retrospective design might give rise to selection bias, despite our efforts to alleviate this issue via time-based allocation. Secondly, the single-center characteristic of the study could restrict the generalizability of the research findings. Thirdly, although IEE notably diminished early complications, its influence on long-term outcomes, including anastomotic stricture or quality of life, remains ambiguous and necessitates further exploration. Future prospective, multi-center studies are required to validate the findings of this research.

CONCLUSION

IEE is a promising method for effectively identifying anastomotic bleeding, discontinuities, strictures, and full-thickness tears. This approach allows for immediate, individualized interventions to be performed intraoperatively, thereby preventing severe postoperative anastomotic complications.