Keywords
Endoscopy Upper GI Tract - Endoscopic resection (ESD, EMRc, ...) - Benign strictures
- Dilation, injection, stenting
Introduction
Submucosal tumors (SMTs) of the gastrointestinal tract, including mesenchymomas, leiomyomas,
lipomas, neurogenic tumors, fibromas, and hemangiomas, have been increasingly detected
and diagnosed through endoscopic ultrasonography (EUS) [1]. The occurrence of SMTs in the upper gastrointestinal tract is predominantly observed
in the esophagus and stomach. Among these, stromal tumors and leiomyomas constitute
the most prevalent pathological types [2]. SMTs exhibit varying growth patterns depending on their location, with some tending
to protrude inward toward the lumen, whereas others may extend outward from the cavity.
Considering the potential for malignancy in SMTs, surgical resection, particularly
endoscopic resection, is viewed as a pivotal therapeutic approach.
Submucosal tunneling endoscopic resection (STER), leveraging its advantage of preserving
the integrity of the digestive tract mucosa, has emerged as a commonly employed endoscopic
technique for managing submucosal tumors (SMTs) situated in the upper digestive tract
[3]
[4]. Although STER has demonstrated its efficacy and safety as a treatment option for
SMTs of the esophagus, it is worth noting that irregular tumor shapes and those with
diameters exceeding 2.5 cm may pose a higher risk of postoperative complications,
including bleeding, esophageal fistula or hematocele, and infection [5]
[6]. Previous research has indicated that in individuals who suffer from giant esophageal
leiomyomas (with a transverse diameter ≥ 3 cm), the likelihood of developing an esophageal
fistula during the procedure of STER is 6.25% [7]. in addition, we observed that as the transverse diameter of esophageal submucosal
tumors increases, and particularly in patients who experience multiple mucosal injuries
during surgery, risk of developing postoperative esophageal fistula and infection
rises accordingly. However, esophageal fistula or infection remains the most severe
complication following STER operation for esophageal submucosal tumors, notably prolonging
the length of hospital stay. Unfortunately, at this juncture, there is a lack of a
straightforward preventive measures to address this issue.
To address the challenge of reducing esophageal fistula and infection complications
following STER procedure for removal of SMTs, we innovatively incorporated a step
positioning the drainage device prior to closing the esophageal mucosa wound with
metal clips. Interestingly, implementing this approach led to a remarkable reduction
in esophageal infection complications among patients with giant SMTs who underwent
STER surgery. This finding underscores the effectiveness and potential of our novel
technique in enhancing postoperative recovery and patient safety.
Patients and methods
Patients
A retrospective study was conducted on 46 patients with large SMTs in the esophagus
who underwent STER in two hospitals from January 2020 to April 2025, including Affiliated
Zhongshan Hospital of Fudan University and The Third Hospital of MianYang. Preoperative
EUS and contrast-enhanced chest computed tomography (CT) were utilized to confirm
the origin of the SMTs from the muscularis propria layer, with the maximum transverse
diameter of the tumors exceeding 5 cm. Prior to the operation, all patients were informed
of the potential benefits and risks associated with the treatment. Written informed
consent was obtained from each patient to ensure informed decision-making and ethical
compliance.
STER procedure
The following instruments and equipment were used for STER: standard single-channel
gastroscope (GIF-Q290J; Olympus Optical Co. Ltd, Tokyo, Japan), transparent cap (D-201–11802;
Olympus), Hybridknife (W0406468, Germany), IT knife (KD-620LR; Olympus), injection
needle (NM-4L-1; Olympus), snare (SD-230U-20; Olympus), Coagrasper hemostatic forceps
(FD-410LR; Olympus), Hemostatic clips (HX-600–135; Olympus; Resolution, Boston, Massachusetts,
United States), CO2 insufflator (Olympus), and ERBE electrosurgical coagulation unit with high-frequency
generator (VIO 200D; ERBE Elektromedizin GmbH, Tübingen, Germany), Nasogastric tube
(Link-02–1, China).
All patients received general anesthesia via endotracheal intubation and were placed
in the left lateral decubitus position. A transparent cap was attached to the distal
end of the endoscope. An incision was made at the mucosa located approximately 5 cm
proximal to the tumor. A mixed solution of epinephrine and indigo carmine diluted
in 0.9% NaCl solution was used for submucosal injection to create a local fluid cushion
in the mucosal layer. Then, a 2-cm mucosal incision was made longitudinally along
the esophagus using a Hybridknife, and the endoscope was inserted through the incision
site into the submucosa. The submucosa and muscularis propria layers were gradually
separated using a Hybridknife. A longitudinal tunnel was created between the two layers
until the tumor was clearly exposed in the tunnel. The tumor was completely dissected
from the surrounding tissues with an intact capsule using a Hybridknife and IT knife.
Tumor extraction was then performed several times using a snare. After tumor resection,
all visible blood vessels were coagulated with hot biopsy forceps. Before closing
the wound with metal clips, an extra step was incorporated. Specifically, a gastric
tube with a 4.7-mm diameter was inserted beneath the wound mucosa to facilitate drainage.
Subsequently, hemostatic clips were utilized to completely seal the tunnel, starting
from the distal end and progressing toward the proximal end. At the proximal end of
the wound, the gastric tube was then led out, serving as a crucial pathway for fluid
removal and ensuring proper management of the post-procedure situation.
Postoperative management
Postoperative medication included proton pump inhibitors and antibiotics, and dietary
restriction was mandatory. Postoperative nursing interventions involved temperature
monitoring and infusion. Daily blood routine examinations were carried out for 3 days
after surgery. The drainage tube was maintained under continuous negative-pressure
suction, and the color and properties of the drained fluid were observed. If the drainage
fluid became turbid, it was necessary to send the drainage fluid for bacterial culture
combined with drug-sensitivity testing. Procalcitonin test and chest CT imaging were
performed on Days 2 and 3 post-STER, respectively. Gastroscopy examination was carried
out 72 hours post-STER for the purpose of evaluating the wound. Simultaneously, patients
with drainage tubes were recommended to have the tubes removed and the defects sealed
with metal clips. In case of infection in the wound, all metal clips were removed
and thoroughly rinsed for drainage.
Data collection and statistical analysis
Collection of clinical records included gender, age, tumor site, pathology, and surgical
scope. SPSS statistical software version 20.0 (IBM Corporation, United States) was
used for data analysis. Descriptive statistics were used to summarize clinicopathological
characteristics of the patients. Categorical variables were compared using the t test,
χ2 test, and Fisher's exact test. The test of significance was a two-sided P < 0.05, and the difference was considered statistically significant.
Results
Clinical characteristics
Baseline characteristics of the 46 patients in this study are shown in [Table 1]. The study was composed of 26 male and 20 female patients. No significant difference
was observed in age, gender, tumor size, pathology results, surgical scope, or mucosal
injury between the two groups studied (P > 0.05). In the non-preventive drainage group, 12 patients suffered from submucosal
infection and/or esophageal fistula; in contrast, in the preventive drainage group,
only two cases of such problems occurred.
Table 1 Clinical characteristics and outcome of different strategy for giant submucosal tumors
in the esophagus.
|
No drainage (n = 18)
|
Preventive drainage (n = 28)
|
P value
|
|
Age, mean (range), years
|
58.06 (22.00–78.00)
|
53.46 (17.00–78.00)
|
0.521
|
|
Gender (male/female)
|
10/8
|
16/12
|
0.382
|
|
Size, median (range), cm
|
5.50 (5.00–6.20)
|
5.72 (5.10–6.30)
|
0.278
|
|
Pathology results, n (%
|
|
Leiomyoma
|
18 (100%)
|
28 (100%)
|
|
|
Surgical scope, n (%)
|
|
Submucosal layer
|
6 (33.33%)
|
10 (35.71%)
|
1.00
|
|
Muscularis propria layer
|
12 (66.67%)
|
18 (64.29%)
|
|
|
Mucosal injury, n (%)
|
7 (38.89%)
|
10 (35.71%)
|
0.56
|
|
Submucosal infection and/or esophageal fistula n (%)
|
12 (66.67%)
|
2 (7.14%)
|
0.038
|
Application of preventive wound drainage in the STER procedure
Esophageal fistula and infection following the STER procedure for removal of SMTs
are indeed severe and concerning complications. To mitigate such complications, a
preventive drainage strategy was devised. This strategy involves surgical steps similar
to the original STER procedure. However, at the crucial stage of closing the tunnel
wound at the end, a distinct step was added. Specifically, a negative-pressure drainage
tube was placed under the mucosa in advance. This anticipatory strategy was expected
to play a vital role in reducing the occurrence of esophageal fistula and infection.
[Fig. 1] shows an example of the STER procedure and drainage.
Fig. 1 Different STER procedure for giant SMTs in the esophagus. a, b, c, d, e The giant submucosal tumor in the esophagus was removed through the traditional STER
surgical method. The black arrow points to the mucosal damage. f, g, h, i, j The traditional STER surgical method combined with preventive wound drainage was
employed for removal of the giant submucosal tumor in the esophagus. The blue arrow
indicates mucosal damage. The green arrow shows the position of the drainage tube.
Preventive wound drainage reduces esophageal fistula or infection after STER of giant
submucosal tumors in the esophagus
To verify that prophylactic wound drainage is capable of reducing the complications
of esophageal fistula and infection following the STER operation, we continuously
monitored the blood routine and measured white blood cell (WBC) levels postoperatively.
It was discovered that prophylactic wound drainage could expedite return of WBC levels
to normal ([Fig. 2]
a). Furthermore, the level of procalcitonin in plasma was significantly lower 48 hours
after the operation than in the control group ([Fig. 2]
b). Simultaneously, we found that preventive drainage reduced fluid and gas accumulation
under the esophageal wound following the STER procedure, which was demonstrated by
chest CT examination 72 hours after the operation ([Fig. 2]
c). To further observe the esophageal wound, routine gastroscopy was performed 72 hours
after the operation. It was discovered that preventive drainage remarkably decreased
tissue necrosis and wound secretion ([Fig. 2]
d).
Fig. 2 Preventive wound drainage reduces esophageal fistula or infection following STER procedure.
a The white blood cell count was measured by blood routine test. ** P < 0.01, t test. b Serum procalcitonin was detected by Elisa test. **P < 0.01, t test. c On the third day following the STER surgery, a chest CT scan was carried out to assess
the condition of the esophagus and its surrounding regions. The blue arrow indicates
fluid and gas accumulation under the esophageal wound. The red arrow shows the position
of the drainage tube. d Seventh-two hours after the STER surgery, a gastroscopy was performed to evaluate
the esophageal wound. Simultaneously, the drainage tube was removed and the remaining
wound was closed with a metal clip.
STER postoperative esophageal fistula or infection is associated with impairment of
the muscularis propria layer and mucosa
Previous investigations have verified that the dimensions, form, and original depth
of esophageal submucosal tumors are elements contributing to risk of postoperative
complications [7]
[8]
[9]. Larger tumors and those with irregular shapes may increase likelihood of intraoperative
esophageal mucosal damage. Consequently, we examined the impact of mucosal and esophageal
muscularis propria injuries on postoperative complications of STER. Intriguingly,
despite our relatively small sample size, we discovered that mucosal and esophageal
muscularis propria injuries significantly increased incidence of esophageal fistula
and infectious complications following STER ([Table 2]).
Table 2 Influence of different layers of esophageal injury on esophageal fistula or infection
after STER.
|
Damage scope
|
Number of occurrences
|
Number of complications
|
Incidence
|
|
STER, submucosal tunneling endoscopic resection.
|
|
Submucosal layer
|
6
|
0
|
0%
|
|
Mucosal layer
|
7
|
6
|
85.71%
|
|
Muscularis propria layer
|
12
|
7
|
58.33%
|
|
Mucosal and Muscularis propria layer
|
6
|
6
|
100%
|
Discussion
STER is a revolutionary endoscopic technique that involves a minimally invasive preservation
of mucosal integrity. Multiple clinical studies have demonstrated the safety and efficacy
of STER for treatment of SMTs. In recent years, several studies have highlighted successful
removal of giant esophageal leiomyomas utilizing either STER or piecemeal STER (P-STER),
but these advancements have also been accompanied by reports of significant postoperative
complications, including bleeding, esophageal fistula or hematocele, and infection
[7]
[8]
[9]. In this paper, we conducted a comprehensive analysis of cases involving submucosal
tumors of the esophagus with a transverse diameter exceeding 5 cm from 2020 to 2024.
Notably, we observed a correlation between serious complications, including esophageal
fistula and infection, and multiple factors related to surgical procedures. These
factors include multiple ruptures of the esophageal mucosa, complete incision of the
esophageal muscle layer, as well as postoperative bleeding. Currently, there is a
notable deficiency in intraoperative prevention strategies aimed at mitigating risks
of postoperative esophageal fistula or infection in patients undergoing STER for giant
submucosal tumors in the esophagus, presenting with the aforementioned high-risk factors.
Here, we have devised an ingenious approach by positioning the drainage device prior
to securing the esophageal mucosa wound with metal clips. This innovative method effectively
addresses the severe complications associated with esophageal fistula and infection,
ensuring a more successful outcome.
Giant submucosal tumors of the esophagus mainly originate from the intrinsic muscle
layer, and the most common pathological type is leiomyoma [10]
[11]. Giant leiomyomas in the esophagus exhibit a distinctive irregular shape. These
tumors display a wide range of sizes and configurations, posing significant challenges
in accurately predicting their appearance. The irregular morphology arises from the
unregulated proliferation of smooth muscle cells, which have the capacity to disseminate
uniformly within the esophageal wall [12]. Previous studies showed that the irregular shape of SMTs is a risk factor for STER-related
major complications [6]
[13]. Endoscopic resection of irregular submucosal tumors is prone to damaging the esophageal
mucosa, constituting the primary factor contributing to postoperative submucosal infections.
Furthermore, resection of irregular submucosal tumors indeed necessitates longer surgery.
The extended operative time inadvertently creates favorable conditions for translocation
of esophageal colonization bacteria, potentially increasing risk of postoperative
infections and complications. In addition, the giant leiomyoma in the esophagus, originating
from the intrinsic muscle layer and exhibiting close and extensive continuity with
this layer, poses a unique challenge during endoscopic resection. Because the entire
muscle layer is detached during the procedure, a substantial cavity forms beneath
the mucosa. Due to the inability of metal clips to fully close this large cavity,
mucosal suturing can lead to favorable fluid accumulation and potential risk of bacterial
infection.
Esophageal fistula or submucosal infection is the most severe STER-related complication
that may require prompt attention and prevent further deterioration and be potentially
life-threatening. Despite administering antibiotics post-STER surgery for removal
of giant esophageal leiomyoma, we noted that a subset of patients exhibited severe
complications, leading to a significant prolongation of their hospital stays [7]
[13]. A previous study confirmed that esophageal stent placement successfully diverted
intraluminal contents from the tunnel, thus preventing contamination of the mediastinum
and thorax [14]. However, utilization of metal stents has not only led to a substantial increase
in hospitalization costs, but has also necessitated rehospitalization of patients
for stent removal. In addition, it is worth noting that not all patients diagnosed
with large esophageal leiomyomas will necessarily develop esophageal fistula or submucosal
infection following STER surgery. Consequently, it is crucial to devise a straightforward
prevention strategy that effectively addresses these clinical challenges and meets
the evolving needs of patients.
Surgical drainage procedures have been widely employed as the primary approach for
managing or averting postoperative infections, owing to their effectiveness in removing
accumulated fluids and debris that can foster bacterial growth and subsequent infection
[14]
[15]. To reduce submucosal infection following STER for giant esophageal leiomyoma, we
placed a gastric tube under the wound mucosa for drainage prior to using metal clips
for wound closure. Simultaneously, we observed the color and volume of the drainage
fluid. After 48 hours, a routine endoscopic examination was performed. If no necrosis
was observed at the wound surface, the drainage tube was immediately removed, and
residual sinuses were closed with metal clips. Remarkably, none of our patients exhibited
any symptoms indicative of esophageal fistula or submucosal infection. This favorable
outcome underscores the effectiveness of our approach in mitigating risks associated
with STER for giant esophageal leiomyoma.
Limitations of this study include the small sample size and absence of a randomized
controlled trial (RCT). First, the surgical strategy necessitates involvement of additional
professionals to offer precise assessments following its implementation, thereby facilitating
determination of whether to proceed with its widespread adoption. Second, a multicenter
RCT should be conducted to further confirm the safety and effectiveness of prophylactic
drainage in reducing esophageal submucosal infection or perforation after endoscopic
resection of giant esophageal submucosal tumors.
Conclusions
Taken together, our study presents a novel strategy aimed at minimizing occurrence
of esophageal fistula complications following STER surgery for giant esophageal submucosal
tumors.
Bibliographical Record
Qiao Yun Liao, Yi Meng Tang, Li Sha Zhan, Yao Fan. Preventive wound drainage reduces
esophageal fistula or infection after endoscopic resection of giant submucosal tumors
in the esophagus. Endosc Int Open 2025; 13: a26873086.
DOI: 10.1055/a-2687-3086
