Endoscopic submucosal dissection for early gastric cancer and precancerous lesions enhances postoperative recovery and mitigates complication risks

Abstract

BACKGROUND

Early gastric cancer (EGC) or precancerous lesions (PCLs) are generally small tumors and carry a diminished chance of nodal infiltration. Thus far, very few studies have examined how endoscopic submucosal dissection (ESD) affects postoperative recovery and complications in such patients.

AIM

To evaluate the influence of ESD on postoperative recovery and complications in patients with EGC or PCL.

METHODS

The study population included patients with EGC and PCL admitted to The First People’s Hospital of Fuyang District between December 2022 and December 2024, who were divided into the research (n = 65) and control (n = 55) groups if they underwent ESD and laparoscopic radical gastrectomy, respectively. Therapeutic outcomes (en bloc and curative resection rates), surgical parameters (incision length, intraoperative bleeding, and operative duration), postoperative recovery indices (time to first ambulation/flatus/first oral intake, and hospital stay duration), complications (infection, outflow obstruction, bleeding, and perforation), and tumor markers [carcinoembryonic antigen (CEA) and carbohydrate antigen (CA) 125/19-9] were comparatively evaluated.

RESULTS

Compared with the control group, the research group achieved a significantly higher en bloc resection rate but a notably lower curative resection rate. Additionally, the research group demonstrated shorter incision lengths, reduced intraoperative bleeding, and shorter operative duration. Regarding postoperative recovery, the research group demonstrated earlier ambulation, faster bowel function restoration, quicker oral intake resumption, and shorter hospital stays. Furthermore, an evidently lower overall complication rate was recorded in the research group, as well as markedly reduced postoperative CEA, CA125, and CA19-9 concentrations.

CONCLUSION

When performed for EGC and PCLs, ESD demonstrates advantages such as higher en bloc resection (although lower curative resection rates), surgical trauma minimization, shortened operative duration, and faster recovery. Moreover, it is effective in reducing serum tumor marker levels while maintaining favorable safety.

Key Words: Endoscopic submucosal dissection; Early gastric cancer; Precancerous lesions; Postoperative recovery; Complications

Core Tip: This study examined how endoscopic submucosal dissection (ESD) influences postoperative recovery and complications in early gastric cancer (EGC) or precancerous lesions (PCLs). Compared with laparoscopic radical gastrectomy, performing ESD for treating EGC and PCLs led to superior en bloc resection, shortened surgical incision length, intraoperative bleeding reduction, and shorter operative duration. Moreover, it effectively accelerated postoperative recovery, lowered complications, and improved serum tumor marker expression.

INTRODUCTION

Gastric cancer (GC), a stomach-derived malignancy, is a growing threat to global well-being[1]. The 2020 statistics indicate over 1 million new GC diagnoses worldwide and approximately 800000 related fatalities[2]. Early GC (EGC), characterized by mucosa- or submucosa-confining invasive growths, now makes up to half of cases owing to the effective implementation of screening initiatives, which consequently leads to markedly better clinical outcomes (5- to 10-year survival rate > 90.0%)[3]. Patients with EGC or precancerous lesion (PCL) typically exhibit limited tumor burden and a diminished chance of nodal infiltration. For such patients, early interventions can significantly extend long-term survival and increase the likelihood of complete cure[4,5]. Laparoscopic radical gastrectomy (LRG), while remaining a common lesion excision technique, is challenged by extended operative durations, high hospitalization expenses, and postoperative recurrence potential[6,7]. Endoscopic submucosal dissection (ESD), being minimally invasive treatment for EGC and PCL, contributes to better quality of life by preserving gastric anatomy while minimizing complications[8]. In a study of EGC treatment by ESD, Ryu et al[9] highlighted the high efficacy of ESD, boosting enduring neoplastic regulation and reduced local recurrence (3.1%). Costa et al[10] corroborated the procedure’s optimal safety and durable therapeutic benefits for EGC and PCLs, accompanied by low recurrence probability. However, research examining how ESD affects postoperative recovery and complications among patients with EGC and PCL is insufficient. Through a methodical study of this under-researched area, this study aimed to produce evidence-based recommendations to guide decision-making and improve the management of these conditions.

MATERIALS AND METHODS

General information

This study enrolled 120 patients with EGC or PCL admitted to our hospital between December 2022 and December 2024. They were divided into the research group who underwent ESD (n = 65) and the control group who received LRG (n = 55).

The eligibility criteria were as follows: Endoscopically identified and biopsy-proven EGC or PCLs[11], initial diagnosis and treatment-naive, surgical candidates for LRG or ESD[12,13], absence of cognitive, communicative, or mental dysfunction, and completeness of clinical data.

The exclusion criteria were as follows: Nodal metastasis identified before operative intervention; coexisting malignancies; pregnant or breastfeeding status; serious cardiac, pulmonary, or renal impairments; coagulopathies or infectious pathologies; malignant involvement of the muscularis propria; gastric ulcers or vascular tumors; and psychopathological conditions.

Treatment methods

Each patient underwent standard presurgical workups, covering hematologic testing, electrocardiography, abdominal computed tomography, and coagulation function assessments. A fasting period of 8-10 hours was required before the procedure.

Control group (LRG): General anesthesia was induced through endotracheal intubation, followed by urinary catheter placement. The patient was positioned in a 20° reverse Trendelenburg (head-up, feet-down) orientation, with intraoperative end-tidal CO₂ maintained between 35 and 45 mmHg. A pneumoperitoneum was created through an umbilical puncture, maintaining a pressure of 12-14 mmHg (1 mmHg = 0.133 kPa). Laparoscopic instruments were introduced following a four-port technique. After identifying the lesion, surrounding veins were dissected using an ultrasonic knife. The right gastroepiploic artery and vein were severed along the transverse colon, and lymph nodes were dissected. The dissection of the right gastroepiploic vessels continued toward the common bile duct. The jejunum was exteriorized through an antecolic approach, and a Roux-en-Y gastrojejunostomy was created 15 cm distal to the ligament of Treitz. Postoperatively, the surgical area was irrigated and sutured, and a drainage tube was placed. Prophylactic antibiotics were administered to prevent infection.

Research group (ESD): After the induction of intravenous general anesthesia, the gastric cavity was examined endoscopically to locate the tumor. The lesion was stained with 0.4% indigo carmine, and marking dots were placed at 2 mm intervals. Then, 0.4% sodium hyaluronate mixed with 1:10000 adrenaline was injected submucosally near the marking points. Once the mucosal layer was elevated by 0.5-0.8 cm, an IT knife was used to incise the mucosa at the edge of the elevation, followed by gradual submucosal dissection. Additional injections of the solution were given as needed to sustain mucosal elevation until the lesion was completely resected. Intraoperative bleeding or perforation was addressed using thermal coagulation or titanium clips. Postoperatively, preventive hemostasis was applied on the wound, which involved using hemostatic forceps for thermal coagulation of exposed vessels or the application of polysaccharide hemostatic bioadhesive to the wound. A drainage tube was routinely placed. Postoperatively, the patient was kept on a 24-hour fasting period. After confirming the absence of bleeding, a gradual transition to a low-residue enteral nutritional solution was initiated (after 48 hours), and dietary intake followed a stepwise progression and small, frequent meals. On the day of surgery, patients were encouraged to engage in limb exercises and regular turning in bed. Ankle pump exercises were encouraged 12 hours postoperatively, and bedside ambulation was initiated after 24 hours. Nursing staff evaluated pain levels, inspected the incision, and provided updates on postoperative recovery to improve patients’ confidence in their rehabilitation.

Evaluation metrics

Treatment efficacy: This was evaluated by comparing the rates of en bloc resection and curative resection between the two groups[14]. En bloc resection refers to the complete removal of suspicious lesions detected during endoscopic examination. Curative resection involves excising the tumor along with cancerous infiltration extending to a depth of ≥ 500 μm beneath the muscularis mucosa.

Surgical parameters: For both groups, the following surgical metrics were monitored and documented: Surgical incision length, intraoperative blood loss, and operative duration.

Postoperative recovery: Postoperative recovery was assessed based on the time to first postoperative ambulation, first flatus, and first oral intake, and duration of hospital stay.

Complication rates: Patients in each group who experienced adverse reactions, such as infection, outflow obstruction, bleeding, and perforation, were observed. Subsequently, the incidence rate was calculated based on these observations.

Tumor markers: Fasting peripheral venous blood samples (5 mL) were collected from patients before treatment and 1 week following treatment. Serum was isolated through centrifugation, and the levels of carcinoembryonic antigen (CEA), carbohydrate antigen (CA)125, and CA19-9 were quantified using enzyme-linked immunosorbent assay.

Statistical analysis

Continuous variables were summarized as mean ± SE of the mean. Between-group differences were analyzed using independent samples t-tests, whereas paired t-tests were employed to compare pre- and post-treatment values within each group. Categorical variables were presented as percentages, and group comparisons were performed using χ² tests. Data analysis was conducted using IBM SPSS Statistics version 22.0, and graphical representations were created using GraphPad Prism 7.0. A P value of < 0.05 was deemed significant.

RESULTS

General characteristics of the research and control groups

No significant differences were observed between the research and control groups in terms of sex, age, body mass index, tumor diameter, presence of single lesion, ulceration, and tumor location (P > 0.05). Table 1 provides detailed information.

Table 1 Baseline characteristics of research and control groups.

Data	Research group (n = 65)	Control group (n = 55)	χ2/t value	P value
Gender (male/female)	42/23	40/15	0.906	0.341
Age (years)	59.72 ± 7.57	61.15 ± 9.22	0.933	0.353
Body mass index (kg/m2)	23.03 ± 2.42	23.25 ± 2.85	0.457	0.648
Tumor diameter (mm)	19.88 ± 1.61	20.18 ± 1.76	0.974	0.332
Single lesion presence (yes/no)	32/33	29/26	0.146	0.703
Ulceration (yes/no)	22/43	25/30	1.685	0.194
Tumor location (antrum/body/cardia and body)	36/16/13	32/15/8	0.629	0.730

Treatment outcomes in the research and control groups

Compared with the control group, the research group demonstrated a markedly higher en bloc resection rate but a notably lower curative resection rate (all P < 0.05). Detailed data are presented in Table 2.

Table 2 Comparison of treatment efficacy between research and control groups, n (%).

Treatment outcome	Research group (n = 65)	Control group (n = 55)	χ2	P value
En bloc resection rate	59 (90.77)	39 (70.91)	7.848	0.005
Curative resection rate	6 (9.23)	16 (29.09)

Surgical parameters in the research and control groups

When compared with the control group, in the research group exhibited significant reductions in the surgical incision length, intraoperative blood loss, and operative duration (P < 0.001). These findings are illustrated in Figure 1.

Figure 1 Comparative analysis of surgical incision length, intraoperative blood loss, and operation duration between groups. A: Comparison of surgical incision length; B: Comparison of intraoperative blood loss; C: Comparison of operation duration. ^aP < 0.001, indicating a significant difference from the control group.

Postoperative recovery metrics across the groups

The research group achieved significantly shorter time to first postoperative ambulation, flatus, and oral intake and shorter overall hospital stays than the control group (P < 0.01). This comparison is depicted in Figure 2.

Figure 2 Postoperative recovery metrics between research and control groups. A: Time to first ambulation in research and control groups; B: Time to first flatus in research and control groups; C: Time to first oral intake in research and control groups; D: Length of hospital stay in research and control groups. ^aP < 0.01, highlighting significant differences from the control group.

Incidence of complications in both groups

The overall complication rate encompassing infection, outflow obstruction, hemorrhage, and perforation was lower in the research group than in the control group (P < 0.05). Specific details are provided in Table 3.

Table 3 Complication rates between research and control groups, n (%).

Complications	Research group (n = 65)	Control group (n = 55)	χ2	P value
Infection	0 (0.00)	3 (5.45)
Outflow obstruction	0 (0.00)	2 (3.64)
Hemorrhage	2 (3.08)	6 (10.91)
Perforation	7 (10.77)	8 (14.55)
Total	9 (13.85)	19 (34.55)	7.135	0.008

Pre- and postoperative tumor marker levels in both groups

Preoperative assessments revealed no significant disparities in CEA, CA125, and CA19-9 Levels between the two groups (P > 0.05). After surgery, all markers decreased significantly (P < 0.05), with the research group exhibiting even lower levels than the control group (P < 0.05). These trends are captured in Figure 3.

Figure 3 Carcinoembryonic antigen, carbohydrate antigen 125, and carbohydrate antigen 19-9 levels pre- and post-surgery in research and control groups. A: Carcinoembryonic antigen levels in research and control groups; B: Carbohydrate antigen (CA)125 levels in research and control groups; C: CA19-9 levels in research and control groups. CEA: Carcinoembryonic antigen; CA: Carbohydrate antigen. ^aP < 0.01, ^bP < 0.001, reflecting significant changes from preoperative levels; ^cP < 0.05, denoting significant differences from the control group.

DISCUSSION

This study involved 120 patients diagnosed with EGC and PCLs to compare the therapeutic outcomes between those undergoing ESD (research group) and those receiving LRG (control group). A notable finding was that ESD yielded a higher en bloc resection rate for EGC and PCLs, albeit with a comparatively lower curative resection rate, than LRG. This could be due to the utilization of a needle knife to excise the mucosa surrounding the lesion in ESD, accompanied by the continuous infusion of a mixed solution during dissection. This method promotes the detachment of the muscular layer from the affected mucosa, proving particularly effective for the removal of extensive and irregularly shaped lesions, thereby increasing the tumor’s en bloc resection rate[15]. Given that malignant lesions may extend beyond the submucosal layer, en bloc resection alone cannot be considered invariably curative[16]. This result was supported by Xu et al[17], who reported that ESD demonstrated a significantly higher curative resection rate and en bloc resection rate than endoscopic mucosal resection (EMR) in patients with EGC and PCLs, closely mirroring our results. Moreover, compared with LRG, ESD for EGC and PCLs was associated with significantly reduced surgical incision length, lesser intraoperative blood loss, and shorter operative duration, implying that ESD imposes less physical trauma on patients, potentially accelerating postoperative recuperation. The postoperative recovery metrics further underscored the superiority of ESD, with patients achieving shorter time to first ambulation, flatus, and oral intake and shorter hospital stays. This finding indicates that ESD effectively aids in the restoration of postoperative gastrointestinal functionality. The precision of ESD in targeting tumor tissue while sparing the normal gastrointestinal architecture likely mitigates surgical stress responses, minimizes collateral damage to adjacent vascular and neural structures, enhances anal exhaust timing, and promotes expedited recovery, culminating in shortened hospital stay[18-20]. Additionally, the minimally invasive nature of ESD, characterized by its procedural simplicity and reduced operative time, further contributes to its recovery benefits[21]. Regarding prevention of complications, ESD demonstrated a clear advantage, significantly lowering the rates of infection, outflow obstruction, hemorrhage, and perforation in patients with EGC and PCL. Although perforation and bleeding are risks associated with ESD, the strategic application of electrocoagulation for hemostasis and the use of clip closures during the procedure have been effective in curtailing these adverse events, thereby diminishing the overall complication rate[22,23]. Furthermore, in this study, ESD was instrumental in significantly decreasing the serum levels of CEA, CA125, and CA19-9 among patients with EGC and PCL. These biomarkers, intimately linked with GC progression, serve as vital indicators for monitoring patient status and disease progression[24,25].

A previous study further highlighted the efficacy of ESD in treating early-stage neoplasms and PCLs. As reported by Tan et al[26], the post-ESD complication rate was merely 12.5% (1/8 cases) in patients with cirrhosis and early-stage cancer or upper gastrointestinal PCLs, with all cases remaining recurrence-free over 45 months of monitoring. Yu et al[27] also demonstrated the effectiveness and safety of ESD in managing early-stage colorectal cancer and PCLs, achieving a 100% local control rate throughout 20 months of postoperative monitoring.

However, this study has several limitations, highlighting the need for further exploration: (1) Validation through larger, multicenter studies is needed, given the restricted sample size that could possibly limit the generalizability and analytical rigor of the study; (2) Owing to the relatively brief observation period, ESD‘s long-term effectiveness and recurrence risks might not be adequately captured, underscoring the need for prolonged surveillance to assess durable outcomes; (3) Differences in biological behaviors among undifferentiated GC subtypes (e.g., pure signet ring cell carcinoma vs mixed forms) and between differentiated and undifferentiated types may remain unclear owing to the lack of stratified research; (4) An in-depth evaluation of ESD and alternative minimally invasive approaches (e.g., EMR) in the removal of sizable lesions remains imperative. Supplementing such analysis would provide clearer insights into optimal patient selection for these interventions; and (5) Given that all procedures were performed by highly skilled endoscopists, the outcomes may reflect expertise-dependent results. Such future analyses could deepen our knowledge of the therapeutic efficacy and clinical outcomes across different subtypes. Subsequent research may address these areas to improve the precision of the conclusions.

CONCLUSION

In summary, ESD performed to treat EGC and PCLs markedly enhances the en bloc resection rate, minimizes surgical incision length, reduces intraoperative blood loss, and shortens operative duration. It also facilitates smoother postoperative recovery, decreases the overall incidence of postoperative complications, and improves serum tumor marker levels, making it a highly recommendable clinical approach. These findings offer robust support for clinical decision-making in the treatment of patients with EGC and PCL.