Risk Factors of Major Intraoperative and Postoperative Bleeding in Gastric ESD

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Risk Factors of Major Intraoperative Bleeding and Postoperative Bleeding Associated with Endoscopic Submucosal Dissection for Gastric Neoplasms

Endoscopic submucosal dissection (ESD) has become a standard treatment for early gastric neoplasms, including intraepithelial neoplasia and early gastric cancer (EGC), due to its high en bloc resection rate. However, ESD carries risks of procedure-related complications, particularly intraoperative bleeding (IB) and postoperative bleeding (PB). This study evaluated the risk factors for major intraoperative bleeding (MIB) and PB using the Endoscopic Resection Bleeding (ERB) classification, a novel system proposed to standardize the assessment of bleeding severity during ESD.

Endoscopic Resection Bleeding Classification

The ERB classification categorizes bleeding into three main grades with five subgrades:

  1. ERB-0: No bleeding observed during ESD due to prophylactic measures.
  2. ERB-controlled (ERB-c): Bleeding controlled endoscopically, subdivided into:
    • ERB-c1: Minor bleeding, easily controlled without affecting vital signs or requiring transfusion.
    • ERB-c2: Moderate bleeding, intermediate in severity between ERB-c1 and ERB-c3.
    • ERB-c3: Major bleeding requiring endoscopic hemostasis and transfusion.
  3. ERB-uncontrolled (ERB-unc): Uncontrollable bleeding necessitating surgical intervention or embolotherapy.

This classification system addresses the variability in reporting bleeding severity across studies and enhances comparability of outcomes.

Methods

Study Design and Patient Cohort

A retrospective analysis included 1,334 patients who underwent gastric ESD between November 2006 and September 2019 at a tertiary medical center. Patients were stratified into two groups:

  • Non-major IB (NMIB): ERB-0, ERB-c1, and ERB-c2.
  • Major IB (MIB): ERB-c3 and ERB-unc.

Exclusion criteria included non-neoplastic lesions, incomplete medical records, and lack of clear endoscopic documentation.

ESD Procedure and Postoperative Care

The ESD protocol included:

  1. Marking and Submucosal Injection: Lesions were circumferentially marked, followed by submucosal injection to lift the mucosa.
  2. Circular Incision and Dissection: Mucosal incision and submucosal dissection were performed using electrocautery tools.
  3. Hemostasis: Exposed vessels were coagulated with argon plasma coagulation (APC), hemostatic forceps, or clips.

Postoperatively, patients received proton pump inhibitors (PPIs), antibiotics for complications like perforation, and a phased dietary progression. PB was defined as hematemesis, melena, hemodynamic instability, or a hemoglobin drop >2 g/dL within 30 days post-ESD.

Statistical Analysis

Risk factors for MIB and PB were analyzed using univariate and multivariate logistic regression. Variables with P < 0.10 in univariate analysis were included in multivariate models.

Results

ERB Classification and Patient Characteristics

Among 1,334 patients, bleeding severity was distributed as follows:

  • ERB-0: 57.95% (773/1,334)
  • ERB-c1: 35.76% (477/1,334)
  • ERB-c2: 5.77% (77/1,334)
  • ERB-c3: 0.52% (7/1,334)
  • ERB-unc: 0%

Male predominance was observed across all ERB categories (P < 0.001), but age, comorbidities (hypertension, diabetes, chronic kidney disease [CKD]), and anticoagulant use showed no significant differences.

Lesion Characteristics

Lesions in the MIB group (ERB-c3) were more frequently located in the upper stomach (57.14%), exhibited submucosal adhesion (42.86%), and had longer procedure times (194.43 ± 153.07 minutes vs. 36–97 minutes in NMIB groups). Ulceration (28.57% in MIB vs. 11.51–19.48% in NMIB) and larger specimen size (4.74 ± 1.72 cm vs. 3.53–4.32 cm) were also associated with MIB.

Procedure-Related Outcomes

  • Procedure Time (PT): Increased significantly with bleeding severity (P < 0.001). ERB-c3 cases had a median PT of 194 minutes, compared to 36 minutes for ERB-0.
  • En Bloc Resection Rate: Declined with higher ERB grades (97.15% in ERB-0 vs. 71.43% in ERB-c3; P < 0.001).
  • Postoperative Bleeding (PB): Rates escalated with ERB severity:
    • ERB-0: 2.20% (17/773)
    • ERB-c1: 3.35% (16/477)
    • ERB-c2: 9.09% (7/77)
    • ERB-c3: 28.57% (2/7)

Risk Factors for Major Intraoperative Bleeding

Multivariate analysis identified two independent predictors of MIB:

  1. Proximal Lesion Location (Upper Stomach): OR 1.488 (95% CI: 1.045–3.645; P = 0.047).
  2. Prolonged Procedure Time (≥120 minutes): OR 19.033 (95% CI: 3.066–118.153; P = 0.002).

Submucosal adhesion and lesion size ≥3 cm were not significant after adjustment.

Risk Factors for Postoperative Bleeding

PB occurred in 3.15% (42/1,334) of cases, with median onset at 2 days post-ESD. Independent risk factors included:

  1. Chronic Kidney Disease (CKD): OR 7.844 (95% CI: 1.637–37.583; P = 0.010).
  2. Major Intraoperative Bleeding (ERB-c3): OR 13.932 (95% CI: 2.585–74.794; P = 0.002).

Notably, 97.62% (41/42) of PB cases occurred within two weeks, and endoscopic hemostasis (APC, clips) was required in 64.29% (27/42).

Discussion

Proximal Lesion Location and Vascular Anatomy

The upper stomach’s complex vascular anatomy and technical challenges in accessing this region likely contribute to its association with MIB. Larger vessels in the proximal mucosa increase bleeding risk during dissection, necessitating meticulous hemostatic techniques.

Chronic Kidney Disease and Coagulopathy

CKD’s association with PB may stem from uremia-induced platelet dysfunction and endothelial damage. Additionally, CKD patients often receive medications exacerbating bleeding risk, underscoring the need for preoperative renal function assessment and tailored hemostatic strategies.

ERB-c3 as a Predictor of Postoperative Bleeding

The strong correlation between ERB-c3 and PB highlights the importance of intraoperative hemostasis quality. Inadequate control of major bleeding during ESD may leave residual vessels prone to delayed rupture, particularly in the lower stomach, where antral peristalsis and bile reflux exacerbate ulcer instability.

Clinical Implications

  1. Prophylactic Measures: Proximal lesions warrant prophylactic coagulation of visible vessels and use of hemostatic powders or clips.
  2. High-Risk Patients: CKD patients and those with ERB-c3 bleeding require intensive postoperative monitoring and extended PPI therapy.
  3. Technical Refinements: Advanced endoscopic tools (e.g., water-jet devices) improve visualization during dissection, aiding early detection of bleeding points.

Limitations

This study’s retrospective design and single-center cohort limit generalizability. The low incidence of ERB-unc (0%) and ERB-c3 (0.52%) restricted multivariate analysis power. Prospective, multicenter studies are needed to validate these findings.

Conclusion

Proximal gastric lesions, CKD, and major intraoperative bleeding (ERB-c3) are critical risk factors for adverse bleeding outcomes in ESD. The ERB classification provides a standardized framework for assessing bleeding severity, guiding clinical management, and enhancing comparability across studies. Tailored interventions for high-risk patients and lesions may improve safety and outcomes in gastric ESD.

https://doi.org/10.1097/CM9.0000000000001840

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