Abstract
Background/Aims
Endoscopic submucosal dissection (ESD) of gastric neoplasm involving the pyloric channel (GNPC) is technically challenging due to difficulty in precise assessment of resection margin and inadequate visualization. The aim of this study was to evaluate the effectiveness and long-term outcome of ESD for GNPC and introduce a noble technique for resection of GNPC.
Methods
A total of 97 patients with GNPC underwent ESD from January 2007 to October 2017. We divided them into a conventional anterograde resection group and a retrograde resection group according to the method of procedure. We compared their clinical outcomes and investigated risk factors for postprocedural complications.
Results
The en bloc resection rate was 87.6%, and complete resection rate was 83.5%. Postprocedure stenosis occurred in 16 cases (16.5%). GNPCs of the retrograde resection group were more frequently located from antrum to bulb, were significantly larger, were related to ≥75% resection of the circumference, and involved significantly longer procedure times than those in the anterograde resection group. Multivariate analysis showed that resection ≥75% of the circumference was the only significant risk factor for postprocedure stenosis.
Conclusions
ESD by retrograde resection method is a novel technique to make the procedure easier, depending on the size, location, and circumference of resection.
Keywords: Gastric neoplasms, Pylorus, Endoscopic submucosal dissection
INTRODUCTION
Endoscopic submucosal dissection (ESD) has been widely accepted as a curative procedure for gastric neoplasm such as early gastric cancer (EGC), gastric adenoma, and gastric subepithelial tumor. With the development and widespread of the screening system in South Korea, the diagnosis of gastric adenoma and EGC has increased. The importance of ESD technique is also increasing. As ESD technique developed, there was no difference in the 5-year overall survival rate in treating gastric neoplasm between ESD and surgery. Thus, ESD is currently considered a standard treatment of EGC if cases are corresponding to absolute and expanded indications.1-4
However, it is technically difficult to perform successful ESD if one of the following reasons is present: (1) the lesion is located at the esophago-gastric junction, cardia, high-body, or pyloro-duodenum; (2) large tumor size; (3) ulceration or fibrotic scar coexists; and (4) demarcation line is not clear.5-10 Among them, ESD of gastric neoplasia involving the pyloric channel (GNPC) is technically challenging due to narrow lumen of channel and difficulty in precise assessment of the distal margin.7,11-13 However, few studies have shown the efficacy and safety of endoscopic resection of GNPC.
The method of ESD through retro-flexion of the endoscope for GNPC was first reported in 2002. Several authors later have reported clinical outcomes of ESD through retro-flexion in case series studies.6,7,12-15 The retrograde resection method has been studied and used a lot in endoscopic resection of rectal lesions. However, in terms of GNPC, the number of cases is relatively small and specific procedure methods are not demonstrated.16,17
In this study, we proposed a novel technique to treat GNPC more effectively and safely. We evaluated the feasibility and effectiveness of the ESD through retro-flexion of the endoscope for GNPC and compared with the conventional anterograde resection method. We also investigated predictive factors for postprocedural stenosis during follow-up.
MATERIALS AND METHODS
1. Patients
We retrospectively reviewed medical records of a total of 97 patients with GNPC who underwent ESD from January 2007 to October 2017 in a tertiary hospital. We obtained informed consent from all patients before the procedure who agreed to undergo endoscopic resection for the treatment of GNPC and the possibility of occurrence of postprocedural complications including pyloric stenosis. This study was approved by the Ethics Committee of Korea University Guro Hospital (IRB number: K2019-2354-001).
2. ESD procedure by retrograde method
All patients underwent ESD procedure under sedation with an intravenous administration of propofol (1.0 mg/kg) or midazolam (0.035 mg/kg) with close cardio-pulmonary function monitoring. We used conventional flexible endoscopy (GIF-Q260J; Olympus, Shinjuku, Tokyo, Japan) for performing ESD. All procedures were performed by an expert (J.J.P.) who had experience of performing more than 2,000 cases of gastric ESD.
Initially, we checked the margin of the lesion and marked it using needle coagulation. Injection of diluted epinephrine saline solution (dilution rate 1:10,000) that was mixed with indigo carmine dye was followed. Precutting and limited incision on both sides of the distal margin around the pyloric ring were done using a needle knife (KD-IL-1; Olympus), serving as a starting point for incision with retro-flexed endoscope and retrograde dissection from the bulb to antrum. The small incision pocket enhanced mucosal contraction and bulging of the dissecting flap during dissection within the bulb. Retrograde dissection using an insulated-tipped electrosurgical knife (KD-610L; Olympus) crossing the pyloric channel was done as far as possible in order to lift up the dissected bulbar portion of the lesion over the pyloric ring to make a “floating tongue-like” flap toward antrum. Then, dissecting with anterograde approach from antrum to pyloric channel was done for complete resection. The more distance is dissected by retrograde approach beyond pyloric channel, the more meeting point moves upwards towards the antrum, making it easier to finalize resection of the lesion with anterograde approach (Fig. 1). After removing the lesion, electro-coagulation or endo-clipping of visible vessel was done to prevent major bleeding.
Fig. 1.
Techniques of retrograde transpyloric antral dissection. (A) A flat lesion is found on the anterior wall of the prepylorus. (B) Precutting and limited incision on both sides of the distal margin around the pyloric ring are done, serving as a starting point for incision. (C) With a retro-flexed endoscope, retrograde dissection is done from the bulb to antrum. (D) Retrograde dissection crossing the pyloric ring is done as far as possible in order to lift up the dissected bulbar portion of the lesion over the pyloric ring to make a “floating tongue-like flap.” (E) Dissection is performed in an antegrade manner from antrum to pyloric channel, where the antegrade dissection (red arrow) and retrograde dissection (yellow arrow) points meet.
We did not perform routine preventive method for possible stenosis after ESD for GNPCs. However, if significant stenosis was found during follow-up esophagogastroduodenoscopy, rescue procedure such as endoscopic balloon dilatation was performed whenever necessary.
3. Definition
We defined GNPC as tumors with the distal margin located within a half centimeter from the pyloric ring when the ring was fully open. We defined en bloc resection when the tumor was completely resected as single piece and complete resection as the lesion was resected en bloc with negative vertical and lateral margin without lympho-vascular invasion on microscopic examination. Recurrence was defined as the new lesion confirmed by endoscopic biopsy after the procedure showed local recurrences, synchronous lesions, metachronous lesions, and distant metastatic lesions.18,19 We defined pyloric stenosis when the endoscope could not pass through the lumen of pyloric channel and patients complained symptoms associated with pyloric stenosis such as nausea and vomiting.
4. Post-ESD follow-up and recurrence assessment
After ESD, an esophagogastroduodenoscopy was performed at intervals of 3 to 6 months for the first year and annually thereafter. Biopsy was performed on ESD scars to confirm local recurrence during endoscopic examination. Random biopsy on antrum and corpus or rapid urease test were performed during follow-up esophagogastroduodenoscopy for evaluation of Helicobacter pylori status. We regarded as current infection of was defined H. pylori if either biopsy with special stain or rapid urease test were positive.
5. Study designs
We subdivided cases based on the location of GNPC, the resection method, and the circumference of resection. First, we subdivided the resection method as anterograde and retrograde resection. In anterograde resection, we performed precut incision from distal margin with forward viewing and dissected the submucosa as standard manner. In contrast, in retrograde resection, we performed precut incision and submucosal dissection of distal part with retroflection of the scope in the bulb and subsequently finished the proximal part with forward viewing. Second, we subdivided the location of GNPC as confined to channel, antrum to channel, channel to bulb, and antrum to bulb through the channel. Third, we subdivided the circumference of resection as <25%, 25% to 75%, and ≥75%. We compared clinical outcomes of anterograde resection to retrograde resection and retrospectively analyzed risk factors with odds ratio for postprocedural stenosis.
6. Statistical analysis
All statistical analyses were performed using SPSS software version 20.0 (IBM Corp., Armonk, NY, USA) with significance level set at p<0.05. The Student t-test was used for continuous data and chi-square test for categorical data to compare clinical outcomes of procedures. A multivariate logistic regression analysis was performed to analyze risk factors and odds ratio for postprocedural stenosis.
RESULTS
1. Baseline Characteristics and procedure outcomes
The mean age of subjects was 63.1±9.6 years (60.8% male). A total of 77 cases (79.4%) were confined to channel with or without involvement of the antrum or bulb. Among them, 23 cases (23.7%) were confined to the channel, 49 cases (50.5%) were confined from the antrum to channel, and 5 cases (5.2%) were confined from the channel to bulb. The other 20 cases (20.6%) were located from the antrum to bulb through the channel. Forty cases (41.2%) showed H. pylori infection. On histopathologic evaluation, 42 cases (43.3%) were low grade dysplasia, 16 cases (16.5%) were high grade dysplasia, and 34 cases (35.1%) were EGC. Mean tumor size was 14.6±9.2 mm (Table 1).
Table 1.
Clinicopathological Characteristics of Gastric Neoplasm Involving the Pyloric Channel
| Variable | Data (n=97) |
|---|---|
| Age, mean±SD, yr | 63.1±9.6 |
| Sex, No. (%) | |
| Male | 59 (60.8) |
| Female | 38 (39.2) |
| Location, No. (%) | |
| Confined to channel, antrum or bulb | 77 (79.4) |
| Confined to channel | 23 (23.7) |
| Antrum–channel | 49 (50.5) |
| Channel–bulb | 5 (5.2) |
| Antrum–bulb | 20 (20.6) |
| Helicobacter pylori infection, No. (%) | 40 (41.2) |
| Histopathology, No. (%) | |
| Low grade dysplasia | 42 (43.3) |
| High grade dysplasia | 16 (16.5) |
| Early gastric cancer | 34 (35.1) |
| Miscellaneous | 5 (5.2) |
| Tumor size, mean±SD, mm | 14.6±9.2 |
All cases were resected with the ESD technique. Circumference of resection was <25% in 16 cases (16.5%), 25% to 75% in 39 cases (40.2%), and ≥75% in 42 cases (43.3%). Mean procedure time was 38.2±19.6 minutes. Only four cases (4.2%) showed major complications (perforation and major bleeding in two cases, respectively). En bloc resection rate and complete resection rate were 87.6% (85/97) and 83.5% (81/97), respectively. Postprocedure stenosis occurred in 16 cases (16.5%). During 37 months (median, 1 to 118 months) of follow-up period, there was one (1.0%) case of recurrence that was done by anterograde resection. Three cases (3.1%) required additional surgery (Table 2).
Table 2.
Technical Outcomes of Endoscopic Submucosal Dissection in Gastric Neoplasm Involving the Pyloric Channel
| Variable | No. (%) |
|---|---|
| Procedure type | |
| Endoscopic submucosal dissection | 97 (100) |
| Circumference of resection | |
| <25% | 16 (16.5) |
| 25% to <75% | 39 (40.2) |
| ≥75% | 42 (43.3) |
| Procedure time, mean±SD, min | 38.2±19.6 |
| Immediate complication | |
| Perforation | 2 (2.1) |
| Major bleeding | 2 (2.1) |
| Loss of hemoglobin, mean±SD, g/dL | 0.5±0.7 |
| En bloc resection | 85 (87.6) |
| Complete resection | 81 (83.5) |
| Postprocedural stenosis | 16 (16.5) |
| Recurrence rate | 1 (1.0) |
| Additional surgery | 3 (3.1) |
2. Comparison of anterograde resection and retrograde resection
Anterograde resection was performed in 47 patients (48.5%), and retrograde resection was performed in 50 patients (51.5%). In the retrograde resection group, lesions were more frequently located from the antrum to bulb through the channel (3 [6.4%] vs 17 [34.0%], p=0.001) and tumor size was significantly larger (11.7±7.2 mm vs 17.4±10.0 mm, p=0.002). Circumference of resection ≥75% was significantly frequent in the retrograde resection group (14 [29.8%] vs 28 [56.0%], p<0.001). Procedure time was significantly longer in the retrograde group (30.8±17.0 minutes vs 45.1±19.4 minutes, p<0.001). Other variables including H. pylori infection rate, histopathology, complication rate, en bloc and complete resection rate, recurrence rate, and percentage of additional surgery were not significantly different between the two groups. Postprocedure stenosis occurred in five (10.6%) cases of the anterograde group and 11 (22.0%) cases of the retrograde group, showing no significant difference between the two groups (p=0.132). Among three patients who needed additional surgery, one case (2.1%) was in the antegrade resection group with recurrence of tumor and two cases (4.0%) were in the retrograde resection group (one was due to postprocedure stenosis and the other was due to involvement of deep resection margin by carcinoma) (Table 3).
Table 3.
Comparison of Clinicopathological Characteristics of Patients in Anterograde Resection and Retrograde Resection Groups
| Variable | Anterograde resection (n=47) | Retrograde resection (n=50) | p-value |
|---|---|---|---|
| Age, yr | 62.7±9.1 | 63.5±10.2 | 0.694 |
| Male sex | 27 (57.4) | 32 (64.0) | 0.509 |
| Location | 0.001 | ||
| Confined to channel, antrum or bulb | 44 (93.6) | 33 (66.0) | |
| Antrum–bulb | 3 (6.4) | 17 (34.0) | |
| Helicobacter pylori infection | 20 (42.6) | 20 (40.0) | 0.798 |
| Histopathology | 0.471 | ||
| Low grade dysplasia | 20 (42.6) | 22 (44.0) | |
| High grade dysplasia | 7 (14.9) | 9 (18.0) | |
| Early gastric cancer | 19 (40.4) | 15 (30.0) | |
| Miscellaneous | 1 (2.1) | 4 (8.0) | |
| Tumor size, mm | 11.7±7.2 | 17.4±10.0 | 0.002 |
| Circumference of resection | <0.001 | ||
| <25% | 15 (31.9) | 1 (2.0) | |
| 25% to <75% | 18 (38.3) | 21 (42.0) | |
| ≥75% | 14 (29.8) | 28 (56.0) | |
| Procedure time, min | 30.8±17.0 | 45.1±19.4 | <0.001 |
| Immediate complication | |||
| Perforation | 1 (2.1) | 1 (2.0) | 0.965 |
| Major bleeding | 1 (2.1) | 1 (2.0) | 0.976 |
| Loss of hemoglobin, g/dL | 0.6±0.7 | 0.5±0.7 | 0.905 |
| En bloc resection | 41 (87.2) | 44 (88.0) | 0.909 |
| Complete resection | 39 (82.9) | 42 (84.0) | 0.892 |
| Postprocedural stenosis | 5 (10.6) | 11 (22.0) | 0.132 |
| Recurrence rate | 1 (2.1) | 0 | 0.300 |
| Additional surgery | 1 (2.1) | 2 (4.0) | 0.228 |
Data are presented as mean±SD or number (%).
3. Multivariate analysis of risk factors for postprocedural stenosis
Multivariate analysis showed that circumference resection ≥75% was the only significant risk factor for postprocedure stenosis (odds ratio, 20.155; 95% confidence interval, 2.105 to 193.000; p=0.009). Location, histopathology, tumor size, procedure time, and piecemeal resection or incomplete resection were not significant risk factors (Table 4).
Table 4.
Multivariate Analysis of Risk Factors for Postprocedural Stenosis
| Variable | Odds ratio (95% CI) | p-value |
|---|---|---|
| Location | ||
| Confined to channel, antrum or bulb |
Reference | |
| Antrum–bulb | 2.703 (0.472–15.479) | 0.264 |
| Histopathology | ||
| Low grade dysplasia | Reference | |
| High grade dysplasia | 8.029 (0.664–97.084) | 0.101 |
| Early gastric cancer | 3.608 (0.377–34.526) | 0.265 |
| Tumor size | 1.142 (0.973–1.341) | 0.103 |
| Circumference of resection | ||
| <75% | Reference | |
| ≥75% | 20.155 (2.105–193.000) | 0.009 |
| Procedure time | 0.968 (0.920–1.018) | 0.204 |
| Piecemeal resection | 0.318 (0.011–9.420) | 0.507 |
| Incomplete resection | 2.433 (0.144–41.018) | 0.537 |
CI, confidence interval.
DISCUSSION
In this study, we tried to devise a more effective endoscopic method for performing endoscopic resection for EGC and gastric adenoma including pyloric channels and to find out which situations might be closely associated with postprocedural complications such as stenosis.
Conventional anterograde resection is an effective treatment for resection of lesions such as low to mid-body and proximal antrum. However, for GNPC, it is technically difficult to properly access the distal margin. As a result, the curative resection rate may decrease and postprocedural complications such as pyloric stenosis may occur.20-22 Thus, we assessed GNPC with retrograde resection, a method of accessing the distal margin through the retro-flexion of endoscope in the duodenal bulb, and compared clinical outcomes with those of conventional anterograde resection.
As mentioned in results, the retrograde resection group had larger lesion size with lesions located through the antrum to bulb and resected circumference over 75%. However, there were no significant differences in en bloc resection rate, complete resection rate, recurrence rate, or frequency of postprocedural complication rate. These results suggest that in GNPC, retrograde resection can be an effective method if the lesion has a larger size or if it is located through the antrum to bulb. This might be caused by the easy access to the distal margin through the retro-flexion of the endoscope.6,13,14 Meanwhile, procedure time was significantly longer in the retrograde resection group, which might be caused by the larger lesion size and difficult assess to the lesion when it is located through antrum and bulb.
Postprocedural stenosis, one of the most concerned postprocedural complications of GNPC, was likely to occur in the case of channel circumference of resection ≥75%. Previous Korean and Japanese studies demonstrated that circumference of resection over 75% were significant risk factors for postprocedural stenosis in ESD of GNPCs in common, which was consistent with our result.23-26 More frequent follow-ups should be considered and endoscopic balloon dilatation might be required if stenosis occurs.23,24
This study was meaningful in that it introduced an effective method of resection of GNPC and identified risk factors for predicting postprocedural stenosis, a major complication. However, this study had several limitations. First, in addition to postprocedural stenosis, this study did not identify risk factors for bleeding or perforation. Bleeding and perforation are severe complications that could occur after ESD. However, we had only two cases of perforation and bleeding, respectively, suggesting that ESD in GNPC might be a safe therapeutic modality. Second, this study was based on a retrospective, single-center study. Therefore, several variables such as range of the lesion, tumor size, circumference of resection and procedure time are not fairly matched. Thus, it is premature to generalize our results. Further studies including larger cases performed by a multicenter are needed in the future.
In conclusion, ESD is a feasible method for treating GNPC and retrograde resection method may be effective for larger tumor located throughout the antrum and bulb with circumference of resection ≥75%. For a successful ESD of GNPCs, a systematic therapeutic strategy and appropriate response to complications based on abundant clinical experiences would be necessary.
Footnotes
CONFLICTS OF INTEREST
No potential conflict of interest relevant to this article was reported.
AUTHOR CONTRIBUTIONS
Study design and concept: S.M.K., J.J.P. Performance of endoscopic procedure: J.J.P. Data collection and statistical analysis: all authors. Writing of manuscript: S.M.K., J.J.P., M.K.J. Advice for study design and writing of manuscript: B.J.L., J.J.P., S.W.L., H.J.C. Reading of article and final approval: all authors.
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