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Original Article Risk Factors and Clinical Outcomes of Non-Curative Resection in Patients with Early Gastric Cancer Treated with Endoscopic Submucosal Dissection: A Retrospective Multicenter Study in Korea
Si Hyung Lee1, Min Cheol Kim1, Seong Woo Jeon2,orcid, Kang Nyeong Lee3, Jong Jae Park4, Su Jin Hong5, Korean Society of Gastrointestinal Endoscopy Endoscopic Submucosal Dissection Research Group
Clinical Endoscopy 2020;53(2):196-205.
DOI: https://doi.org/10.5946/ce.2019.123
Published online: October 25, 2019

1Department of Internal Medicine, Yeungnam University College of Medicine, Daegu, Korea

2Department of Internal Medicine, School of Medicine, Kyungpook National University, Daegu, Korea

3Department of Internal Medicine, Hanyang University College of Medicine, Seoul, Korea

4Department of Internal Medicine, Korea University College of Medicine, Seoul, Korea

5Department of Internal Medicine, Soonchunhyang University College of Medicine, Bucheon, Korea

Correspondence: Seong Woo Jeon Department of Internal Medicine, School of Medicine, Kyungpook National University Chilgok Hospital, 807 Hoguk-ro, Buk-gu, Daegu 41404, Korea Tel: +82-53-200-3517, Fax: +82-53-200-2027, E-mail: swjeon@knu.ac.kr
• Received: June 22, 2019   • Revised: August 12, 2019   • Accepted: August 13, 2019

Copyright © 2020 Korean Society of Gastrointestinal Endoscopy

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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See letter "Non-Curative Resection: Should Clinicians Consider Providing Additional Surgery for All Patients? " in Volume 53 on page 109.
  • Background/Aims
    The purpose of this study was to investigate the risk factors and long-term clinical outcomes of non-curative resection (NCR) in a large-scale patient population.
  • Methods
    We retrospectively analyzed the clinical data of 3,094 patients who underwent endoscopic submucosal dissection (ESD) of early gastric cancer from March 2005 to March 2018 at 13 institutions in Korea. We analyzed the risk factors for NCR and the survival between patients with curative resection and those with NCR with no additional treatment.
  • Results
    The NCR rate was 21.4% (661/3,094). In multivariate regression analysis, the risk factors affecting NCR with ESD were old age, undifferentiated tumor, tumor location in the upper body, tumor size ≥2 cm, and presence of an ulcer. In Cox proportional hazard regression analysis, tumor size ≥2 cm, submucosal invasion, positive horizontal margin, and lymphovascular invasion were risk factors for local recurrence. In Kaplan-Meier analysis, there was no statistically significant difference in the overall survival between the two groups (log-rank p=0.788). However, disease-specific survival was significantly lower in the NCR group (log-rank p=0.038).
  • Conclusions
    Clinicians should be aware of the risk factors for NCR and local recurrence after ESD for early gastric cancer, and should consider providing additional treatment after NCR.
Gastric cancer is the fourth most common cancer and has the second highest cancer-related mortality rate worldwide [1,2]. Early detection and early treatment can significantly reduce mortality [3,4]. In Korea, with the increase in individual health examinations and the expansion of the national cancer screening program that provides upper gastrointestinal endoscopy every 2 years for people aged >40 years, the number of patients diagnosed with early gastric cancer (EGC) has increased [2,5]. Traditionally, surgical resection was the standard treatment for gastric cancer; however, in recent years, endoscopic resection has become widely used. At present, endoscopic submucosal dissection (ESD) is accepted as a standard treatment for gastric cancer in patients with a negligible risk of lymph node or distant metastasis [6-9].
Endoscopic resection of EGC is indicated on the basis of tumor differentiation, size, ulceration, and invasion depth, and its goal is “curative resection” (CR) [10]. In cases of non-curative resection (NCR), additional treatment is needed because of local recurrence and lymph node metastasis, for which the standard treatment is gastrectomy with lymphadenectomy [11-13]. However, for reasons such as an increased proportion of elderly patients owing to the increase in average life expectancy, concomitant diseases, poor general health, or a patient’s refusal to undergo surgery, patients with NCR may be treated with redo-ESD, argon plasma coagulation, or careful observation without further treatment [14-16].
Although several studies have reported the long-term clinical outcomes of NCR in patients with EGC treated with ESD, studies on large-scale populations are lacking [17-19]. The aims of this retrospective multicenter study were to investigate the risk factors associated with NCR and to assess the long-term clinical outcomes after NCR with no additional treatment in a large-scale patient population.
Study design
We performed a retrospective multicenter study at 13 Korean institutions by using ESD registry data collected under the supervision of the ESD research group of the Korean Society of Gastrointestinal Endoscopy. The study protocol adhered to the ethical principles of the Declaration of Helsinki and was approved by the institutional review board of each institution (2019-05-035).
Patients
We retrospectively analyzed the clinical data of 3,929 patients aged >20 years who underwent endoscopic resection of EGC from March 2005 to March 2018 at 13 institutions in Korea. We excluded patients who met any of the following exclusion criteria: (1) history of previous endoscopic resection (n=101), (2) history of previous abdominal surgery for stomach cancer (n=14), (3) EGC treated with endoscopic mucosal resection (n=237), (4) surgery performed immediately after ESD because of NCR or meeting the expanded criteria (n=115), or (5) loss to follow-up or <6 months of follow-up (n=368). A total of 3,094 patients were finally enrolled (Fig. 1).
Endoscopic submucosal dissection procedure
Among patients diagnosed with EGC by using standard endoscopy, ESD was performed in those who met the indications for endoscopic resection. All patients were sedated using midazolam and/or propofol with cardiopulmonary monitoring. The target lesion was identified and marking dots were placed circumferentially 2 mm outside the lesion to determine the ESD range. Thereafter, a submucosal solution, such as saline or sodium hyaluronate with epinephrine, was injected into the submucosal layer to lift it off the muscle layer and a circumferential mucosal incision was made outside the marking dots with an electrosurgical knife. The submucosal layer was then dissected with an IT-knife or an IT-knife2 while performing hemostasis on any oozing vessel or on vessels exposed both during and after the procedure.
Histopathological evaluation and curability
The endoscopically resected specimens were sectioned at 2-mm intervals and stained with hematoxylin and eosin after fixation in 10% formalin and embedding in paraffin for histopathological evaluation. At each institution, a pathologist evaluated the specimens for histopathological type, invasion depth, horizontal and vertical margins, ulcerations, and lymphovascular invasion according to the Japanese classification of gastric carcinoma [20]. Differentiated adenocarcinoma included tubular adenocarcinoma and papillary adenocarcinoma, whereas undifferentiated adenocarcinoma included poorly differentiated adenocarcinoma, signet ring cell carcinoma, and mucinous adenocarcinoma. Tumoral infiltration of the submucosa (SM) was subclassified as SM1 (<500 μm from the muscularis mucosa) or SM2 (≥500 μm from the muscularis mucosa).
According to the Japanese gastric cancer treatment guidelines, the indications for CR are as follows: en bloc resection, tumor size ≤2 cm, histologically differentiated type, pT1a, negative horizontal margin (HM0), negative vertical margin (VM0), and no lymphovascular invasion. In addition, a resection was considered curative for the expanded indications when all of the following conditions were fulfilled: en bloc resection, HM0, VM0, no lymphovascular invasion with (1) tumor size >2 cm, differentiated, pT1a, no ulcerative findings; (2) tumor size ≤3 cm, differentiated, pT1a, ulcerative findings; (3) tumor size ≤2 cm, undifferentiated, pT1a, no ulcerative findings; and (4) tumor size ≤3 cm, differentiated, pT1b (SM1). Any resection that did not satisfy any of the above criteria (expanded indications) was considered NCR.
Follow-up and clinical outcomes
After ESD, regular follow-up was performed at 3 months, 6 months, and every year thereafter. In this study, local recurrence was defined as a recurrence of the index cancer at the site of ESD. Synchronous cancer was defined as a development of new cancer at a site other than the ESD site within 1 year after ESD. Metachronous cancer was defined as the development of new cancer beyond 1 year after ESD. Overall survival (OS) was defined as the period from the initial ESD until death due to any cause or last patient contact. Disease-specific survival (DSS) was defined as the period from the initial ESD until gastric cancer-related death or last patient contact. Disease-free survival was defined as the period from the initial ESD to local or distant recurrence of the index cancer, or death or last patient contact.
Statistical analysis
Continuous and categorical variables were expressed as mean±standard deviation and n (%), respectively. Patient characteristics were analyzed for the status of NCR by using Student’s t-test for continuous variables and the chi-square test or Fisher’s exact test, as appropriate, for categorical variables. Logistic regression analysis was used to determine the risk factors for NCR. The odds ratio (OR) was considered to be statistically significant if the 95% confidence interval (CI) did not include 1.0. Cumulative local recurrence rate, OS, and DSS were calculated according to the Kaplan–Meier method and analyzed using the log-rank test. Cox proportional hazard regression analysis was used to calculate univariate and multivariate-adjusted hazard ratios and 95% CIs for risk factors for local recurrence in the follow-up. Statistical analysis was performed using SPSS version 25.0 (IBM, Armonk, NY, USA), and the level of statistical significance was set at p<0.05.
Baseline characteristics
Of the 3,094 patients with EGC treated with ESD, 661 patients (21.4%) were found to have undergone NCR. The baseline characteristics of the NCR group are shown in Table 1. No differences in age, family history, smoking history, or comorbidities were seen between the two groups; however, the proportion of male patients in the CR group was higher than that in the NCR group. Certain characteristics of EGC, including undifferentiated carcinoma, upper third location, large tumor, ulceration, and submucosal invasion, were more frequent in the NCR group. With respect to the procedure, the mean procedure time was longer and complications related to the procedure were more frequent in the NCR group. Table 2 shows the characteristics of the NCR group.
Independent risk factors for non-curative resection
Table 3 shows the risk factors for NCR after ESD in patients with EGC. In multivariate regression analysis after adjusting for confounding factors, the risk factors affecting NCR of ESD were old age (OR, 1.42; 95% CI, 1.17–1.74; p<0.001), undifferentiated tumor (OR, 9.47; 95% CI, 7.23–12.41; p<0.001), tumor location in the upper body (OR, 2.17; 95% CI, 1.55–3.05; p<0.001), tumor size ≥2 cm (OR, 3.81; 95% CI, 3.12–4.66; p<0.001), and presence of an ulcer (OR, 1.93; 95% CI, 1.47–2.53; p<0.001).
Local recurrence after non-curative resection
During the study, the local recurrence rate was significantly higher in the NCR group than in the CR group (10.6% vs. 2.5%, p<0.001) (Table 1). The cumulative local recurrence rate, calculated using Kaplan-Meier analysis, was significantly higher in the NCR group than in the CR group (Fig. 2). However, the cumulative recurrence rate at distant sites was not related to NCR (Fig. 3). Table 4 shows the risk factors affecting local recurrence. In Cox proportional hazard regression analysis, after adjusting for confounding factors, a tumor size of ≥2 cm (OR, 1.51; 95% CI, 1.05–2.17; p<0.028), submucosal invasion (SM1: OR, 1.84; 95% CI, 1.13–3.51; p=0.017 and ≥SM2: OR, 1.84; 95% CI, 1.05–3.21; p=0.033), positive horizontal margin (OR, 3.78; 95% CI, 2.38–6.00; p<0.001), and lymphovascular invasion (OR, 2.58; 95% CI, 1.33–5.01; p=0.005) were risk factors for local recurrence.
Overall survival rate and disease-specific survival rate after non-curative resection
A comparison by Kaplan-Meier analysis of the OS of the CR and NCR groups when patients received no additional surgery is shown in Fig. 4. The OS rates at 3, 5, and 10 years were 99.4%, 98.8%, and 97.1%, respectively, in the CR group and 99.4%, 98.9%, and 96.8%, respectively, in the NCR group. There was no statistically significant difference in OS between the two groups (log-rank p=0.788). Fig. 5. shows the Kaplan-Meier analysis of DSS between the two groups. The DSS rates at 3, 5, and 10 years were 100%, 99.9%, and 99.7%, respectively, in the CR group and 99.6%, 99.3%, and 99.3%, respectively, in the NCR group. DSS was significantly lower in the NCR group than in the CR group (log-rank p=0.038).
The aim of this retrospective multicenter study was to analyze the risk factors associated with NCR and the long-term clinical outcomes of NCR with no additional treatment in a large-scale population of patients.
According to several studies, the incidence of NCR after endoscopic resection of EGC is approximately 11.9%–18.5% [15,19,21-23]. In our study, the incidence of NCR was 21.4%, which was somewhat higher than that reported in other studies. In Korea, the number of ESD procedures is steadily increasing because of several factors, including an increase in the number of individual health examinations and the expansion of national cancer screening programs [5]. In addition, ESD is now more frequently performed with larger lesions since the introduction of the expanded criteria for ESD of EGC [13].
The aim of endoscopic resection of EGC is CR; however, unintended NCR may occur owing to various factors. Several previous studies have analyzed the risk factors associated with NCR in endoscopic resection of EGC. In a study of 784 patients who underwent ESD, the risk of NCR was the highest in patients with a tumor size of >3 cm, the presence of an ulcer, and a tumor located in the upper body [21]. In Korea, 1,639 patients with EGC who underwent ESD were retrospectively analyzed for risk factors associated with NCR. The seven factors found to be associated with NCR in that study were large tumor size (≥2 cm), tumor location in the upper body, presence of an ulcer, fusion of gastric folds, absence of mucosal nodularity, spontaneous bleeding, and undifferentiated tumor. The higher the score, the higher the risk of NCR [24]. In addition, a study reported that a tumor size of >2 cm, a superficial elevated and depressed type, and an undifferentiated type were risk factors for NCR [25]. In addition to the characteristics of the lesion at the time of the procedure, the effects of an operator’s endoscopic technique and the pre- and post-procedure discrepancies in NCR were analyzed in one study [22]. By combining the results of these previous studies, the risk factors associated with NCR in endoscopic resection of EGC were large tumor size, tumor location in the upper body, ulceration, undifferentiated tumor, indications falling outside of the absolute and expanded indications for endoscopic resection, improper endoscopic technique, and discrepancies in diagnosis before and after the treatment. These results were not significantly different in our study.
In our study, we analyzed the local recurrence rate and its associated risk factors after ESD. Local recurrence was observed in 10.6% of the ESD sites in the NCR group during the median follow-up period of approximately 50 months, and this rate was significantly higher than the local recurrence rate of 2.5% in the CR group. The risk factors affecting local recurrence in this study were tumor size ≥2 cm, submucosal invasion, positive horizontal margin, and lymphovascular invasion. Previous studies that analyzed the risk factors for local recurrence after endoscopic resection showed similar results. A study that analyzed 152 cases of NCR of EGC reported that there was a high risk of local recurrence in cases of incomplete resection, in cases that exceeded the ESD criteria, and in cases with lymphovascular invasion [26]. A study that analyzed 222 patients with EGC treated with ESD reported that a positive horizontal margin, piecemeal resection, and lymphovascular invasion were risk factors for local recurrence [27]. In two studies in patients with a positive horizontal margin after NCR of EGC, the risk of local recurrence was the highest in patients with a positive horizontal margin of >6 mm length [11,28].
In our study, there was no difference in the OS rate between the CR and NCR groups when patients received no additional treatment, but the DSS rate was significantly lower in the NCR group than in the CR group. This means that the OS rate is offset by the difference between the two groups due to various causes of death; however, given the specificity of survival in gastric cancer, the incidence of gastric cancer-related death in the NCR group was higher than that in the CR group. In other words, additional treatment should be considered for patients with NCR because the DSS rate may be lower without additional treatment in these patients. There are several studies that support our results. In a retrospective study of EGC cases that were outside the indications for endoscopic resection, 1,799 patients who underwent gastrectomy as the first treatment were compared with 219 patients who underwent endoscopic resection as the first treatment, There was no significant difference in mortality and gastric cancer recurrence rates between patients who initially underwent gastrectomy and patients who underwent gastrectomy after NCR; however, the mortality and gastric cancer recurrence rates were significantly higher in patients who did not undergo gastrectomy after NCR than in those who underwent gastrectomy as the first treatment [29].
Our study has some limitations. First, as it is a retrospective study, there may be some bias in patient selection. However, we believe that such a bias is compensated for by the largescale multicenter design. Second, this study included data on local recurrence in the post-ESD prognosis, but no data were collected on lymph node metastasis or distant metastasis after ESD. Third, in the survival analysis, the survival rate was analyzed only in patients with CR and in those who received no additional treatment after NCR. We believe that it is also necessary to analyze the survival rate in patients who received additional treatment, such as redo-ESD or gastrectomy after NCR.
In summary, the risk factors for NCR were older age, undifferentiated tumor, upper location of the tumor, tumor size >2 cm, and presence of an ulcer. The local recurrence rate was significantly higher in NCR, and the risk factors for local recurrence are tumor size >2 cm, submucosal invasion, horizontal margin positive, and lymphovascular invasion. In terms of survival, the DSS rate was significantly lower in NCR without further treatment than in CR. Therefore, if patients can tolerate surgical treatment, additional surgery is recommended in cases of NCR after ESD for EGC.
The authors thank Suck Chei Choi, Jun-Hyung Cho, Kwang Bum Cho, Jae Young Jang, Jae Myung Park, Jae Kyu Sung, Moon Kyung Joo, Jung Won Jeon, Weon Jin Ko, Sun Moon Kim, Yeong Dae Kim, Chan Gyoo Kim, Eun Ran Kim, Gwang Ho Baik, Dong Hoon Baek, Chul-Hyun Lim, and Hyun Joo Jang.
Fig. 1.
Flowchart of patient enrollment. EGCA, early gastric cancer; EMR, endoscopic mucosal resection; ESD, endoscopic submucosal dissection; Hx, history; NCR, non-curative resection.
ce-2019-123f1.jpg
Fig. 2.
Kaplan-Meier analysis for cumulative recurrence rates at previous endoscopic submucosal dissection site according to non-curative resection. Log-rank p<0.001.
ce-2019-123f2.jpg
Fig. 3.
Kaplan-Meier analysis for cumulative recurrence rates at other site according to non-curative resection. Log-rank p=0.585.
ce-2019-123f3.jpg
Fig. 4.
Kaplan-Meier analysis for cumulative overall survival rates according to non-curative resection. Log-rank p=0.788.
ce-2019-123f4.jpg
Fig. 5.
Kaplan-Meier analysis for cumulative disease-specific survival rates according to non-curative resection. Logrank p=0.038.
ce-2019-123f5.jpg
Table 1.
Baseline Characteristics
Curative resection (n=2,433) Non-curative resection (n=661) p-value
Age, yr 63.51±9.57 63.89±10.41 0.404
 ≥65 yr 1,253 (51.5%) 317 (48.0%) 0.106
Male 1,777 (73.0%) 443 (67.0%) 0.002
Family history of stomach cancer 156 (6.4%) 33 (5.0%) 0.177
Smoking history 0.629
 Non-smoker 1408 (57.9%) 396 (59.9%)
 Ex-smoker 546 (22.4%) 143 (21.5%)
 Current smoker 479 (19.7%) 122 (18.5%)
Co-morbidity disease
 Hypertension 945 (38.8%) 247 (37.4%) 0.490
 Diabetes mellitus 418 (17.2%) 116 (17.5%) 0.824
 Cardiovascular disease 145 (6.0%) 36 (5.4%) 0.618
 Cerebrovascular attack 112 (4.6%) 31 (4.7%) 0.925
 Liver cirrhosis 36 (1.5%) 15 (2.3%) 0.157
 Chronic kidney disease 17 (0.7%) 9 (1.4%) 0.098
Aspirin use 259 (10.6%) 78 (11.8%) 0.398
Pre-procedure diagnosis <0.001
 Adenoma or atypical cells 1,043 (42.9%) 135 (20.4%)
 Differentiated 1,302 (53.5%) 367 (55.5%)
 Undifferentiated 88 (3.6%) 159 (24.1%)
Post-procedure diagnosis
 Differentiated 2,325 (95.6%) 438 (66.3%) <0.001
 Undifferentiated 108 (4.4%) 223 (33.7%)
Tumor location, long axis <0.001
 Lower 1,636 (67.2%) 325 (49.2%)
 Middle 640 (26.3%) 261 (39.5%)
 Upper 157 (6.5%) 75 (11.3%)
Tumor location, short axis 0.295
 Lesser curvature 973 (40.0%) 254 (38.4%)
 Greater curvature 510 (21.0%) 139 (21.0%)
 Posterior wall 496 (20.4%) 156 (23.6%)
 Anterior wall 454 (18.7%) 112 (16.9%)
Gross type 0.001
 Elevated 1,134 (46.6%) 272 (41.1%)
 Flat 478 (19.6%) 172 (26.0%)
 Depressed 821 (33.7%) 217 (32.8%)
Tumor size, mm 14.56±9.89 23.13±14.12 <0.001
Ulceration 272 (11.2%) 119 (18.0%) <0.001
Depth of tumor <0.001
 Mucosal lesion 2,336 (96.0%) 394 (59.6%)
 Submucosal lesion 97 (4.0%) 262 (40.4%)
Procedure time, min 42.88±33.77 62.46±45.42 <0.001
En bloc resection 2,433 (100.0%) 552 (83.5%) <0.001
Complication
 Bleeding, during procedure 405 (16.6%) 140 (21.2%) 0.007
 Bleeding, after procedure 157 (6.5%) 51 (7.7%) 0.250
 Hypoxia 0 (0.0%) 2 (0.1%) 0.046
 Perforation 28 (1.2%) 18 (2.7%) 0.003
Helicobacter infection state <0.001
 Non-infected 814 (33.5%) 234 (35.4%)
 Infected, successfully eradication 808 (33.2%) 169 (25.6%)
 Infected, eradication, but failed 67 (2.8%) 7 (1.1%)
 Infected, no treatment 358 (14.7%) 116 (17.5%)
 Un-evaluated 386 (15.9%) 135 (20.4%)
Follow up period, mo 50.1±29.6 50.6±28.5 0.308
Local recurrence 61 (2.5%) 70 (10.6%) <0.001
Recurrence at other site 141 (5.8%) 35 (5.3%) 0.622
 Synchronous EGC (<1 yr) 68 (2.8%) 13 (2.0%) 0.237
 Metachronous EGC (≥1 yr) 73 (3.0%) 22 (3.3%) 0.665

EGC, early gastric cancer.

Table 2.
Characteristics of Non-Curative Resection
Non-curative resection (n=661)
Resection
En bloc resection 552 (83.5%)
 Piecemeal resection 109 (16.5%)
Tumor size ≥2 cm 335 (50.7%)
Depth of tumor
 M 394 (59.6%)
 SM1 74 (11.2%)
 ≥SM2 193 (29.2%)
Margin involvement
 Clear margin 437 (66.1%)
 Horizontal margin positive only 142 (21.5%)
 Vertical margin positive only 67 (10.1%)
 Both margin positive 15 (2.3%)
 Vertical margin positive + SM invasion 51 (7.7%)
Lymphovascular invasion 87 (13.2%)
Procedure time ≥60 min 259 (39.2%)

M, mucosa; SM, submucosa.

Table 3.
Risk Factors for Non-Curative Resection
Variables Univariate analysis
Multivariate analysis
OR (95% CI) p-value OR (95% CI) p-value
Age
 <65 yr 1 <0.001 1 <0.001
 ≥65 yr 1.44 (1.18–1.76) 1.42 (1.17–1.74)
Sex
 Male 1 0.983
 Female 1.00 (0.81–1.25)
Tumor histopathology
 Differentiated 1 <0.001 1 <0.001
 Undifferentiated 9.18 (6.96–12.11) 9.47 (7.23–12.41)
Tumor location
 Lower 1 1
 Middle 1.58 (1.28–1.95) <0.001 1.57 (1.27–1.94) <0.001
 Upper 2.14 (1.53–3.01) <0.001 2.17 (1.55–3.05) <0.001
Gross type
 Elevated 1
 Flat 1.19 (0.92–1.54) 0.187
 Depressed 1.14 (0.90–1.44) 0.277
Tumor size
 <2 cm 1 <0.001 1 <0.001
 ≥2 cm 3.88 (3.17–4.76) 3.81 (3.12–4.66)
Ulceration
 No 1 <0.001 1 <0.001
 Yes 1.89 (1.43–2.48) 1.93 (1.47–2.53)

CI, confidence interval; OR, odds ratio.

Table 4.
Risk Factors Affecting Local Recurrence at Previous Endoscopic Submucosal Dissection Site after Endoscopic Submucosal Dissection
Variables Univariate analysis
Multivariate analysis
HR (95% CI) p-value HR (95% CI) p-value
Age
 <65 yr 1 0.342
 ≥65 yr 1.19 (0.84–1.68)
Sex
 Male 1 0.067 1 0.105
 Female 0.67 (0.44–1.03) 0.71 (0.47–1.08)
Post-procedure diagnosis
 Differentiated 1 0.136
 Undifferentiated 1.45 (0.89–2.37)
Tumor location
 Lower 1
 Middle 1.15 (0.78–1.69) 0.482
 Upper 1.25 (0.69–2.26) 0.465
Tumor size
 <2 cm 1 0.071 1 0.028
 ≥2 cm 1.41 (0.97–2.04) 1.51 (1.05–2.17)
Depth of tumor
 M 1 1
 SM1 1.82 (1.01–3.27) 0.046 1.99 (1.13–3.51) 0.017
 ≥SM2 1.59 (0.86–2.93) 0.137 1.84 (1.05–3.21) 0.033
Horizontal margin positive
 No 1 <0.001 1 <0.001
 Yes 3.50 (2.17–5.64) 3.78 (2.38–6.00)
Vertical margin positive
 No 1 0.608
 Yes 1.22 (0.57–2.60)
Lymphovascular invasion
 No 1 0.005 1 0.005
 Yes 2.65 (1.35–5.21) 2.58 (1.33–5.01)
Helicobacter pylori infection state
 Noa) 1
 Yesb) 1.25 (0.80–1.93) 0.331
 Un-evaluated 1.17 (0.74–1.84) 0.510

CI, confidence interval; HR, hazard ratio; M, mucosa; SM, submucosa.

a)Non-infected and infected but successfully eradicated.

b)Infected but failed to eradicate and infected but not treated.

  • 1. Karimi P, Islami F, Anandasabapathy S, Freedman ND, Kamangar F. Gastric cancer: descriptive epidemiology, risk factors, screening, and prevention. Cancer Epidemiol Biomarkers Prev 2014;23:700–713.ArticlePubMedPMC
  • 2. Jung KW, Won YJ, Oh CM, Kong HJ, Lee DH, Lee KH. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2014. Cancer Res Treat 2017;49:292–305.ArticlePubMedPMCPDF
  • 3. Tsukuma H, Oshima A, Narahara H, Morii T. Natural history of early gastric cancer: a non-concurrent, long term, follow up study. Gut 2000;47:618–621.ArticlePubMedPMC
  • 4. Mun YG, Choi MG, Lim CH, et al. Factors affecting endoscopic curative resection of gastric cancer in the population-based screening era. Clin Endosc 2018;51:478–484.ArticlePubMedPMCPDF
  • 5. Kang KJ, Lee JH. Characteristics of gastric cancer in Korea - with an emphasis on the increase of the early gastric cancer (EGC). J Korean Med Assoc 2010;53:283–289.Article
  • 6. Kim YI, Kim YW, Choi IJ, et al. Long-term survival after endoscopic resection versus surgery in early gastric cancers. Endoscopy 2015;47:293–301.ArticlePubMedPDF
  • 7. Pyo JH, Lee H, Min BH, et al. Long-term outcome of endoscopic resection vs. surgery for early gastric cancer: a non-inferiority-matched cohort study. Am J Gastroenterol 2016;111:240–249.ArticlePubMedPDF
  • 8. Kim SG, Ji SM, Lee NR, et al. Quality of life after endoscopic submucosal dissection for early gastric cancer: a prospective multicenter cohort study. Gut Liver 2017;11:87–92.ArticlePubMedPMCPDF
  • 9. Kim JH. Strategy for curative endoscopic resection of undifferentiated-type early gastric cancer. Clin Endosc 2019;52:9–14.ArticlePubMedPMCPDF
  • 10. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer 2017;20:1–19.ArticlePubMedPMCPDF
  • 11. Sekiguchi M, Suzuki H, Oda I, et al. Risk of recurrent gastric cancer after endoscopic resection with a positive lateral margin. Endoscopy 2014;46:273–278.ArticlePubMedPDF
  • 12. Sekiguchi M, Suzuki H, Oda I, et al. Favorable long-term outcomes of endoscopic submucosal dissection for locally recurrent early gastric cancer after endoscopic resection. Endoscopy 2013;45:708–713.ArticlePubMedPDF
  • 13. Nonaka S, Oda I, Nakaya T, et al. Clinical impact of a strategy involving endoscopic submucosal dissection for early gastric cancer: determining the optimal pathway. Gastric Cancer 2011;14:56–62.ArticlePubMedPDF
  • 14. Bae SY, Jang TH, Min BH, et al. Early additional endoscopic submucosal dissection in patients with positive lateral resection margins after initial endoscopic submucosal dissection for early gastric cancer. Gastrointest Endosc 2012;75:432–436.ArticlePubMed
  • 15. Kim SG. Treatment strategy after incomplete endoscopic resection of early gastric cancer. Clin Endosc 2016;49:332–335.ArticlePubMedPMCPDF
  • 16. Lee SH, Park BS. Is radical surgery necessary for all patients diagnosed as having non-curative endoscopic submucosal dissection? Clin Endosc 2019;52:21–29.ArticlePubMedPMCPDF
  • 17. Ahn JY, Jung HY, Choi JY, et al. Natural course of noncurative endoscopic resection of differentiated early gastric cancer. Endoscopy 2012;44:1114–1120.ArticlePubMedPDF
  • 18. Kawata N, Kakushima N, Takizawa K, et al. Risk factors for lymph node metastasis and long-term outcomes of patients with early gastric cancer after non-curative endoscopic submucosal dissection. Surg Endosc 2017;31:1607–1616.ArticlePubMedPDF
  • 19. Hatta W, Gotoda T, Oyama T, et al. Is radical surgery necessary in all patients who do not meet the curative criteria for endoscopic submucosal dissection in early gastric cancer? A multi-center retrospective study in Japan. J Gastroenterol 2017;52:175–184.ArticlePubMedPDF
  • 20. Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 2011;14:101–112.ArticlePubMedPDF
  • 21. Hirasawa K, Kokawa A, Oka H, et al. Risk assessment chart for curability of early gastric cancer with endoscopic submucosal dissection. Gastrointest Endosc 2011;74:1268–1275.ArticlePubMed
  • 22. Toyokawa T, Inaba T, Omote S, et al. Risk factors for non-curative resection of early gastric neoplasms with endoscopic submucosal dissection: analysis of 1,123 lesions. Exp Ther Med 2015;9:1209–1214.ArticlePubMedPMC
  • 23. Suzuki H, Oda I, Abe S, et al. Clinical outcomes of early gastric cancer patients after noncurative endoscopic submucosal dissection in a large consecutive patient series. Gastric Cancer 2017;20:679–689.ArticlePubMedPDF
  • 24. Kim EH, Park JC, Song IJ, et al. Prediction model for non-curative resection of endoscopic submucosal dissection in patients with early gastric cancer. Gastrointest Endosc 2017;85:976–983.ArticlePubMed
  • 25. Ohara Y, Toshikuni N, Matsueda K, Mouri H, Yamamoto H. The superficial elevated and depressed lesion type is an independent factor associated with non-curative endoscopic submucosal dissection for early gastric cancer. Surg Endosc 2016;30:4880–4888.ArticlePubMedPDF
  • 26. Han JP, Hong SJ, Kim HK, et al. Risk stratification and management of non-curative resection after endoscopic submucosal dissection for early gastric cancer. Surg Endosc 2016;30:184–189.ArticlePubMedPDF
  • 27. Kim JH, Lee JH, Chung JW, et al. Risk factors for local recurrence of early gastric cancer after endoscopic submucosal dissection. Korean J Med 2013;85:285–293.ArticlePDF
  • 28. Kim TK, Kim GH, Park DY, et al. Risk factors for local recurrence in patients with positive lateral resection margins after endoscopic submucosal dissection for early gastric cancer. Surg Endosc 2015;29:2891–2898.ArticlePubMedPDF
  • 29. Eom BW, Kim YI, Kim KH, et al. Survival benefit of additional surgery after noncurative endoscopic resection in patients with early gastric cancer. Gastrointest Endosc 2017;85:155–163; e3.ArticlePubMed

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REFERENCES

    Citations

    Citations to this article as recorded by  
    • Management Strategy of Non-curative ESD in Gastric Cancer: Curative Criteria, and the Critical Building Block for Determining Beyond It
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      Journal of Physiology & Pathology in Korean Medicine.2023; 37(4): 81.     CrossRef
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      Journal of the Korean Medical Association.2022; 65(5): 276.     CrossRef
    • Therapeutic approach to non-curative resection after endoscopic treatment in early gastric cancer
      Eun Jeong Gong, Chang Seok Bang
      Journal of the Korean Medical Association.2022; 65(5): 284.     CrossRef
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      Dong Chan Joo, Gwang Ha Kim
      Journal of the Korean Medical Association.2022; 65(5): 267.     CrossRef
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      Seung Kim, Moon Joo, Ah-Young Yoo, Seong Kim, Won Kim, Beom Lee, Jong Park, Hoon Chun, Sang Lee
      Oncology Letters.2022;[Epub]     CrossRef
    • Clinico-pathologic determinants of non-e-curative outcome following en-bloc endoscopic submucosal dissection in patients with early gastric neoplasia
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      BMC Cancer.2021;[Epub]     CrossRef
    • Factors associated with overall survival in early gastric cancer patients who underwent additional surgery after endoscopic submucosal dissection
      Zhi Zheng, Fan-Di Bu, Hao Chen, Jie Yin, Rui Xu, Jun Cai, Jun Zhang, Hong-Wei Yao, Zhong-Tao Zhang
      World Journal of Clinical Cases.2021; 9(10): 2192.     CrossRef
    • Establishing Machine Learning Models to Predict Curative Resection in Early Gastric Cancer with Undifferentiated Histology: Development and Usability Study
      Chang Seok Bang, Ji Yong Ahn, Jie-Hyun Kim, Young-Il Kim, Il Ju Choi, Woon Geon Shin
      Journal of Medical Internet Research.2021; 23(4): e25053.     CrossRef
    • Population Attributable Fraction of Helicobacter pylori Infection–Related Gastric Cancer in Korea: A Meta-Analysis
      Yoon Park, Moran Ki
      Cancer Research and Treatment.2021; 53(3): 744.     CrossRef
    • Very low rate of residual neoplasia after non-curative endoscopic submucosal dissection: a western single-center experience
      João Santos-Antunes, Margarida Marques, Fátima Carneiro, Guilherme Macedo
      European Journal of Gastroenterology & Hepatology.2021; 33(9): 1161.     CrossRef
    • Editors' Choice of Noteworthy Clinical Endoscopy Publications in the First Decade
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      Clinical Endoscopy.2021; 54(5): 633.     CrossRef
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      Clinical Endoscopy.2020; 53(2): 109.     CrossRef
    • Protocol for expanded indications of endoscopic submucosal dissection for early gastric cancer in China: a multicenter, ambispective, observational, open-cohort study
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      Risk Factors and Clinical Outcomes of Non-Curative Resection in Patients with Early Gastric Cancer Treated with Endoscopic Submucosal Dissection: A Retrospective Multicenter Study in Korea
      Clin Endosc. 2020;53(2):196-205.   Published online October 25, 2019
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    Risk Factors and Clinical Outcomes of Non-Curative Resection in Patients with Early Gastric Cancer Treated with Endoscopic Submucosal Dissection: A Retrospective Multicenter Study in Korea
    Image Image Image Image Image
    Fig. 1. Flowchart of patient enrollment. EGCA, early gastric cancer; EMR, endoscopic mucosal resection; ESD, endoscopic submucosal dissection; Hx, history; NCR, non-curative resection.
    Fig. 2. Kaplan-Meier analysis for cumulative recurrence rates at previous endoscopic submucosal dissection site according to non-curative resection. Log-rank p<0.001.
    Fig. 3. Kaplan-Meier analysis for cumulative recurrence rates at other site according to non-curative resection. Log-rank p=0.585.
    Fig. 4. Kaplan-Meier analysis for cumulative overall survival rates according to non-curative resection. Log-rank p=0.788.
    Fig. 5. Kaplan-Meier analysis for cumulative disease-specific survival rates according to non-curative resection. Logrank p=0.038.
    Risk Factors and Clinical Outcomes of Non-Curative Resection in Patients with Early Gastric Cancer Treated with Endoscopic Submucosal Dissection: A Retrospective Multicenter Study in Korea
    Curative resection (n=2,433) Non-curative resection (n=661) p-value
    Age, yr 63.51±9.57 63.89±10.41 0.404
     ≥65 yr 1,253 (51.5%) 317 (48.0%) 0.106
    Male 1,777 (73.0%) 443 (67.0%) 0.002
    Family history of stomach cancer 156 (6.4%) 33 (5.0%) 0.177
    Smoking history 0.629
     Non-smoker 1408 (57.9%) 396 (59.9%)
     Ex-smoker 546 (22.4%) 143 (21.5%)
     Current smoker 479 (19.7%) 122 (18.5%)
    Co-morbidity disease
     Hypertension 945 (38.8%) 247 (37.4%) 0.490
     Diabetes mellitus 418 (17.2%) 116 (17.5%) 0.824
     Cardiovascular disease 145 (6.0%) 36 (5.4%) 0.618
     Cerebrovascular attack 112 (4.6%) 31 (4.7%) 0.925
     Liver cirrhosis 36 (1.5%) 15 (2.3%) 0.157
     Chronic kidney disease 17 (0.7%) 9 (1.4%) 0.098
    Aspirin use 259 (10.6%) 78 (11.8%) 0.398
    Pre-procedure diagnosis <0.001
     Adenoma or atypical cells 1,043 (42.9%) 135 (20.4%)
     Differentiated 1,302 (53.5%) 367 (55.5%)
     Undifferentiated 88 (3.6%) 159 (24.1%)
    Post-procedure diagnosis
     Differentiated 2,325 (95.6%) 438 (66.3%) <0.001
     Undifferentiated 108 (4.4%) 223 (33.7%)
    Tumor location, long axis <0.001
     Lower 1,636 (67.2%) 325 (49.2%)
     Middle 640 (26.3%) 261 (39.5%)
     Upper 157 (6.5%) 75 (11.3%)
    Tumor location, short axis 0.295
     Lesser curvature 973 (40.0%) 254 (38.4%)
     Greater curvature 510 (21.0%) 139 (21.0%)
     Posterior wall 496 (20.4%) 156 (23.6%)
     Anterior wall 454 (18.7%) 112 (16.9%)
    Gross type 0.001
     Elevated 1,134 (46.6%) 272 (41.1%)
     Flat 478 (19.6%) 172 (26.0%)
     Depressed 821 (33.7%) 217 (32.8%)
    Tumor size, mm 14.56±9.89 23.13±14.12 <0.001
    Ulceration 272 (11.2%) 119 (18.0%) <0.001
    Depth of tumor <0.001
     Mucosal lesion 2,336 (96.0%) 394 (59.6%)
     Submucosal lesion 97 (4.0%) 262 (40.4%)
    Procedure time, min 42.88±33.77 62.46±45.42 <0.001
    En bloc resection 2,433 (100.0%) 552 (83.5%) <0.001
    Complication
     Bleeding, during procedure 405 (16.6%) 140 (21.2%) 0.007
     Bleeding, after procedure 157 (6.5%) 51 (7.7%) 0.250
     Hypoxia 0 (0.0%) 2 (0.1%) 0.046
     Perforation 28 (1.2%) 18 (2.7%) 0.003
    Helicobacter infection state <0.001
     Non-infected 814 (33.5%) 234 (35.4%)
     Infected, successfully eradication 808 (33.2%) 169 (25.6%)
     Infected, eradication, but failed 67 (2.8%) 7 (1.1%)
     Infected, no treatment 358 (14.7%) 116 (17.5%)
     Un-evaluated 386 (15.9%) 135 (20.4%)
    Follow up period, mo 50.1±29.6 50.6±28.5 0.308
    Local recurrence 61 (2.5%) 70 (10.6%) <0.001
    Recurrence at other site 141 (5.8%) 35 (5.3%) 0.622
     Synchronous EGC (<1 yr) 68 (2.8%) 13 (2.0%) 0.237
     Metachronous EGC (≥1 yr) 73 (3.0%) 22 (3.3%) 0.665
    Non-curative resection (n=661)
    Resection
    En bloc resection 552 (83.5%)
     Piecemeal resection 109 (16.5%)
    Tumor size ≥2 cm 335 (50.7%)
    Depth of tumor
     M 394 (59.6%)
     SM1 74 (11.2%)
     ≥SM2 193 (29.2%)
    Margin involvement
     Clear margin 437 (66.1%)
     Horizontal margin positive only 142 (21.5%)
     Vertical margin positive only 67 (10.1%)
     Both margin positive 15 (2.3%)
     Vertical margin positive + SM invasion 51 (7.7%)
    Lymphovascular invasion 87 (13.2%)
    Procedure time ≥60 min 259 (39.2%)
    Variables Univariate analysis
    Multivariate analysis
    OR (95% CI) p-value OR (95% CI) p-value
    Age
     <65 yr 1 <0.001 1 <0.001
     ≥65 yr 1.44 (1.18–1.76) 1.42 (1.17–1.74)
    Sex
     Male 1 0.983
     Female 1.00 (0.81–1.25)
    Tumor histopathology
     Differentiated 1 <0.001 1 <0.001
     Undifferentiated 9.18 (6.96–12.11) 9.47 (7.23–12.41)
    Tumor location
     Lower 1 1
     Middle 1.58 (1.28–1.95) <0.001 1.57 (1.27–1.94) <0.001
     Upper 2.14 (1.53–3.01) <0.001 2.17 (1.55–3.05) <0.001
    Gross type
     Elevated 1
     Flat 1.19 (0.92–1.54) 0.187
     Depressed 1.14 (0.90–1.44) 0.277
    Tumor size
     <2 cm 1 <0.001 1 <0.001
     ≥2 cm 3.88 (3.17–4.76) 3.81 (3.12–4.66)
    Ulceration
     No 1 <0.001 1 <0.001
     Yes 1.89 (1.43–2.48) 1.93 (1.47–2.53)
    Variables Univariate analysis
    Multivariate analysis
    HR (95% CI) p-value HR (95% CI) p-value
    Age
     <65 yr 1 0.342
     ≥65 yr 1.19 (0.84–1.68)
    Sex
     Male 1 0.067 1 0.105
     Female 0.67 (0.44–1.03) 0.71 (0.47–1.08)
    Post-procedure diagnosis
     Differentiated 1 0.136
     Undifferentiated 1.45 (0.89–2.37)
    Tumor location
     Lower 1
     Middle 1.15 (0.78–1.69) 0.482
     Upper 1.25 (0.69–2.26) 0.465
    Tumor size
     <2 cm 1 0.071 1 0.028
     ≥2 cm 1.41 (0.97–2.04) 1.51 (1.05–2.17)
    Depth of tumor
     M 1 1
     SM1 1.82 (1.01–3.27) 0.046 1.99 (1.13–3.51) 0.017
     ≥SM2 1.59 (0.86–2.93) 0.137 1.84 (1.05–3.21) 0.033
    Horizontal margin positive
     No 1 <0.001 1 <0.001
     Yes 3.50 (2.17–5.64) 3.78 (2.38–6.00)
    Vertical margin positive
     No 1 0.608
     Yes 1.22 (0.57–2.60)
    Lymphovascular invasion
     No 1 0.005 1 0.005
     Yes 2.65 (1.35–5.21) 2.58 (1.33–5.01)
    Helicobacter pylori infection state
     Noa) 1
     Yesb) 1.25 (0.80–1.93) 0.331
     Un-evaluated 1.17 (0.74–1.84) 0.510
    Table 1. Baseline Characteristics

    EGC, early gastric cancer.

    Table 2. Characteristics of Non-Curative Resection

    M, mucosa; SM, submucosa.

    Table 3. Risk Factors for Non-Curative Resection

    CI, confidence interval; OR, odds ratio.

    Table 4. Risk Factors Affecting Local Recurrence at Previous Endoscopic Submucosal Dissection Site after Endoscopic Submucosal Dissection

    CI, confidence interval; HR, hazard ratio; M, mucosa; SM, submucosa.

    Non-infected and infected but successfully eradicated.

    Infected but failed to eradicate and infected but not treated.


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