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  • 1. Aims and Scope

    Gut and Liver is an international journal of gastroenterology, focusing on the gastrointestinal tract, liver, biliary tree, pancreas, motility, and neurogastroenterology. Gut atnd Liver delivers up-to-date, authoritative papers on both clinical and research-based topics in gastroenterology. The Journal publishes original articles, case reports, brief communications, letters to the editor and invited review articles in the field of gastroenterology. The Journal is operated by internationally renowned editorial boards and designed to provide a global opportunity to promote academic developments in the field of gastroenterology and hepatology. +MORE

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    Yong Chan Lee Professor of Medicine
    Director, Gastrointestinal Research Laboratory
    Veterans Affairs Medical Center, Univ. California San Francisco
    San Francisco, USA

    Deputy Editor

    Deputy Editor
    Jong Pil Im Seoul National University College of Medicine, Seoul, Korea
    Robert S. Bresalier University of Texas M. D. Anderson Cancer Center, Houston, USA
    Steven H. Itzkowitz Mount Sinai Medical Center, NY, USA
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Original Article

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Clinical Outcomes of Metachronous Gastric Cancer after Endoscopic Resection for Early Gastric Cancer

Jue Lie Kim1 , Sang Gyun Kim1 , Jung Kim2 , Jae Yong Park3 , Hyo-Joon Yang4 , Hyun Ju Kim5 , and Hyunsoo Chung1

1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, 2Division of Gastroenterology, Department of Internal Medicine, Armed Forces Capital Hospital, Seongnam, 3Division of Gastroenterology, Department of Internal Medicine, Chung-Ang University Hospital, 4Division of Gastroenterology, Department of Internal Medicine and Gastrointestinal Cancer Center, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, and 5Health Promotion Center, Seoul National University Hospital, Seoul, Korea

Correspondence to:Sang Gyun Kim
Division of Gastroenterology, Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, 101 Daehakno, Jongno-gu, Seoul 03080, Korea
Tel: +82-2-740-8112, Fax: +82-2-743-6701, E-mail: harley1333@hanmail.net

Received: December 27, 2018; Revised: February 13, 2019; Accepted: April 4, 2019

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Gut and Liver 2020; 14(2): 190-198

Published online March 15, 2020 https://doi.org/10.5009/gnl18575

Copyright © Gut and Liver.

Abstract

Background/Aims: Patients treated with endoscopic submucosal dissection (ESD) for early gastric cancer (EGC) are at risk of developing metachronous gastric cancer (MGC). The aim of this study was to evaluate the clinical outcomes of MGC after ESD for EGC between the re-ESD and surgery groups. Methods: In total, data from 1,510 patients who underwent ESD for EGC from January 2005 to May 2014 were retrospectively reviewed, and data from 112 patients with MGC were analyzed according to the type of treatment, namely, re-ESD and surgery. The clinicopathological factors affecting the subsequent treatment and outcomes of MGC were evaluated. Results: The median duration to the development of MGC was 47 months. In multivariate analysis, lower body mass index (BMI) (p=0.037) and multiplicity (p=0.014) of index cases were significantly associated with subsequent surgery for MGC. In cases of MGC, a diffuse or mixed-type Lauren classification (p=0.009), the depth of tumor mucosal invasion (p=0.001), and an upper stomach location (p=0.049) were associated with surgery. Overall survival was significantly shorter in the surgery group than in the re-ESD group after treatment for MGC (log-rank test, p=0.01). Conclusions: Lower BMI and multiplicity of index cancers were significantly associated with the surgical resection of MGC. Close follow-up is needed to minimize additional treatment for cases at high risk of advanced MGC after ESD for EGC.

Keywords: Early gastric cancer, Endoscopic submucosal dissection, Metachronous gastric cancer, Surgery, Survival rate


Article

Original Article

Gut and Liver 2020; 14(2): 190-198

Published online March 15, 2020 https://doi.org/10.5009/gnl18575

Copyright © Gut and Liver.

Clinical Outcomes of Metachronous Gastric Cancer after Endoscopic Resection for Early Gastric Cancer

Jue Lie Kim1 , Sang Gyun Kim1 , Jung Kim2 , Jae Yong Park3 , Hyo-Joon Yang4 , Hyun Ju Kim5 , and Hyunsoo Chung1

1Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, 2Division of Gastroenterology, Department of Internal Medicine, Armed Forces Capital Hospital, Seongnam, 3Division of Gastroenterology, Department of Internal Medicine, Chung-Ang University Hospital, 4Division of Gastroenterology, Department of Internal Medicine and Gastrointestinal Cancer Center, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, and 5Health Promotion Center, Seoul National University Hospital, Seoul, Korea

Correspondence to:Sang Gyun Kim
Division of Gastroenterology, Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, 101 Daehakno, Jongno-gu, Seoul 03080, Korea
Tel: +82-2-740-8112, Fax: +82-2-743-6701, E-mail: harley1333@hanmail.net

Received: December 27, 2018; Revised: February 13, 2019; Accepted: April 4, 2019

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background/Aims: Patients treated with endoscopic submucosal dissection (ESD) for early gastric cancer (EGC) are at risk of developing metachronous gastric cancer (MGC). The aim of this study was to evaluate the clinical outcomes of MGC after ESD for EGC between the re-ESD and surgery groups. Methods: In total, data from 1,510 patients who underwent ESD for EGC from January 2005 to May 2014 were retrospectively reviewed, and data from 112 patients with MGC were analyzed according to the type of treatment, namely, re-ESD and surgery. The clinicopathological factors affecting the subsequent treatment and outcomes of MGC were evaluated. Results: The median duration to the development of MGC was 47 months. In multivariate analysis, lower body mass index (BMI) (p=0.037) and multiplicity (p=0.014) of index cases were significantly associated with subsequent surgery for MGC. In cases of MGC, a diffuse or mixed-type Lauren classification (p=0.009), the depth of tumor mucosal invasion (p=0.001), and an upper stomach location (p=0.049) were associated with surgery. Overall survival was significantly shorter in the surgery group than in the re-ESD group after treatment for MGC (log-rank test, p=0.01). Conclusions: Lower BMI and multiplicity of index cancers were significantly associated with the surgical resection of MGC. Close follow-up is needed to minimize additional treatment for cases at high risk of advanced MGC after ESD for EGC.

Keywords: Early gastric cancer, Endoscopic submucosal dissection, Metachronous gastric cancer, Surgery, Survival rate

Fig 1.

Figure 1.Study flowchart showing patient enrollment.
ESD, endoscopic submucosal dissection; EGC, early gastric cancer.
Gut and Liver 2020; 14: 190-198https://doi.org/10.5009/gnl18575

Fig 2.

Figure 2.Cumulative incidence of metachronous gastric cancer (MGC) after endoscopic submucosal dissection (ESD). (A) Cumulative incidence of MGC after ESD and (B) cumulative incidence of MGC after ESD (curative resection versus noncurative resection).
Gut and Liver 2020; 14: 190-198https://doi.org/10.5009/gnl18575

Fig 3.

Figure 3.Overall survival after re-ESD or surgery for metachronous gastric cancer: re-ESD versus surgery groups.
ESD, endoscopic submucosal dissection.
Gut and Liver 2020; 14: 190-198https://doi.org/10.5009/gnl18575

Table 1 Baseline and Index Tumor Characteristics of the Re-ESD and Surgery Groups

Baseline and index tumor characteristicsOverall (n=112)Re-ESD (n=90)Surgery (n=22)p-value
Clinical characteristics
Age, yr64.5±9.564.7±9.663.6±8.90.596
Sex male91 (81.3)74 (82.2)17 (77.3)0.594
BMI, kg/m224.5±2.724.7±2.723.3±2.40.025
Pathologic characteristics at index cases
Index H. pylori infection0.242
Positive58 (51.8)49 (54.4)9 (40.9)
Negative44 (39.3)32 (35.6)12 (54.5)
Atrophy*0.891
Moderate to marked43 (38.4)35 (38.9)8 (36.4)
Absent to mild46 (41.1)36 (40)10 (45.5)
Intestinal metaplasia0.029
Moderate to marked79 (70.5)67 (74.4)12 (54.5)
Absent to mild23 (20.5)14 (15.6)9 (40.9)
Gross type0.754
Elevated44 (39.3)36 (40)8 (36.4)
Non-elevated68 (60.7)54 (60)14 (63.6)
Multiple cancer0.09
One102 (91.1)84 (93.3)18 (81.8)
Multiple (>1)10 (8.9)6 (6.7)4 (18.2)
Lauren type0.054
Intestinal106 (94.6)87 (96.7)19 (86.4)
Diffuse or mixed6 (5.4)3 (3.3)3 (13.6)
Differentiation type0.054
Differentiated106 (94.6)87 (96.7)19 (86.4)
Undifferentiated6 (5.4)3 (3.3)3 (13.6)
Depth0.147
T1m104 (92.8)83 (92.2)22 (100)
T1sm8 (7.2)7 (7.7)0
Tumor location0.424
Upper4 (3.6)4 (4.4)0
Middle27 (24.1)23 (25.6)4 (18.2)
Lower81 (72.3)63 (70)18 (81.8)
Tumor size, mm1.9±1.218.5±10.619.5±11.20.538
Ulcer*0.527
Yes3 (2.7)3 (3.3)0
No107 (95.5)85 (94.4)22 (100)
Venous invasion-
Yes000
No112 (100)90 (80.4)22 (19.6)
Lymphatic invasion0.48
Yes2 (1.8)2 (2.2)0
No110 (98.2)88 (97.8)22 (20)
Vertical resection margin0.276
Positive2 (1.8)1 (1.1)1 (4.5)
Negative110 (98.2)89 (98.9)21 (95.5)
Curative resection0.923
Yes96 (85.7)77 (85.6)19 (86.4)
No16 (14.3)13 (14.4)3 (13.6)
Duration from index ESD to diagnosis of metachronous cancer, mo53.8±31.353.0±30.656.9±34.40.698

Data are presented as mean±SD or number (%).

ESD, endoscopic submucosal dissection; BMI, body mass index; H. pylori, Helicobacter pylori; m, mucosal cancer; sm, submucosal cancer.

*Exception where pathologic evaluation is inapplicable or medical record is absent.


Table 2 Multivariate Analysis of the Baseline and Index Tumor Characteristics in the Re-ESD and Surgery Groups

Baseline and index tumor characteristicsp-valueExp (B)95% CI for Exp (B)
BMI0.0370.744(0.563–0.983)
Male sex0.552
Initial multiple cancer (yes)0.01429.131(1.982–428.465)
Atrophy, index case (moderate to marked)0.133
Intestinal metaplasia, index case (moderate to marked)0.226
Index H. pylori infection (positive)0.971
Differentiation type (undifferentiated)0.751

ESD, endoscopic submucosal dissection; CI, confidence interval; BMI, body mass index; H. pylori, Helicobacter pylori.


Table 3 Treatment Outcomes of Re-ESD versus Surgery for MGC: Univariate analysis for the Pathological Features of Metachronous Cancer

Pathologic characteristicsOverall (n=112)Re-ESD (n=90)Surgery (n=22)p-value
Persistent H. pylori infection0.047
Negative or eradicated50 (44.6)38 (42.2)12 (54.5)
Persistent40 (35.7)37 (41.1)3 (13.6)
Unknown22 (19.6)15 (16.7)7 (31.8)
Atrophy0.774
Moderate to severe25 (22.5)22 (24.4)3 (13.6)
Absent to mild40 (36)37 (41.2)4 (18.1)
Intestinal metaplasia0.594
Moderate to severe57 (51.3)51 (56.7)6 (27.3)
Absent to mild20 (17.9)17 (18.9)3 (13.6)
Gross type0.976
Elevated10 (8.9)8 (8.9)2 (9.1)
Non-elevated102 (91.1)82 (91.1)20 (90.9)
Multiple cancer0.394
One102 (91.1)83 (92.2)19 (86.4)
Multiple (>1)10 (8.9)7 (7.8)3 (13.6)
Lauren type*<0.001
Intestinal81 (85.4)72 (87.8)10 (50)
Diffuse or mixed14 (14.6)4 (28.6)10 (50)
Differentiation type<0.001
Differentiated96 (85.7)85 (94.4)11 (50)
Undifferentiated16 (14.3)5 (5.6)11 (50)
Depth0.001
T1m88 (78.6)77 (85.6)14 (63.7)
≥T1sm24 (21.4)13 (14.4)8 (36.3)
Tumor location0.038
Upper8 (7.1)4 (4.4)4 (18.2)
Middle or lower104 (92.9)86 (95.6)18 (81.8)
Tumor size, mm19.7±1.318±126.8±20.012
Ulcer†<0.05
Yes1 (0.9)1 (1.1)0
No92 (82.1)89 (98.9)10 (45.5)
Venous invasion0.999
Yes1 (0.9)01 (4.5)
No111 (99.1)90 (100)21 (95.5)
Lymphatic invasion0.129
Yes7 (6.3)4 (4.4)3 (13.6)
No105 (5.4)86 (95.6)19 (86.4)
Lymph node metastasis-
Positive--5 (22.7)
Negative--17 (77.3)
Vertical resection margin0.999
Positive5 (4.5)5 (5.6)0
Negative104 (92.9)84 (93.3)20 (90.6)
Unknown3 (2.7)1 (5.6)2 (9.1)
Lateral resection margin0.37
Positive11 (9.8)10 (11.1)1 (4.5)
Negative101 (90.2)80 (88.9)21 (95.5)

Data are presented as number (%) or mean±SD.

ESD, endoscopic submucosal dissection; MGC, metachronous gastric cancer; H. pylori, Helicobacter pylori.

*Exception where pathologic reports are unknown or indeterminate; Exception where pathologic evaluation is inapplicable or medical record is absent.


Table 4 Treatment Outcomes of Re-ESD versus Surgery for MGC: Multivariate Analysis for the Pathological Features of Metachronous Cancer

Pathological characteristicsp-valueExp (B)95% CI for Exp (B)
Persistent H. pylori infection0.0550.163(0.026–1.038)
Lauren type (non-intestinal type)0.00911.176(1.842–67.792)
Differentiation (undifferentiated)-
Depth of invasion (≥T1sm )0.00119.864(3.329–118.506)
Tumor location (middle or lower part of stomach)0.0490.088(0.008–0.991)
Tumor size0.206

ESD, endoscopic submucosal dissection; MCG, metachronous gastric cancer; CI, confidence interval; H. pylori, Helicobacter pylori; sm, submucosal cancer.


Gut and Liver

Vol.15 No.6
November, 2021

pISSN 1976-2283
eISSN 2005-1212

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