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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
| Yong Chan Lee |
Professor of Medicine Director, Gastrointestinal Research Laboratory Veterans Affairs Medical Center, Univ. California San Francisco San Francisco, USA |
| 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 |
All papers submitted to Gut and Liver are reviewed by the editorial team before being sent out for an external peer review to rule out papers that have low priority, insufficient originality, scientific flaws, or the absence of a message of importance to the readers of the Journal. A decision about these papers will usually be made within two or three weeks.
The remaining articles are usually sent to two reviewers. It would be very helpful if you could suggest a selection of reviewers and include their contact details. We may not always use the reviewers you recommend, but suggesting reviewers will make our reviewer database much richer; in the end, everyone will benefit. We reserve the right to return manuscripts in which no reviewers are suggested.
The final responsibility for the decision to accept or reject lies with the editors. In many cases, papers may be rejected despite favorable reviews because of editorial policy or a lack of space. The editor retains the right to determine publication priorities, the style of the paper, and to request, if necessary, that the material submitted be shortened for publication.
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Jue Lie Kim1 
, Sang Gyun Kim1 , Jung Kim2 , Jae Yong Park3 , Hyo-Joon Yang4 , Hyun Ju Kim5 , Hyunsoo Chung1
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
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 Liver 2020;14(2):190-198. https://doi.org/10.5009/gnl18575
Published online November 11, 2019, Published date March 15, 2020
Copyright © Gut and Liver.
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
Gut and Liver 2020; 14(2): 190-198
Published online March 15, 2020 https://doi.org/10.5009/gnl18575
Copyright © Gut and Liver.
Jue Lie Kim1 , Sang Gyun Kim1 , Jung Kim2 , Jae Yong Park3 , Hyo-Joon Yang4 , Hyun Ju Kim5 , 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
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.
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
Table 1 Baseline and Index Tumor Characteristics of the Re-ESD and Surgery Groups
| Baseline and index tumor characteristics | Overall (n=112) | Re-ESD (n=90) | Surgery (n=22) | p-value |
|---|---|---|---|---|
| Clinical characteristics | ||||
| Age, yr | 64.5±9.5 | 64.7±9.6 | 63.6±8.9 | 0.596 |
| Sex male | 91 (81.3) | 74 (82.2) | 17 (77.3) | 0.594 |
| BMI, kg/m2 | 24.5±2.7 | 24.7±2.7 | 23.3±2.4 | 0.025 |
| Pathologic characteristics at index cases | ||||
| Index | 0.242 | |||
| Positive | 58 (51.8) | 49 (54.4) | 9 (40.9) | |
| Negative | 44 (39.3) | 32 (35.6) | 12 (54.5) | |
| Atrophy* | 0.891 | |||
| Moderate to marked | 43 (38.4) | 35 (38.9) | 8 (36.4) | |
| Absent to mild | 46 (41.1) | 36 (40) | 10 (45.5) | |
| Intestinal metaplasia | 0.029 | |||
| Moderate to marked | 79 (70.5) | 67 (74.4) | 12 (54.5) | |
| Absent to mild | 23 (20.5) | 14 (15.6) | 9 (40.9) | |
| Gross type | 0.754 | |||
| Elevated | 44 (39.3) | 36 (40) | 8 (36.4) | |
| Non-elevated | 68 (60.7) | 54 (60) | 14 (63.6) | |
| Multiple cancer | 0.09 | |||
| One | 102 (91.1) | 84 (93.3) | 18 (81.8) | |
| Multiple (>1) | 10 (8.9) | 6 (6.7) | 4 (18.2) | |
| Lauren type | 0.054 | |||
| Intestinal | 106 (94.6) | 87 (96.7) | 19 (86.4) | |
| Diffuse or mixed | 6 (5.4) | 3 (3.3) | 3 (13.6) | |
| Differentiation type | 0.054 | |||
| Differentiated | 106 (94.6) | 87 (96.7) | 19 (86.4) | |
| Undifferentiated | 6 (5.4) | 3 (3.3) | 3 (13.6) | |
| Depth | 0.147 | |||
| T1m | 104 (92.8) | 83 (92.2) | 22 (100) | |
| T1sm | 8 (7.2) | 7 (7.7) | 0 | |
| Tumor location | 0.424 | |||
| Upper | 4 (3.6) | 4 (4.4) | 0 | |
| Middle | 27 (24.1) | 23 (25.6) | 4 (18.2) | |
| Lower | 81 (72.3) | 63 (70) | 18 (81.8) | |
| Tumor size, mm | 1.9±1.2 | 18.5±10.6 | 19.5±11.2 | 0.538 |
| Ulcer* | 0.527 | |||
| Yes | 3 (2.7) | 3 (3.3) | 0 | |
| No | 107 (95.5) | 85 (94.4) | 22 (100) | |
| Venous invasion | - | |||
| Yes | 0 | 0 | 0 | |
| No | 112 (100) | 90 (80.4) | 22 (19.6) | |
| Lymphatic invasion | 0.48 | |||
| Yes | 2 (1.8) | 2 (2.2) | 0 | |
| No | 110 (98.2) | 88 (97.8) | 22 (20) | |
| Vertical resection margin | 0.276 | |||
| Positive | 2 (1.8) | 1 (1.1) | 1 (4.5) | |
| Negative | 110 (98.2) | 89 (98.9) | 21 (95.5) | |
| Curative resection | 0.923 | |||
| Yes | 96 (85.7) | 77 (85.6) | 19 (86.4) | |
| No | 16 (14.3) | 13 (14.4) | 3 (13.6) | |
| Duration from index ESD to diagnosis of metachronous cancer, mo | 53.8±31.3 | 53.0±30.6 | 56.9±34.4 | 0.698 |
Data are presented as mean±SD or number (%).
ESD, endoscopic submucosal dissection; BMI, body mass index;
*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 characteristics | p-value | Exp (B) | 95% CI for Exp (B) |
|---|---|---|---|
| BMI | 0.037 | 0.744 | (0.563–0.983) |
| Male sex | 0.552 | ||
| Initial multiple cancer (yes) | 0.014 | 29.131 | (1.982–428.465) |
| Atrophy, index case (moderate to marked) | 0.133 | ||
| Intestinal metaplasia, index case (moderate to marked) | 0.226 | ||
| Index | 0.971 | ||
| Differentiation type (undifferentiated) | 0.751 |
ESD, endoscopic submucosal dissection; CI, confidence interval; BMI, body mass index;
Table 3 Treatment Outcomes of Re-ESD versus Surgery for MGC: Univariate analysis for the Pathological Features of Metachronous Cancer
| Pathologic characteristics | Overall (n=112) | Re-ESD (n=90) | Surgery (n=22) | p-value |
|---|---|---|---|---|
| Persistent | 0.047 | |||
| Negative or eradicated | 50 (44.6) | 38 (42.2) | 12 (54.5) | |
| Persistent | 40 (35.7) | 37 (41.1) | 3 (13.6) | |
| Unknown | 22 (19.6) | 15 (16.7) | 7 (31.8) | |
| Atrophy | 0.774 | |||
| Moderate to severe | 25 (22.5) | 22 (24.4) | 3 (13.6) | |
| Absent to mild | 40 (36) | 37 (41.2) | 4 (18.1) | |
| Intestinal metaplasia | 0.594 | |||
| Moderate to severe | 57 (51.3) | 51 (56.7) | 6 (27.3) | |
| Absent to mild | 20 (17.9) | 17 (18.9) | 3 (13.6) | |
| Gross type | 0.976 | |||
| Elevated | 10 (8.9) | 8 (8.9) | 2 (9.1) | |
| Non-elevated | 102 (91.1) | 82 (91.1) | 20 (90.9) | |
| Multiple cancer | 0.394 | |||
| One | 102 (91.1) | 83 (92.2) | 19 (86.4) | |
| Multiple (>1) | 10 (8.9) | 7 (7.8) | 3 (13.6) | |
| Lauren type* | <0.001 | |||
| Intestinal | 81 (85.4) | 72 (87.8) | 10 (50) | |
| Diffuse or mixed | 14 (14.6) | 4 (28.6) | 10 (50) | |
| Differentiation type | <0.001 | |||
| Differentiated | 96 (85.7) | 85 (94.4) | 11 (50) | |
| Undifferentiated | 16 (14.3) | 5 (5.6) | 11 (50) | |
| Depth | 0.001 | |||
| T1m | 88 (78.6) | 77 (85.6) | 14 (63.7) | |
| ≥T1sm | 24 (21.4) | 13 (14.4) | 8 (36.3) | |
| Tumor location | 0.038 | |||
| Upper | 8 (7.1) | 4 (4.4) | 4 (18.2) | |
| Middle or lower | 104 (92.9) | 86 (95.6) | 18 (81.8) | |
| Tumor size, mm | 19.7±1.3 | 18±1 | 26.8±2 | 0.012 |
| Ulcer† | <0.05 | |||
| Yes | 1 (0.9) | 1 (1.1) | 0 | |
| No | 92 (82.1) | 89 (98.9) | 10 (45.5) | |
| Venous invasion | 0.999 | |||
| Yes | 1 (0.9) | 0 | 1 (4.5) | |
| No | 111 (99.1) | 90 (100) | 21 (95.5) | |
| Lymphatic invasion | 0.129 | |||
| Yes | 7 (6.3) | 4 (4.4) | 3 (13.6) | |
| No | 105 (5.4) | 86 (95.6) | 19 (86.4) | |
| Lymph node metastasis | - | |||
| Positive | - | - | 5 (22.7) | |
| Negative | - | - | 17 (77.3) | |
| Vertical resection margin | 0.999 | |||
| Positive | 5 (4.5) | 5 (5.6) | 0 | |
| Negative | 104 (92.9) | 84 (93.3) | 20 (90.6) | |
| Unknown | 3 (2.7) | 1 (5.6) | 2 (9.1) | |
| Lateral resection margin | 0.37 | |||
| Positive | 11 (9.8) | 10 (11.1) | 1 (4.5) | |
| Negative | 101 (90.2) | 80 (88.9) | 21 (95.5) | |
Data are presented as number (%) or mean±SD.
ESD, endoscopic submucosal dissection; MGC, metachronous gastric cancer;
*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 characteristics | p-value | Exp (B) | 95% CI for Exp (B) |
|---|---|---|---|
| Persistent | 0.055 | 0.163 | (0.026–1.038) |
| Lauren type (non-intestinal type) | 0.009 | 11.176 | (1.842–67.792) |
| Differentiation (undifferentiated) | - | ||
| Depth of invasion (≥T1sm ) | 0.001 | 19.864 | (3.329–118.506) |
| Tumor location (middle or lower part of stomach) | 0.049 | 0.088 | (0.008–0.991) |
| Tumor size | 0.206 |
ESD, endoscopic submucosal dissection; MCG, metachronous gastric cancer; CI, confidence interval;
pISSN 1976-2283
eISSN 2005-1212
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
| Yong Chan Lee |
Professor of Medicine Director, Gastrointestinal Research Laboratory Veterans Affairs Medical Center, Univ. California San Francisco San Francisco, USA |
| 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 |
All papers submitted to Gut and Liver are reviewed by the editorial team before being sent out for an external peer review to rule out papers that have low priority, insufficient originality, scientific flaws, or the absence of a message of importance to the readers of the Journal. A decision about these papers will usually be made within two or three weeks.
The remaining articles are usually sent to two reviewers. It would be very helpful if you could suggest a selection of reviewers and include their contact details. We may not always use the reviewers you recommend, but suggesting reviewers will make our reviewer database much richer; in the end, everyone will benefit. We reserve the right to return manuscripts in which no reviewers are suggested.
The final responsibility for the decision to accept or reject lies with the editors. In many cases, papers may be rejected despite favorable reviews because of editorial policy or a lack of space. The editor retains the right to determine publication priorities, the style of the paper, and to request, if necessary, that the material submitted be shortened for publication.
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