KjG The Korean Journal of Gastroenterology Korean J Gastroenterol 1598-9992 2233-6869 Korean Society of Gastroenterology 10.4166/kjg.2017.70.3.128 kjg-70-128 Review Article Treatment Strategies after Noncurative Endoscopic Resection of Early Gastric Cancer KimShin Hee HongSu Jin Digestive Disease Center and Research Institute, Department of Internal Medicine, Soonchunhyang University College of Medicine, Bucheon, Korea Correspondence to: Su Jin Hong, Digestive Disease Center and Research Institute, Department of Internal Medicine, Soonchunhyang University College of Medicine, 170 Jomaru-ro, Wonmi-gu, Bucheon 14584, Korea. Tel: +82-32-621-5094, Fax: +82-32-621-5080, E-mail: sjhong@schmc.ac.kr 10 2017 04 10 2017 703 128 133 08082017 16092017 18092017 Copyright © 2017 Korean Ophthalmological Society 2017 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

The cases of non-curative endoscopic resection (NCR) of early gastric cancer have increased due to the widespread use of endoscopic submucosal dissection (ESD). NCR is associated with augmenting chances of local recurrence and lymph node metastasis (LNM). Therefore, some additional treatment strategies after NCR are needed. Treatment strategies for NCR should be determined by considering the risk of residual tumor or local recurrence and LNM. Additional surgical treatment such as gastrectomy and lymph node dissection are recommended in patients who have high-risk of LNM. Close observation without additional treatment is considered for selected patients with a less possibility of local recurrence or LNM. Also it may be suggested if there is no or less benefit from surgery in elderly patients or patients with underlying diseases. Additional endoscopic procedures including ESD, endoscopic mucosal resection or argon coagulation therapy are suggested alternatively for highly selected patients not at risk of LNM based on the absolute or expanded criteria of ESD.

 Gastric cancers Endoscopic submucosal dissection Residual tumors Lymphatic metastasis Therapeutics References Gotoda T Yanagisawa A Sasako M Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers Gastric Cancer 2000 3219225 Kim YI Kim YW Choi IJ Longterm survival after endoscopic resection versus surgery in early gastric cancers Endoscopy 2015 47293301 Pyo JH Lee H Min BH Longterm outcome of endoscopic resection vs. surgery for early gastric cancer: a non-inferiority- matched Cohort Study Am J Gastroenterol 2016 111240249 Japanese Gastric Cancer Association Japanese gastric cancer treatment guidelines 2014 (ver. 4) Gastric Cancer 2017 20119 Oda I Gotoda T Sasako M Treatment strategy after noncurative endoscopic resection of early gastric cancer Br J Surg 2008 9514951500 Ahn JY Jung HY Choi KD Endoscopic and oncologic outcomes after endoscopic resection for early gastric cancer:1370 cases of absolute and extended indications Gastrointest Endosc 2011 74485493 Kim ER Lee H Min BH Effect of rescue surgery after noncurative endoscopic resection of early gastric cancer Br J Surg 2015 10213941401 Toyokawa T Inaba T Omote S Risk factors for non-curative resection of early gastric neoplasms with endoscopic submucosal dissection: Analysis of 1,123 lesions Exp Ther Med 2015 912091214 Hirasawa K Kokawa A Oka H Risk assessment chart for curability of early gastric cancer with endoscopic submucosal dissection Gastrointest Endosc 2011 7412681275 Lee JH Min YW Lee JH Diagnostic group classifications of gastric neoplasms by endoscopic resection criteria before and after treatment: real-world experience Surg Endosc 2016 3039873993 Kang MS Hong SJ Kim DY Longterm outcome after endoscopic submucosal dissection for early gastric cancer: focusing on a group beyond the expanded indication J Dig Dis 2015 16713 Kim EH Park JC Song IJ Prediction model for non-curative resection of endoscopic submucosal dissection in patients with early gastric cancer Gastrointest Endosc 2017 85976983 Takenaka R Kawahara Y Okada H Risk factors associated with local recurrence of early gastric cancers after endoscopic submucosal dissection Gastrointest Endosc 2008 68887894 Jung H Bae JM Choi MG Noh JH Sohn TS Kim S Surgical outcome after incomplete endoscopic submucosal dissection of gastric cancer Br J Surg 2011 987378 Ryu KW Choi IJ Doh YW Surgical indication for non-curative endoscopic resection in early gastric cancer Ann Surg Oncol 2007 1434283434 Nagano H Ohyama S Fukunaga T Indications for gastrectomy after incomplete EMR for early gastric cancer Gastric Cancer 2005 8149154 Jang JS Choi SR Qureshi W Longterm outcomes of endoscopic submucosal dissection in gastric neoplastic lesions at a single institution in South Korea Scand J Gastroenterol 2009 4413151322 Han JP Hong SJ Choi MH Clinical outcomes of early gastric cancer with lateral margin positivity after endoscopic submucosal dissection Gastrointest Endosc 2013 78956961 Han JP Hong SJ Kim HK Risk stratification and management of non-curative resection after endoscopic submucosal dissection for early gastric cancer Surg Endosc 2016 30184189 Kim TK Kim GH Park DY Risk factors for local recurrence in patients with positive lateral resection margins after endoscopic submucosal dissection for early gastric cancer Surg Endosc 2015 2928912898 Yoon H Kim SG Choi J Risk factors of residual or recurrent tumor in patients with a tumor-positive resection margin after endoscopic resection of early gastric cancer Surg Endosc 2013 2715611568 Sekiguchi M Suzuki H Oda I Risk of recurrent gastric cancer after endoscopic resection with a positive lateral margin Endoscopy 2014 46273278 Kim HS Ahn JY Kim SO Kim BS Can further gastrectomy be avoided in patients with incomplete endoscopic resection? Surg Endosc 2017 Apr 19 [Epub ahead of print] Son SY Park JY Ryu KW The risk factors for lymph node metastasis in early gastric cancer patients who underwent endoscopic resection: is the minimal lymph node dissection appli-cable? A retrospective study Surg Endosc 2013 2732473253 Kawata N Kakushima N Takizawa K 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 3116071616 Park YD Chung YJ Chung HY Factors related to lymph node metastasis and the feasibility of endoscopic mucosal resection for treating poorly differentiated adenocarcinoma of the stomach Endoscopy 2008 40710 Chung JW Jung HY Choi KD Extended indication of endoscopic resection for mucosal early gastric cancer: analysis of a single center experience J Gastroenterol Hepatol 2011 26884887 Yoon HJ Kim YH Kim JH Are new criteria for mixed histology necessary for endoscopic resection in early gastric cancer? Pathol Res Pract 2016 212410414 Kang HJ Kim DH Jeon TY Lymph node metastasis from intestinal-type early gastric cancer: experience in a single institution and reassessment of the extended criteria for endoscopic submucosal dissection Gastrointest Endosc 2010 72508515 Kim HW Kim JH Park JC Additive endoscopic resection may be sufficient for patients with a positive lateral margin after endoscopic resection of early gastric cancer Gastrointest Endosc 2017 Mar 10 [Epub ahead of print] Toya Y Endo M Nakamura S Clinical outcomes of noncurative endoscopic submucosal dissection with negative resected margins for gastric cancer Gastrointest Endosc 2017 8512181224 Oka S Tanaka S Kaneko I Endoscopic submucosal dissection for residual/local recurrence of early gastric cancer after endoscopic mucosal resection Endoscopy 2006 389961000 Kusano C Iwasaki M Kaltenbach T Conlin A Oda I Gotoda T Should elderly patients undergo additional surgery after noncurative endoscopic resection for early gastric cancer? Longterm comparative outcomes Am J Gastroenterol 2011 10610641069 Eom BW Kim YI Kim KH Survival benefit of additional surgery after noncurative endoscopic resection in patients with early gastric cancer Gastrointest Endosc 2017 85155163.e3 Ahn JY Jung HY Choi JY Natural course of noncurative endoscopic resection of differentiated early gastric cancer Endoscopy 2012 4411141120 Hatta W Gotoda T Oyama T A scoring system to stratify curability after endoscopic submucosal dissection for early gastric cancer: “eCura system” Am J Gastroenterol 2017 112874881 Abe N Mori T Takeuchi H Laparoscopic lymph node dissection after endoscopic submucosal dissection: a novel and minimally invasive approach to treating early-stage gastric cancer Am J Surg 2005 190496503 Abe N Takeuchi H Ohki A Longterm outcomes of combination of endoscopic submucosal dissection and laparoscopic lymph node dissection without gastrectomy for early gastric cancer patients who have a potential risk of lymph node metastasis Gastrointest Endosc 2011 74792797 Goto O Takeuchi H Kitagawa Y Yahagi N Hybrid surgery for early gastric cancer Transl Gastroenterol Hepatol 2016 126 Jung DH Lee YC Kim JH Additive treatment improves survival in elderly patients after non-curative endoscopic resection for early gastric cancer Surg Endosc 2017 3113761382 Pyo JH Lee H Min BH Comparison of long-term outcomes after non-curative endoscopic resection in older patients with early gastric cancer Ann Surg Oncol 2017 2426242631 Figures and Tables

Algorithm for treatment strategies after non-curative resection of early gastric cancer (This figure was modified and created with reference to Japanese gastric cancer treatment guidelines 2014 [ver.4]).4 a It can be performed selectively for patients who want to preserve remnant stomach; b It can be performed selectively for patients who have difficulty in endoscopic resection or want to preserve remnant stomach. pT1a, tumor invades muscularis mucosa; pT1b (SM1), tumor invades submucosa, <500 µm from the muscularis mucosa; APC, argon plasma coagulation; EFTR, endoscopic full-thickness resection; LLND, laparoscopic lymph node dissection.

Definition of Curative Resection

Curative resection: fulfill all of the following conditions
En bloc resection tumor size ≤2 cm
Histologically of differentiated type
pT1a
HM0
VM0
Ly (−)
V (−)
Curative resection for tumors of expanded indication: fulfill all of the following conditions
   En bloc resection, HM0, VM0, Ly (−), V (−) and
   (a) Tumor size >2 cm, histologically of differentiated type, pT1a, ulcer (−)
   (b) Tumor size ≤3 cm, histologically of differentiated type, pT1a, ulcer (+)
   (c) Tumor size ≤2 cm, histologically of undifferentiated type, pT1a, ulcer (−)
   (d) Tumor size ≤3 cm, histologically of differentiated type, pT1b (SM1)

This table was modified with reference to Japanese gastric cancer treatment guidelines 2014 (ver. 4).4 pT1a, Tumor invades muscularis mucosa; pT1b (SM1), Tumor invades submucosa, <500 µm from the muscularis mucosa; HM0, Negative horizontal margin; VM0, Negative vertical margin; Ly, Lymphatic infiltration; V, Vascular infiltration.