Intest Res.  2021 Apr;19(2):127-157. 10.5217/ir.2020.00020.

Clinical practice guideline for endoscopic resection of early gastrointestinal cancer

• Park CH
• Yang DH
• Kim JW
• Kim JH
• Kim JH
• Min YW
• Lee SH
• Bae JH
• Chung H
• Choi KD
• Park JC
• Lee H
• Kwak MS
• Kim B
• Lee HJ
• Lee HS
• Choi M
• Park DA
• Lee JY
• Byeon JS
• Park CG
• Cho JY
• Lee ST
• Chun HJ

• KMID: 2515474
• DOI: http://doi.org/10.5217/ir.2020.00020

Abstract

Although surgery was the standard treatment for early gastrointestinal cancers, endoscopic resection is now a standard treatment for early gastrointestinal cancers without regional lymph node metastasis. High-definition white light endoscopy, chromoendoscopy, and image-enhanced endoscopy such as narrow band imaging are performed to assess the edge and depth of early gastrointestinal cancers for delineation of resection boundaries and prediction of the possibility of lymph node metastasis before the decision of endoscopic resection. Endoscopic mucosal resection and/or endoscopic submucosal dissection can be performed to remove early gastrointestinal cancers completely by en bloc fashion. Histopathological evaluation should be carefully made to investigate the presence of risk factors for lymph node metastasis such as depth of cancer invasion and lymphovascular invasion. Additional treatment such as radical surgery with regional lymphadenectomy should be considered if the endoscopically resected specimen shows risk factors for lymph node metastasis. This is the first Korean clinical practice guideline for endoscopic resection of early gastrointestinal cancer. This guideline was developed by using mainly de novo methods and encompasses endoscopic management of superficial esophageal squamous cell carcinoma, early gastric cancer, and early colorectal cancer. This guideline will be revised as new data on early gastrointestinal cancer are collected.

Keyword

Superficial esophageal squamous cell carcinoma; Early gastric cancer; Early colorectal cancer; Endoscopic resection; Guideline

Reference

1. Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T, et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy. 2015; 47:829–854.

2. Eom BW, Jung KW, Won YJ, Yang H, Kim YW. Trends in gastric cancer incidence according to the clinicopathological characteristics in Korea, 1999-2014. Cancer Res Treat. 2018; 50:1343–1350.

3. Kim SG, Lyu DH, Park CM, et al. Current status of endoscopic submucosal dissection for early gastric cancer in Korea: role and benefits. Korean J Intern Med. 2019; 34:785–793.

4. Miyamoto S, Muto M, Hamamoto Y, et al. A new technique for endoscopic mucosal resection with an insulated-tip electrosurgical knife improves the completeness of resection of intramucosal gastric neoplasms. Gastrointest Endosc. 2002; 55:576–581.

5. Bok GH, Cho JY. ESD Hands-on course using ex vivo and in vivo models in South Korea. Clin Endosc. 2012; 45:358–361.

6. Park CH, Lee H, Kim DW, et al. Clinical safety of endoscopic submucosal dissection compared with surgery in elderly patients with early gastric cancer: a propensity-matched analysis. Gastrointest Endosc. 2014; 80:599–609.

7. Japanese Gastric Cancer A. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer. 2017; 20:1–19.

8. Bosch SL, Teerenstra S, de Wilt JH, Cunningham C, Nagtegaal ID. Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions. Endoscopy. 2013; 45:827–834.

9. Kim TJ, Kim ER, Hong SN, Kim YH, Chang DK. Current practices in endoscopic submucosal dissection for colorectal neoplasms: a survey of indications among Korean endoscopists. Intest Res. 2017; 15:228–235.

10. Ebi M, Shimura T, Yamada T, et al. Multicenter, prospective trial of white-light imaging alone versus white-light imaging followed by magnifying endoscopy with narrow-band imaging for the real-time imaging and diagnosis of invasion depth in superficial esophageal squamous cell carcinoma. Gastrointest Endosc. 2015; 81:1355–1361.

11. Ishihara R, Matsuura N, Hanaoka N, et al. Endoscopic imaging modalities for diagnosing invasion depth of superficial esophageal squamous cell carcinoma: a systematic review and meta-analysis. BMC Gastroenterol. 2017; 17:24.

12. Nagahama T, Yao K, Maki S, et al. Usefulness of magnifying endoscopy with narrow-band imaging for determining the horizontal extent of early gastric cancer when there is an unclear margin by chromoendoscopy (with video). Gastrointest Endosc. 2011; 74:1259–1267.

13. Kato M, Kaise M, Yonezawa J, et al. Magnifying endoscopy with narrow-band imaging achieves superior accuracy in the differential diagnosis of superficial gastric lesions identified with white-light endoscopy: a prospective study. Gastrointest Endosc. 2010; 72:523–529.

14. Mocellin S, Marchet A, Nitti D. EUS for the staging of gastric cancer: a meta-analysis. Gastrointest Endosc. 2011; 73:1122–1134.

15. Backes Y, Moss A, Reitsma JB, Siersema PD, Moons LM. Narrow band imaging, magnifying chromoendoscopy, and gross morphological features for the optical diagnosis of t1 colorectal cancer and deep submucosal invasion: a systematic review and meta-analysis. Am J Gastroenterol. 2017; 112:54–64.

16. Ajani JA, D’Amico TA, Bentrem DJ, et al. Esophageal and esophagogastric junction cancers, Version 2.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2019; 17:855–883.

17. Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: part I. Esophagus. 2017; 14:1–36.

18. Sterne JAC, Savović J, Page MJ, et al. RoB 2: a revised tool for assessing risk of bias in randomised trials. Bmj. 2019; 366–l4898.

19. Higgins JPT, Green S. Cochrane handbook for systematic reviews of interventions, version 5.1.0 [Internet]. c2011 [cited 2019 Jul 26]. https://handbook-5-1.cochrane.org/.

20. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010; 25:603–605.

21. Whiting PF, Rutjes AW, Westwood ME, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011; 155:529–536.

22. Guyatt GH, Oxman AD, Kunz R, et al. Incorporating considerations of resources use into grading recommendations. BMJ. 2008; 336:1170–1173.

23. Ajani JA, D’Amico TA, Almhanna K, et al. Esophageal and esophagogastric junction cancers, version 1.2015. J Natl Compr Canc Netw. 2015; 13:194–227.

24. Endoscopic Classification Review Group. Update on the Paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy. 2005; 37:570–578.

25. Lee WC, Lee TH, Jang JY, et al. Staging accuracy of endoscopic ultrasound performed by nonexpert endosonographers in patients with resectable esophageal squamous cell carcinoma: is it possible? Dis Esophagus. 2015; 28:574–578.

26. Thosani N, Singh H, Kapadia A, et al. Diagnostic accuracy of EUS in differentiating mucosal versus submucosal invasion of superficial esophageal cancers: a systematic review and meta-analysis. Gastrointest Endosc. 2012; 75:242–253.

27. Dhupar R, Rice RD, Correa AM, et al. Endoscopic ultrasound estimates for tumor depth at the gastroesophageal junction are inaccurate: implications for the liberal use of endoscopic resection. Ann Thorac Surg. 2015; 100:1812–1816.

28. Oyama T, Inoue H, Arima M, et al. Prediction of the invasion depth of superficial squamous cell carcinoma based on microvessel morphology: magnifying endoscopic classification of the Japan Esophageal Society. Esophagus. 2017; 14:105–112.

29. Ra J, Paulson EC, Kucharczuk J, et al. Postoperative mortality after esophagectomy for cancer: development of a preoperative risk prediction model. Ann Surg Oncol. 2008; 15:1577–1584.

30. Chang AC, Ji H, Birkmeyer NJ, Orringer MB, Birkmeyer JD. Outcomes after transhiatal and transthoracic esophagectomy for cancer. Ann Thorac Surg. 2008; 85:424–429.

31. Connors RC, Reuben BC, Neumayer LA, Bull DA. Comparing outcomes after transthoracic and transhiatal esophagectomy: a 5-year prospective cohort of 17,395 patients. J Am Coll Surg. 2007; 205:735–740.

32. Min YW, Lee H, Song BG, et al. Comparison of endoscopic submucosal dissection and surgery for superficial esophageal squamous cell carcinoma: a propensity score-matched analysis. Gastrointest Endosc. 2018; 88:624–633.

33. Zhang Y, Ding H, Chen T, et al. Outcomes of endoscopic submucosal dissection vs esophagectomy for T1 esophageal squamous cell carcinoma in a real-world cohort. Clin Gastroenterol Hepatol. 2019; 17:73–81.

34. Shimizu Y, Omori T, Yokoyama A, et al. Endoscopic diagnosis of early squamous neoplasia of the esophagus with iodine staining: high-grade intra-epithelial neoplasia turns pink within a few minutes. J Gastroenterol Hepatol. 2008; 23:546–550.

35. Ishihara R, Kanzaki H, Iishi H, et al. Pink-color sign in esophageal squamous neoplasia, and speculation regarding the underlying mechanism. World J Gastroenterol. 2013; 19:4300–4308.

36. Uedo N, Fujishiro M, Goda K, et al. Role of narrow band imaging for diagnosis of early-stage esophagogastric cancer: current consensus of experienced endoscopists in Asia-Pacific region. Dig Endosc. 2011; 23 Suppl 1:58–71.

37. Gai W, Jin XF, Du R, Li L, Chai TH. Efficacy of narrow-band imaging in detecting early esophageal cancer and risk factors for its occurrence. Indian J Gastroenterol. 2018; 37:79–85.

38. Goda K, Dobashi A, Yoshimura N, et al. Narrow-band imaging magnifying endoscopy versus lugol chromoendoscopy with pink-color sign assessment in the diagnosis of superficial esophageal squamous neoplasms: a randomised noninferiority trial. Gastroenterol Res Pract. 2015; 2015:639462.

39. Rice TW, Patil DT, Blackstone EH. 8th edition AJCC/UICC staging of cancers of the esophagus and esophagogastric junction: application to clinical practice. Ann Cardiothorac Surg. 2017; 6:119–130.

40. Puli SR, Reddy JB, Bechtold ML, Antillon D, Ibdah JA, Antillon MR. Staging accuracy of esophageal cancer by endoscopic ultrasound: a meta-analysis and systematic review. World J Gastroenterol. 2008; 14:1479–1490.

41. Goda K, Tajiri H, Ikegami M, et al. Magnifying endoscopy with narrow band imaging for predicting the invasion depth of superficial esophageal squamous cell carcinoma. Dis Esophagus. 2009; 22:453–460.

42. Katada C, Tanabe S, Wada T, et al. Retrospective assessment of the diagnostic accuracy of the depth of invasion by narrow band imaging magnifying endoscopy in patients with superficial esophageal squamous cell carcinoma. J Gastrointest Cancer. 2019; 50:292–297.

43. Ishihara R, Iishi H, Uedo N, et al. Comparison of EMR and endoscopic submucosal dissection for en bloc resection of early esophageal cancers in Japan. Gastrointest Endosc. 2008; 68:1066–1072.

44. Takahashi H, Arimura Y, Masao H, et al. Endoscopic submucosal dissection is superior to conventional endoscopic resection as a curative treatment for early squamous cell carcinoma of the esophagus (with video). Gastrointest Endosc. 2010; 72:255–264.

45. Teoh AY, Chiu PW, Yu Ngo DK, Wong SK, Lau JY, Ng EK. Outcomes of endoscopic submucosal dissection versus endoscopic mucosal resection in management of superficial squamous esophageal neoplasms outside Japan. J Clin Gastroenterol. 2010; 44:e190–e194.

46. Urabe Y, Hiyama T, Tanaka S, Yoshihara M, Arihiro K, Chayama K. Advantages of endoscopic submucosal dissection versus endoscopic oblique aspiration mucosectomy for superficial esophageal tumors. J Gastroenterol Hepatol. 2011; 26:275–280.

47. Yamashita T, Zeniya A, Ishii H, et al. Endoscopic mucosal resection using a cap-fitted panendoscope and endoscopic submucosal dissection as optimal endoscopic procedures for superficial esophageal carcinoma. Surg Endosc. 2011; 25:2541–2546.

48. Guo HM, Zhang XQ, Chen M, Huang SL, Zou XP. Endoscopic submucosal dissection vs endoscopic mucosal resection for superficial esophageal cancer. World J Gastroenterol. 2014; 20:5540–5547.

49. Cao Y, Liao C, Tan A, Gao Y, Mo Z, Gao F. Meta-analysis of endoscopic submucosal dissection versus endoscopic mucosal resection for tumors of the gastrointestinal tract. Endoscopy. 2009; 41:751–757.

50. Ono S, Fujishiro M, Niimi K, et al. Predictors of postoperative stricture after esophageal endoscopic submucosal dissection for superficial squamous cell neoplasms. Endoscopy. 2009; 41:661–665.

51. Hashimoto S, Kobayashi M, Takeuchi M, Sato Y, Narisawa R, Aoyagi Y. The efficacy of endoscopic triamcinolone injection for the prevention of esophageal stricture after endoscopic submucosal dissection. Gastrointest Endosc. 2011; 74:1389–1393.

52. Hanaoka N, Ishihara R, Takeuchi Y, et al. Intralesional steroid injection to prevent stricture after endoscopic submucosal dissection for esophageal cancer: a controlled prospective study. Endoscopy. 2012; 44:1007–1011.

53. Takahashi H, Arimura Y, Okahara S, et al. A randomized controlled trial of endoscopic steroid injection for prophylaxis of esophageal stenoses after extensive endoscopic submucosal dissection. BMC Gastroenterol. 2015; 15:1.

54. Kataoka M, Anzai S, Shirasaki T, et al. Efficacy of short period, low dose oral prednisolone for the prevention of stricture after circumferential endoscopic submucosal dissection (ESD) for esophageal cancer. Endosc Int Open. 2015; 3:E113–E117.

55. Zhou G, Yuan F, Cai J, et al. Efficacy of prednisone for prevention of esophageal stricture after endoscopic submucosal dissection for superficial esophageal squamous cell carcinoma. Thorac Cancer. 2017; 8:489–494.

56. Yamaguchi N, Isomoto H, Nakayama T, et al. Usefulness of oral prednisolone in the treatment of esophageal stricture after endoscopic submucosal dissection for superficial esophageal squamous cell carcinoma. Gastrointest Endosc. 2011; 73:1115–1121.

57. Sato H, Inoue H, Kobayashi Y, et al. Control of severe strictures after circumferential endoscopic submucosal dissection for esophageal carcinoma: oral steroid therapy with balloon dilation or balloon dilation alone. Gastrointest Endosc. 2013; 78:250–257.

58. Nagami Y, Shiba M, Tominaga K, et al. Locoregional steroid injection prevents stricture formation after endoscopic submucosal dissection for esophageal cancer: a propensity score matching analysis. Surg Endosc. 2016; 30:1441–1449.

59. Eguchi T, Nakanishi Y, Shimoda T, et al. Histopathological criteria for additional treatment after endoscopic mucosal resection for esophageal cancer: analysis of 464 surgically resected cases. Mod Pathol. 2006; 19:475–480.

60. Akutsu Y, Uesato M, Shuto K, et al. The overall prevalence of metastasis in T1 esophageal squamous cell carcinoma: a retrospective analysis of 295 patients. Ann Surg. 2013; 257:1032–1038.

61. Choi JY, Park YS, Jung HY, et al. Feasibility of endoscopic resection in superficial esophageal squamous carcinoma. Gastrointest Endosc. 2011; 73:881–889.

62. Tachibana M, Yoshimura H, Kinugasa S, et al. Clinicopathological features of superficial squamous cell carcinoma of the esophagus. Am J Surg. 1997; 174:49–53.

63. Endo M, Yoshino K, Kawano T, Nagai K, Inoue H. Clinicopathologic analysis of lymph node metastasis in surgically resected superficial cancer of the thoracic esophagus. Dis Esophagus. 2000; 13:125–129.

64. Araki K, Ohno S, Egashira A, Saeki H, Kawaguchi H, Sugimachi K. Pathologic features of superficial esophageal squamous cell carcinoma with lymph node and distal metastasis. Cancer. 2002; 94:570–575.

65. Bollschweiler E, Baldus SE, Schroder W, et al. High rate of lymph-node metastasis in submucosal esophageal squamous-cell carcinomas and adenocarcinomas. Endoscopy. 2006; 38:149–156.

66. Kim DU, Lee JH, Min BH, et al. Risk factors of lymph node metastasis in T1 esophageal squamous cell carcinoma. J Gastroenterol Hepatol. 2008; 23:619–625.

67. Moriya H, Ohbu M, Kobayashi N, et al. Lymphatic tumor emboli detected by D2-40 immunostaining can more accurately predict lymph-node metastasis. World J Surg. 2011; 35:2031–2037.

68. Yamashina T, Ishihara R, Nagai K, et al. Long-term outcome and metastatic risk after endoscopic resection of superficial esophageal squamous cell carcinoma. Am J Gastroenterol. 2013; 108:544–551.

69. Oyama T, Tomori A, Hotta K, et al. Endoscopic submucosal dissection of early esophageal cancer. Clin Gastroenterol Hepatol. 2005; 3:S67–S70.

70. Katada C, Muto M, Momma K, et al. Clinical outcome after endoscopic mucosal resection for esophageal squamous cell carcinoma invading the muscularis mucosae: a multicenter retrospective cohort study. Endoscopy. 2007; 39:779–783.

71. Park HC, Kim DH, Gong EJ, et al. Ten-year experience of esophageal endoscopic submucosal dissection of superficial esophageal neoplasms in a single center. Korean J Intern Med. 2016; 31:1064–1072.

72. Song BG, Min YW, Cha RR, et al. Endoscopic submucosal dissection under general anesthesia for superficial esophageal squamous cell carcinoma is associated with better clinical outcomes. BMC Gastroenterol. 2018; 18:80.

73. Motoori M, Yano M, Ishihara R, et al. Comparison between radical esophagectomy and definitive chemoradiotherapy in patients with clinical T1bN0M0 esophageal cancer. Ann Surg Oncol. 2012; 19:2135–2141.

74. Kawaguchi G, Sasamoto R, Abe E, et al. The effectiveness of endoscopic submucosal dissection followed by chemoradiotherapy for superficial esophageal cancer. Radiat Oncol. 2015; 10:31.

75. Ikeda A, Hoshi N, Yoshizaki T, et al. Endoscopic submucosal dissection (ESD) with additional therapy for superficial esophageal cancer with submucosal invasion. Intern Med. 2015; 54:2803–2813.

76. Hamada K, Ishihara R, Yamasaki Y, et al. Efficacy and safety of endoscopic resection followed by chemoradiotherapy for superficial esophageal squamous cell carcinoma: a retrospective study. Clin Transl Gastroenterol. 2017; 8:e110.

77. Kurokawa Y, Muto M, Minashi K, Boku N, Fukuda H; Gastrointestinal Oncology Study Group of Japan Clinical Oncology G. A phase II trial of combined treatment of endoscopic mucosal resection and chemoradiotherapy for clinical stage I esophageal carcinoma: Japan Clinical Oncology Group Study JCOG0508. Jpn J Clin Oncol. 2009; 39:686–689.

78. Minashi K, Nihei K, Mizusawa J, et al. Efficacy of endoscopic resection and selective chemoradiotherapy for stage I esophageal squamous cell carcinoma. Gastroenterology. 2019; 157:382–390.

79. Ezoe Y, Muto M, Uedo N, et al. Magnifying narrowband imaging is more accurate than conventional white-light imaging in diagnosis of gastric mucosal cancer. Gastroenterology. 2011; 141:2017–2025.

80. Kawahara Y, Takenaka R, Okada H, et al. Novel chromoendoscopic method using an acetic acid-indigocarmine mixture for diagnostic accuracy in delineating the margin of early gastric cancers. Dig Endosc. 2009; 21:14–19.

81. Lee BE, Kim GH, Park DY, et al. Acetic acid-indigo carmine chromoendoscopy for delineating early gastric cancers: its usefulness according to histological type. BMC Gastroenterol. 2010; 10:97.

82. Tsujii Y, Kato M, Inoue T, et al. Integrated diagnostic strategy for the invasion depth of early gastric cancer by conventional endoscopy and EUS. Gastrointest Endosc. 2015; 82:452–459.

83. Choi J, Kim SG, Im JP, Kim JS, Jung HC, Song IS. Is endoscopic ultrasonography indispensable in patients with early gastric cancer prior to endoscopic resection? Surg Endosc. 2010; 24:3177–3185.

84. Choi J, Kim SG, Im JP, Kim JS, Jung HC, Song IS. Comparison of endoscopic ultrasonography and conventional endoscopy for prediction of depth of tumor invasion in early gastric cancer. Endoscopy. 2010; 42:705–713.

85. Yanai H, Noguchi T, Mizumachi S, et al. A blind comparison of the effectiveness of endoscopic ultrasonography and endoscopy in staging early gastric cancer. Gut. 1999; 44:361–365.

86. Yanai H, Matsumoto Y, Harada T, et al. Endoscopic ultrasonography and endoscopy for staging depth of invasion in early gastric cancer: a pilot study. Gastrointest Endosc. 1997; 46:212–216.

87. Okada K, Fujisaki J, Kasuga A, et al. Endoscopic ultrasonography is valuable for identifying early gastric cancers meeting expanded-indication criteria for endoscopic submucosal dissection. Surg Endosc. 2011; 25:841–848.

88. Akashi K, Yanai H, Nishikawa J, et al. Ulcerous change decreases the accuracy of endoscopic ultrasonography diagnosis for the invasive depth of early gastric cancer. Int J Gastrointest Cancer. 2006; 37:133–138.

89. Yoshida S, Tanaka S, Kunihiro K, et al. Diagnostic ability of high-frequency ultrasound probe sonography in staging early gastric cancer, especially for submucosal invasion. Abdom Imaging. 2005; 30:518–523.

90. Gotoda T, Yanagisawa A, Sasako M, et al. Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer. 2000; 3:219–225.

91. Nishizawa T, Yahagi N. Long-term outcomes of using endoscopic submucosal dissection to treat early gastric cancer. Gut Liver. 2018; 12:119–124.

92. Abdelfatah MM, Barakat M, Lee H, et al. The incidence of lymph node metastasis in early gastric cancer according to the expanded criteria in comparison with the absolute criteria of the Japanese Gastric Cancer Association: a systematic review of the literature and meta-analysis. Gastrointest Endosc. 2018; 87:338–347.

93. Choi KS, Jung HY, Choi KD, et al. EMR versus gastrectomy for intramucosal gastric cancer: comparison of long-term outcomes. Gastrointest Endosc. 2011; 73:942–948.

94. Choi IJ, Lee JH, Kim YI, et al. Long-term outcome comparison of endoscopic resection and surgery in early gastric cancer meeting the absolute indication for endoscopic resection. Gastrointest Endosc. 2015; 81:333–341.

95. Hahn KY, Park CH, Lee YK, et al. Comparative study between endoscopic submucosal dissection and surgery in patients with early gastric cancer. Surg Endosc. 2018; 32:73–86.

96. Choi JH, Kim ES, Lee YJ, et al. Comparison of quality of life and worry of cancer recurrence between endoscopic and surgical treatment for early gastric cancer. Gastrointest Endosc. 2015; 82:299–307.

97. Kim JH, Kim SS, Lee JH, et al. Early detection is important to reduce the economic burden of gastric cancer. J Gastric Cancer. 2018; 18:82–89.

98. Kim YI, Kim YA, Kim CG, et al. Serial intermediate-term quality of life comparison after endoscopic submucosal dissection versus surgery in early gastric cancer patients. Surg Endosc. 2018; 32:2114–2122.

99. Kim TS, Min BH, Kim KM, Lee JH, Rhee PL, Kim JJ. Endoscopic submucosal dissection for papillary adenocarcinoma of the stomach: low curative resection rate but favorable long-term outcomes after curative resection. Gastric Cancer. 2019; 22:363–368.

100. Lee S, Choi KD, Han M, et al. Long-term outcomes of endoscopic submucosal dissection versus surgery in early gastric cancer meeting expanded indication including undifferentiated-type tumors: a criteria-based analysis. Gastric Cancer. 2018; 21:490–499.

101. Min BH, Kim ER, Kim KM, et al. Surveillance strategy based on the incidence and patterns of recurrence after curative endoscopic submucosal dissection for early gastric cancer. Endoscopy. 2015; 47:784–793.

102. Chang JY, Shim KN, Tae CH, et al. Comparison of clinical outcomes after endoscopic submucosal dissection and surgery in the treatment of early gastric cancer: a single-institute study. Medicine (Baltimore). 2017; 96:e7210.

103. Chiu PW, Teoh AY, To KF, et al. Endoscopic submucosal dissection (ESD) compared with gastrectomy for treatment of early gastric neoplasia: a retrospective cohort study. Surg Endosc. 2012; 26:3584–3591.

104. Cho JH, Cha SW, Kim HG, et al. Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: a comparison study to surgery using propensity score-matched analysis. Surg Endosc. 2016; 30:3762–3773.

105. Feng F, Sun L, Xu G, et al. Is it reasonable to treat early gastric cancer with mucosal infiltration and well differentiation by endoscopic submucosal resection? J Gastrointest Surg. 2015; 19:2111–2119.

106. Fukunaga S, Nagami Y, Shiba M, et al. Long-term prognosis of expanded-indication differentiated-type early gastric cancer treated with endoscopic submucosal dissection or surgery using propensity score analysis. Gastrointest Endosc. 2017; 85:143–152.

107. Gong EJ, Kim DH, Ahn JY, et al. Comparison of long-term outcomes of endoscopic submucosal dissection and surgery for esophagogastric junction adenocarcinoma. Gastric Cancer. 2017; 20:84–91.

108. Kim YI, Kim YW, Choi IJ, et al. Long-term survival after endoscopic resection versus surgery in early gastric cancers. Endoscopy. 2015; 45:293–301.

109. 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.

110. Fujiya K, Takizawa K, Tokunaga M, et al. The value of diagnostic endoscopic submucosal dissection for patients with clinical submucosal invasive early gastric cancer. Gastric Cancer. 2018; 21:124–132.

111. Lee HD, Chung H, Kim SG, et al. Exploring the possibility of endoscopic submucosal dissection for clinical submucosal invasive early gastric cancers. Surg Endosc. 2019; 33:4008–4015.

112. Kim DY, Joo JK, Ryu SY, Kim YJ, Kim SK. Factors related to lymph node metastasis and surgical strategy used to treat early gastric carcinoma. World J Gastroenterol. 2004; 10:737–740.

113. Kim JH, Lee YC, Kim H, et al. Endoscopic resection for undifferentiated early gastric cancer. Gastrointest Endosc. 2009; 69:e1–e9.

114. Abe S, Oda I, Suzuki H, et al. Short- and long-term outcomes of endoscopic submucosal dissection for undifferentiated early gastric cancer. Endoscopy. 2013; 45:703–707.

115. Ahn JY, Park HJ, Park YS, et al. Endoscopic resection for undifferentiated-type early gastric cancer: immediate endoscopic outcomes and long-term survivals. Dig Dis Sci. 2016; 61:1158–1164.

116. Kim JH, Kim YH, Jung DH, et al. Follow-up outcomes of endoscopic resection for early gastric cancer with undifferentiated histology. Surg Endosc. 2014; 28:2627–2633.

117. Oda I, Oyama T, Abe S, et al. Preliminary results of multicenter questionnaire study on long-term outcomes of curative endoscopic submucosal dissection for early gastric cancer. Dig Endosc. 2014; 26:214–219.

118. Park JC, Lee YK, Kim SY, et al. Long-term outcomes of endoscopic submucosal dissection in comparison to surgery in undifferentiated-type intramucosal gastric cancer using propensity score analysis. Surg Endosc. 2018; 32:2046–2057.

119. Fujishiro M, Chiu PW, Wang HP. Role of antisecretory agents for gastric endoscopic submucosal dissection. Dig Endosc. 2013; 25 Suppl 1:86–93.

120. Ono H, Yao K, Fujishiro M, et al. Guidelines for endoscopic submucosal dissection and endoscopic mucosal resection for early gastric cancer. Dig Endosc. 2016; 28:3–15.

121. Park CH, Lee SK. Preventing and controlling bleeding in gastric endoscopic submucosal dissection. Clin Endosc. 2013; 46:456–462.

122. Takizawa K, Oda I, Gotoda T, et al. Routine coagulation of visible vessels may prevent delayed bleeding after endoscopic submucosal dissection: an analysis of risk factors. Endoscopy. 2008; 40:179–183.

123. Kang SH, Lee K, Lee HW, Park GE, Hong YS, Min BH. Delayed perforation occurring after endoscopic submucosal dissection for early gastric cancer. Clin Endosc. 2015; 48:251–255.

124. Lee H, Cheoi KS, Chung H, et al. Clinical features and predictive factors of coagulation syndrome after endoscopic submucosal dissection for early gastric neoplasm. Gastric Cancer. 2012; 15:83–90.

125. Uedo N, Takeuchi Y, Yamada T, et al. Effect of a proton pump inhibitor or an H2-receptor antagonist on prevention of bleeding from ulcer after endoscopic submucosal dissection of early gastric cancer: a prospective randomized controlled trial. Am J Gastroenterol. 2007; 102:1610–1616.

126. Ye BD, Cheon JH, Choi KD, et al. Omeprazole may be superior to famotidine in the management of iatrogenic ulcer after endoscopic mucosal resection: a prospective randomized controlled trial. Aliment Pharmacol Ther. 2006; 24:837–843.

127. Imaeda H, Hosoe N, Suzuki H, et al. Effect of lansoprazole versus roxatidine on prevention of bleeding and promotion of ulcer healing after endoscopic submucosal dissection for superficial gastric neoplasia. J Gastroenterol. 2011; 46:1267–1272.

128. Tomita T, Kim Y, Yamasaki T, et al. Prospective randomized controlled trial to compare the effects of omeprazole and famotidine in preventing delayed bleeding and promoting ulcer healing after endoscopic submucosal dissection. J Gastroenterol Hepatol. 2012; 27:1441–1446.

129. Yang Z, Wu Q, Liu Z, Wu K, Fan D. Proton pump inhibitors versus histamine-2-receptor antagonists for the management of iatrogenic gastric ulcer after endoscopic mucosal resection or endoscopic submucosal dissection: a meta-analysis of randomized trials. Digestion. 2011; 84:315–320.

130. Arai M, Matsumura T, Okimoto K, et al. Two-week treatment with proton pump inhibitor is sufficient for healing post endoscopic submucosal dissection ulcers. World J Gastroenterol. 2014; 20:16318–16322.

131. Niimi K, Fujishiro M, Goto O, et al. Prospective single-arm trial of two-week rabeprazole treatment for ulcer healing after gastric endoscopic submucosal dissection. Dig Endosc. 2012; 24:110–116.

132. Lee SH, Lee CK, Chung IK, et al. Optimal duration of proton pump inhibitor in the treatment of endoscopic submucosal dissection-induced ulcers: a retrospective analysis and prospective validation study. Dig Dis Sci. 2012; 57:429–434.

133. Shin WG, Kim SJ, Choi MH, et al. Can rebamipide and proton pump inhibitor combination therapy promote the healing of endoscopic submucosal dissection-induced ulcers? A randomized, prospective, multicenter study. Gastrointest Endosc. 2012; 75:739–747.

134. Higuchi K, Takeuchi T, Uedo N, et al. Efficacy and safety of 1-week Helicobacter pylori eradication therapy and 7-week rebamipide treatment after endoscopic submucosal dissection of early gastric cancer in comparison with 8-week PPI standard treatment: a randomized, controlled, prospective, multicenter study. Gastric Cancer. 2015; 18:612–617.

135. Fujiwara S, Morita Y, Toyonaga T, et al. A randomized controlled trial of rebamipide plus rabeprazole for the healing of artificial ulcers after endoscopic submucosal dissection. J Gastroenterol. 2011; 46:595–602.

136. Jung SW, Kim SY, Choe JW, et al. Standard and double-dose intravenous proton pump inhibitor injections for prevention of bleeding after endoscopic resection. J Gastroenterol Hepatol. 2017; 32:778–781.

137. Park JH, Baek EK, Choi CH, et al. Comparison of the efficacy of 4- and 8-week lansoprazole treatment for ESD-induced gastric ulcers: a randomized, prospective, controlled study. Surg Endosc. 2014; 28:235–241.

138. Nakamura K, Ihara E, Akiho H, et al. Limited effect of rebamipide in addition to proton pump inhibitor (PPI) in the treatment of post-endoscopic submucosal dissection gastric ulcers: a randomized controlled trial comparing PPI plus rebamipide combination therapy with PPI monotherapy. Gut Liver. 2016; 10:917–924.

139. Kawano S, Okada H, Kawahara Y, et al. Proton pump inhibitor dose-related healing rate of artificial ulcers after endoscopic submucosal dissection: a prospective randomized controlled trial. Digestion. 2011; 84:46–53.

140. Kim EH, Park SW, Nam E, Lee JG, Park CH. Comparative efficacy of various anti-ulcer medications after gastric endoscopic submucosal dissection: a systematic review and network meta-analysis. Surg Endosc. 2019; 33:1271–1283.

141. Oh TH, Jung HY, Choi KD, et al. Degree of healing and healing-associated factors of endoscopic submucosal dissectioninduced ulcers after pantoprazole therapy for 4 weeks. Dig Dis Sci. 2009; 54:1494–1499.

142. Park HJ, Kim HS, Kim BR, et al. Half-dose rabeprazole has an equal efficacy to standard-dose rabeprazole on endoscopic submucosal dissection-induced ulcer. Dig Dis Sci. 2013; 58:1054–1061.

143. Mochizuki S, Uedo N, Oda I, et al. Scheduled second-look endoscopy is not recommended after endoscopic submucosal dissection for gastric neoplasms (the SAFE trial): a multicentre prospective randomised controlled non-inferiority trial. Gut. 2015; 64:397–405.

144. Ryu HY, Kim JW, Kim HS, et al. Second-look endoscopy is not associated with better clinical outcomes after gastric endoscopic submucosal dissection: a prospective, randomized, clinical trial analyzed on an as-treated basis. Gastrointest Endosc. 2013; 78:285–294.

145. Nishizawa T, Suzuki H, Akimoto T, et al. Effects of preoperative proton pump inhibitor administration on bleeding after gastric endoscopic submucosal dissection: a systematic review and meta-analysis. United European Gastroenterol J. 2016; 4:5–10.

146. Oda I, Suzuki H, Nonaka S, Yoshinaga S. Complications of gastric endoscopic submucosal dissection. Dig Endosc. 2013; 25 Suppl 1:71–78.

147. Jeon SW, Jung MK, Kim SK, et al. Clinical outcomes for perforations during endoscopic submucosal dissection in patients with gastric lesions. Surg Endosc. 2010; 24:911–916.

148. Jeong G, Lee JH, Yu MK, et al. Non-surgical management of microperforation induced by EMR of the stomach. Dig Liver Dis. 2006; 38:605–608.

149. Minami S, Gotoda T, Ono H, Oda I, Hamanaka H. Complete endoscopic closure of gastric perforation induced by endoscopic resection of early gastric cancer using endoclips can prevent surgery (with video). Gastrointest Endosc. 2006; 63:596–601.

150. Paspatis GA, Dumonceau JM, Barthet M, et al. Diagnosis and management of iatrogenic endoscopic perforations: European Society of Gastrointestinal Endoscopy (ESGE) position statement. Endoscopy. 2014; 46:693–711.

151. Fu K, Ishikawa T, Yamamoto T, Kaji Y. Paracentesis for successful treatment of tension pneumoperitoneum related to endoscopic submucosal dissection. Endoscopy. 2009; 41 Suppl 2:E245.

152. ASGE Technology Committee, Lo SK, Fujii-Lau LL, et al. The use of carbon dioxide in gastrointestinal endoscopy. Gastrointest Endosc. 2016; 83:857–865.

153. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer. 2011; 14:113–123.

154. Hirasawa T, Gotoda T, Miyata S, et al. Incidence of lymph node metastasis and the feasibility of endoscopic resection for undifferentiated-type early gastric cancer. Gastric Cancer. 2009; 12:148–152.

155. Pyo JH, Shin CM, Lee H, et al. A risk-prediction model based on lymph-node metastasis for incorporation into a treatment algorithm for signet ring cell-type intramucosal gastric cancer. Ann Surg. 2016; 264:1038–1043.

156. Hatta W, Gotoda T, Oyama T, et al. A scoring system to stratify curability after endoscopic submucosal dissection for early gastric cancer: “eCura system”. Am J Gastroenterol. 2017; 112:874–881.

157. 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.

158. 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.

159. 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.

160. Pyo JH, Lee H, Min YW, et al. Feasibility of endoscopic resection in early gastric cancer with lymphovascular invasion. Ann Surg Oncol. 2019; 26:449–455.

161. Choi JY, Jeon SW, Cho KB, et al. Non-curative endoscopic resection does not always lead to grave outcomes in submucosal invasive early gastric cancer. Surg Endosc. 2015; 29:1842–1849.

162. Toyokawa T, Ohira M, Tanaka H, et al. Optimal management for patients not meeting the inclusion criteria after endoscopic submucosal dissection for gastric cancer. Surg Endosc. 2016; 30:2404–2414.

163. Toya Y, Endo M, Nakamura S, et al. Clinical outcomes of non-curative endoscopic submucosal dissection with negative resected margins for gastric cancer. Gastrointest Endosc. 2017; 85:1218–1224.

164. Hatta W, Gotoda T, Oyama T, et al. Is the eCura system useful for selecting patients who require radical surgery after noncurative endoscopic submucosal dissection for early gastric cancer? A comparative study. Gastric Cancer. 2018; 21:481–489.

165. 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.

166. Kim ER, Lee H, Min BH, et al. Effect of rescue surgery after non-curative endoscopic resection of early gastric cancer. Br J Surg. 2015; 102:1394–1401.

167. Suzuki S, Gotoda T, Hatta W, et al. Survival benefit of additional surgery after non-curative endoscopic submucosal dissection for early gastric cancer: a propensity score matching analysis. Ann Surg Oncol. 2017; 24:3353–3360.

168. Jung DH, Lee YC, Kim JH, et al. Additive treatment improves survival in elderly patients after non-curative endoscopic resection for early gastric cancer. Surg Endosc. 2017; 31:1376–1382.

169. Kusano C, Iwasaki M, Kaltenbach T, Conlin A, Oda I, Gotoda T. Should elderly patients undergo additional surgery after non-curative endoscopic resection for early gastric cancer? Long-term comparative outcomes. Am J Gastroenterol. 2011; 106:1064–1069.

170. Pyo JH, Lee H, Min BH, et al. Comparison of long-term outcomes after non-curative endoscopic resection in older patients with early gastric cancer. Ann Surg Oncol. 2017; 24:2624–2631.

171. 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.

172. 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.

173. Jeon MY, Park JC, Hahn KY, Shin SK, Lee SK, Lee YC. Longterm outcomes after noncurative endoscopic resection of early gastric cancer: the optimal time for additional endoscopic treatment. Gastrointest Endosc. 2018; 87:1003–1013.

174. Oh S, Kim SG, Choi JM, et al. Ablation of residual gastric tumor by argon plasma coagulation after endoscopic resection. Surg Endosc. 2017; 31:1093–1100.

175. Fukase K, Kato M, Kikuchi S, et al. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet. 2008; 372:392–397.

176. Kim SG, Jung HK, Lee HL, et al. Guidelines for the diagnosis and treatment of Helicobacter pylori infection in Korea, 2013 revised edition. J Gastroenterol Hepatol. 2014; 29:1371–1386.

177. Malfertheiner P, Megraud F, O’Morain CA, et al. Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report. Gut. 2017; 66:6–30.

178. Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG clinical guideline: treatment of Helicobacter pylori infection. Am J Gastroenterol. 2017; 112:212–239.

179. Mahachai V, Vilaichone RK, Pittayanon R, et al. Helicobacter pylori management in ASEAN: The Bangkok consensus report. J Gastroenterol Hepatol. 2018; 33:37–56.

180. Liu WZ, Xie Y, Lu H, et al. Fifth Chinese national consensus report on the management of Helicobacter pylori infection. Helicobacter. 2018; 23:e12475.

181. Yoon SB, Park JM, Lim CH, Cho YK, Choi MG. Effect of Helicobacter pylori eradication on metachronous gastric cancer after endoscopic resection of gastric tumors: a meta-analysis. Helicobacter. 2014; 19:243–248.

182. Bang CS, Baik GH, Shin IS, et al. Helicobacter pylori eradication for prevention of metachronous recurrence after endoscopic resection of early gastric cancer. J Korean Med Sci. 2015; 30:749–756.

183. Lee YC, Chiang TH, Chou CK, et al. Association between Helicobacter pylori eradication and gastric cancer incidence: a systematic review and meta-analysis. Gastroenterology. 2016; 150:1113–1124.

184. Sugano K. Effect of Helicobacter pylori eradication on the incidence of gastric cancer: a systematic review and meta-analysis. Gastric Cancer. 2019; 22:435–445.

185. Choi IJ, Kook MC, Kim YI, et al. Helicobacter pylori therapy for the prevention of metachronous gastric cancer. N Engl J Med. 2018; 378:1085–1095.

186. Choi JM, Kim SG, Choi J, et al. Effects of Helicobacter pylori eradication for metachronous gastric cancer prevention: a randomized controlled trial. Gastrointest Endosc. 2018; 88:475–485.

187. Lee JH, Kim JG, Jung HK, et al. Synopsis on clinical practice guideline of gastric cancer in Korea: an evidence-based approach. Korean J Gastroenterol. 2014; 63:66–81.

188. Kim SG, Park CM, Lee NR, et al. Long-term clinical outcomes of endoscopic submucosal dissection in patients with early gastric cancer: a prospective multicenter cohort study. Gut Liver. 2018; 12:402–410.

189. Kato M, Nishida T, Yamamoto K, et al. Scheduled endoscopic surveillance controls secondary cancer after curative endoscopic resection for early gastric cancer: a multicentre retrospective cohort study by Osaka University ESD study group. Gut. 2013; 62:1425–1432.

190. Nasu J, Doi T, Endo H, Nishina T, Hirasaki S, Hyodo I. Characteristics of metachronous multiple early gastric cancers after endoscopic mucosal resection. Endoscopy. 2005; 37:990–993.

191. Abe S, Oda I, Suzuki H, et al. Long-term surveillance and treatment outcomes of metachronous gastric cancer occurring after curative endoscopic submucosal dissection. Endoscopy. 2015; 47:1113–1118.

192. Hahn KY, Park JC, Kim EH, et al. Incidence and impact of scheduled endoscopic surveillance on recurrence after curative endoscopic resection for early gastric cancer. Gastrointest Endosc. 2016; 84:628–638.

193. Yang HJ, Kim SG, Lim JH, et al. Novel risk stratification for metachronous recurrence after curative endoscopic submucosal dissection for early gastric cancer. Gastrointest Endosc. 2018; 87:419–428.

194. Lee S, Choi KD, Hong SM, et al. Pattern of extragastric recurrence and the role of abdominal computed tomography in surveillance after endoscopic resection of early gastric cancer: Korean experiences. Gastric Cancer. 2017; 20:843–852.

195. Choi KS, Kim SH, Kim SG, Han JK. Early gastric cancers: is ct surveillance necessary after curative endoscopic submucosal resection for cancers that meet the expanded criteria? Radiology. 2016; 281:444–453.

196. Park CH, Kim EH, Chung H, et al. Role of computed tomography scan for the primary surveillance of mucosal gastric cancer after complete resection by endoscopic submucosal dissection. Surg Endosc. 2014; 28:1307–1313.

197. Jung SA, Yang SK, Kang GH, et al. Risk factors of lymph node metastasis in submucosally invasive colorectal carcinoma: with special reference to the depth of invasion. Korean J Gastrointest Endosc. 2001; 22:411–418.

198. Choi PW, Yu CS, Jang SJ, Jung SH, Kim HC, Kim JC. Risk factors for lymph node metastasis in submucosal invasive colorectal cancer. World J Surg. 2008; 32:2089–2094.

199. Sung HY, Kang WK, Kim SW, et al. Risk factors for lymph node metastasis in patients with submucosal invasive colorectal carcinoma. Journal of the Korean Surgical Society. 2010; 78:207–212.

200. Lee SH, Kang HJ, Ahn BK, et al. Clinicopathologic factors for prediction of lymph node metastasis in submucosally invasive colorectal carcinoma. J Korean Surg Soc. 2011; 80:111–118.

201. Ueno H, Hase K, Hashiguchi Y, et al. Novel risk factors for lymph node metastasis in early invasive colorectal cancer: a multi-institution pathology review. J Gastroenterol. 2014; 49:1314–1323.

202. Han J, Hur H, Min BS, Lee KY, Kim NK. Predictive factors for lymph node metastasis in submucosal invasive colorectal carcinoma: a new proposal of depth of invasion for radical surgery. World J Surg. 2018; 42:2635–2641.

203. Kim B, Kim EH, Park SJ, et al. The risk of lymph node metastasis makes it unsafe to expand the conventional indications for endoscopic treatment of T1 colorectal cancer: a retrospective study of 428 patients. Medicine (Baltimore). 2016; 95:e4373.

204. Al-Sukhni E, Attwood K, Gabriel EM, LeVea CM, Kanehira K, Nurkin SJ. Lymphovascular and perineural invasion are associated with poor prognostic features and outcomes in colorectal cancer: a retrospective cohort study. Int J Surg. 2017; 37:42–49.

205. Ha RK, Han KS, Sohn DK, et al. Histopathologic risk factors for lymph node metastasis in patients with T1 colorectal cancer. Ann Surg Treat Res. 2017; 93:266–271.

206. Beaton C, Twine CP, Williams GL, Radcliffe AG. Systematic review and meta-analysis of histopathological factors influencing the risk of lymph node metastasis in early colorectal cancer. Colorectal Dis. 2013; 15:788–797.

207. Mou S, Soetikno R, Shimoda T, Rouse R, Kaltenbach T. Pathologic predictive factors for lymph node metastasis in submucosal invasive (T1) colorectal cancer: a systematic review and meta-analysis. Surg Endosc. 2013; 27:2692–2703.

208. Choi JY, Jung SA, Shim KN, et al. Meta-analysis of predictive clinicopathologic factors for lymph node metastasis in patients with early colorectal carcinoma. J Korean Med Sci. 2015; 30:398–406.

209. Tanaka S, Haruma K, Teixeira CR, et al. Endoscopic treatment of submucosal invasive colorectal carcinoma with special reference to risk factors for lymph node metastasis. J Gastroenterol. 1995; 30:710–717.

210. Kikuchi R, Takano M, Takagi K, et al. Management of early invasive colorectal cancer. Risk of recurrence and clinical guidelines. Dis Colon Rectum. 1995; 38:1286–1295.

211. Kudo S. Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy. 1993; 25:455–461.

212. Haggitt RC, Glotzbach RE, Soffer EE, Wruble LD. Prognostic factors in colorectal carcinomas arising in adenomas: implications for lesions removed by endoscopic polypectomy. Gastroenterology. 1985; 89:328–336.

213. Park YJ, Kim WH, Paeng SS, Park JG. Histoclinical analysis of early colorectal cancer. World J Surg. 2000; 24:1029–1035.

214. Choi DH, Sohn DK, Chang HJ, Lim SB, Choi HS, Jeong SY. Indications for subsequent surgery after endoscopic resection of submucosally invasive colorectal carcinomas: a prospective cohort study. Dis Colon Rectum. 2009; 52:438–445.

215. Lim KH, Jung SW, Jeong ID, et al. Risk factors for lymph node metastasis after endoscopic resection for early colorectal cancer. Intest Res. 2008; 6:103–109.

216. Lee SH, Cho HD, Park DI, et al. Pathological predictors for defining a therapeutic strategy for early colon cancer after endoscopic resection: multicenter retrospective analysis from surgically resected specimens. Hepatogastroenterology. 2014; 61:642–646.

217. Nakadoi K, Oka S, Tanaka S, et al. Condition of muscularis mucosae is a risk factor for lymph node metastasis in T1 colorectal carcinoma. Surg Endosc. 2014; 28:1269–1276.

218. Nishida T, Egashira Y, Akutagawa H, et al. Predictors of lymph node metastasis in T1 colorectal carcinoma: an immunophenotypic analysis of 265 patients. Dis Colon Rectum. 2014; 57:905–915.

219. Kawachi H, Eishi Y, Ueno H, et al. A three-tier classification system based on the depth of submucosal invasion and budding/sprouting can improve the treatment strategy for T1 colorectal cancer: a retrospective multicenter study. Modern Pathology. 2015; 28:872–879.

220. Barresi V, Reggiani Bonetti L, Vitarelli E, Di Gregorio C, Ponz de Leon M, Barresi G. Immunohistochemical assessment of lymphovascular invasion in stage I colorectal carcinoma: prognostic relevance and correlation with nodal micrometastases. Am J Surg Pathol. 2012; 36:66–72.

221. Wada H, Shiozawa M, Katayama K, et al. Systematic review and meta-analysis of histopathological predictive factors for lymph node metastasis in T1 colorectal cancer. J Gastroenterol. 2015; 50:727–734.

222. Ueno H, Murphy J, Jass JR, Mochizuki H, Talbot IC. Tumour ‘budding’ as an index to estimate the potential of aggressiveness in rectal cancer. Histopathology. 2002; 40:127–132.

223. Cappellesso R, Luchini C, Veronese N, et al. Tumor budding as a risk factor for nodal metastasis in pT1 colorectal cancers: a meta-analysis. Human Pathology. 2017; 65:62–70.

224. Masaki T, Matsuoka H, Sugiyama M, Abe N, Sakamoto A, Atomi Y. Actual number of tumor budding as a new tool for the individualization of treatment of T1 colorectal carcinomas. J Gastroenterol Hepatol. 2006; 21:1115–1121.

225. Yim K, Won DD, Lee IK, Oh ST, Jung ES, Lee SH. Novel predictors for lymph node metastasis in submucosal invasive colorectal carcinoma. World J Gastroenterol. 2017; 23:5936–5944.

226. Gangireddy VGR, Coleman T, Kanneganti P, et al. Polypectomy versus surgery in early colon cancer: size and location of colon cancer affect long-term survival. Int J Colorectal Dis. 2018; 33:1349–1357.

227. Mounzer R, Das A, Yen RD, et al. Endoscopic and surgical treatment of malignant colorectal polyps: a population-based comparative study. Gastrointest Endosc. 2015; 81:733–740.

228. Kogler P, Kafka-Ritsch R, Öfner D, et al. Is limited surgery justified in the treatment of T1 colorectal cancer? Surg Endosc. 2013; 27:817–825.

229. Belderbos TD, van Erning FN, de Hingh IH, van Oijen MG, Lemmens VE, Siersema PD. Long-term recurrence-free survival after standard endoscopic resection versus surgical resection of submucosal invasive colorectal cancer: a population-based study. Clin Gastroenterol Hepatol. 2017; 15:403–411.

230. Kim JB, Lee HS, Lee HJ, et al. Long-term outcomes of endoscopic versus surgical resection of superficial submucosal colorectal cancer. Dig Dis Sci. 2015; 60:2785–2792.

231. Heo J, Jeon SW, Jung MK, Kim SK, Kim J, Kim S. Endoscopic resection as the first-line treatment for early colorectal cancer: comparison with surgery. Surg Endosc. 2014; 28:3435–3442.

232. Yoda Y, Ikematsu H, Matsuda T, et al. A large-scale multicenter study of long-term outcomes after endoscopic resection for submucosal invasive colorectal cancer. Endoscopy. 2013; 45:718–724.

233. Yoshii S, Nojima M, Nosho K, et al. Factors associated with risk for colorectal cancer recurrence after endoscopic resection of T1 tumors. Clin Gastroenterol Hepatol. 2014; 12:292–302.

234. Asayama N, Oka S, Tanaka S, et al. Long-term outcomes after treatment for T1 colorectal carcinoma. Int J Colorectal Dis. 2016; 31:571–578.

235. Tamaru Y, Oka S, Tanaka S, et al. Long-term outcomes after treatment for T1 colorectal carcinoma: a multicenter retrospective cohort study of Hiroshima GI Endoscopy Research Group. J Gastroenterol. 2017; 52:1169–1179.

236. Kudo S, Tamura S, Nakajima T, Yamano H, Kusaka H, Watanabe H. Diagnosis of colorectal tumorous lesions by magnifying endoscopy. Gastrointest Endosc. 1996; 44:8–14.

237. Hurlstone DP, Cross SS, Adam I, et al. Endoscopic morphological anticipation of submucosal invasion in flat and depressed colorectal lesions: clinical implications and subtype analysis of the kudo type V pit pattern using high-magnification-chromoscopic colonoscopy. Colorectal Dis. 2004; 6:369–375.

238. Ohta A, Tominaga K, Sakai Y. Efficacy of magnifying colonoscopy for the diagnosis of colorectal neoplasia: comparison with histopathological findings. Dig Endosc. 2004; 16:308–314.

239. Tanaka S, Haruma K, Nagata S, Oka S, Chayama K. Diagnosis of invasion depth in early colorectal carcinoma by pit pattern analysis with magnifying endoscopy. Dig Endosc. 2001; 13:S2–S5.

240. Matsuda T, Fujii T, Saito Y, et al. Efficacy of the invasive/non-invasive pattern by magnifying chromoendoscopy to estimate the depth of invasion of early colorectal neoplasms. Am J Gastroenterol. 2008; 103:2700–2706.

241. Zhang QW, Teng LM, Zhang XT, et al. Narrow-band imaging in the diagnosis of deep submucosal colorectal cancers: a systematic review and meta-analysis. Endoscopy. 2017; 49:564–580.

242. Hirata M, Tanaka S, Oka S, et al. Evaluation of microvessels in colorectal tumors by narrow band imaging magnification. Gastrointest Endosc. 2007; 66:945–952.

243. Wada Y, Kudo SE, Kashida H, et al. Diagnosis of colorectal lesions with the magnifying narrow-band imaging system. Gastrointest Endosc. 2009; 70:522–531.

244. Yoo HY, Lee MS, Ko BM, et al. Correlation of narrow band imaging with magnifying colonoscopy and histology in colorectal tumors. Clin Endosc. 2011; 44:44–50.

245. Ikematsu H, Matsuda T, Emura F, et al. Efficacy of capillary pattern type IIIA/IIIB by magnifying narrow band imaging for estimating depth of invasion of early colorectal neoplasms. BMC Gastroenterol. 2010; 10:33.

246. Oba S, Tanaka S, Oka S, et al. Characterization of colorectal tumors using narrow-band imaging magnification: combined diagnosis with both pit pattern and microvessel features. Scand J Gastroenterol. 2010; 45:1084–1092.

247. Sumimoto K, Tanaka S, Shigita K, et al. Clinical impact and characteristics of the narrow-band imaging magnifying endoscopic classification of colorectal tumors proposed by the Japan NBI Expert Team. Gastrointest Endosc. 2017; 85:816–821.

248. Iwatate M, Sano Y, Tanaka S, et al. Validation study for development of the Japan NBI Expert Team classification of colorectal lesions. Dig Endosc. 2018; 30:642–651.

249. Li X, Chen H, Gao Y, Chen X, Ge Z. Prediction of histology and invasive depth of colorectal neoplasia based on morphology of surface depression using magnifying chromocolonoscopy. Int J Colorectal Dis. 2010; 25:79–85.

250. Hisabe T, Tsuda S, Hoashi T, et al. Validity of conventional endoscopy using “non-extension sign” for optical diagnosis of colorectal deep submucosal invasive cancer. Endosc Int Open. 2018; 6:E156–E164.

251. Uno Y, Munakata A. The non-lifting sign of invasive colon cancer. Gastrointest Endosc. 1994; 40:485–489.

252. Kobayashi N, Saito Y, Sano Y, et al. Determining the treatment strategy for colorectal neoplastic lesions: endoscopic assessment or the non-lifting sign for diagnosing invasion depth? Endoscopy. 2007; 39:701–705.

253. Sakamoto T, Nakajima T, Matsuda T, et al. Comparison of the diagnostic performance between magnifying chromoendoscopy and magnifying narrow-band imaging for superficial colorectal neoplasms: an online survey. Gastrointest Endosc. 2018; 87:1318–1323.

254. De Ceglie A, Hassan C, Mangiavillano B, et al. Endoscopic mucosal resection and endoscopic submucosal dissection for colorectal lesions: a systematic review. Crit Rev Oncol Hematol. 2016; 104:138–155.

255. Belderbos TD, Leenders M, Moons LM, Siersema PD. Local recurrence after endoscopic mucosal resection of nonpedunculated colorectal lesions: systematic review and meta-analysis. Endoscopy. 2014; 46:388–402.

256. Fuccio L, Repici A, Hassan C, et al. Why attempt en bloc resection of non-pedunculated colorectal adenomas? A systematic review of the prevalence of superficial submucosal invasive cancer after endoscopic submucosal dissection. Gut. 2018; 67:1464–1474.

257. Fujiya M, Tanaka K, Dokoshi T, et al. Efficacy and adverse events of EMR and endoscopic submucosal dissection for the treatment of colon neoplasms: a meta-analysis of studies comparing EMR and endoscopic submucosal dissection. Gastrointest Endosc. 2015; 81:583–595.

258. Arezzo A, Passera R, Marchese N, Galloro G, Manta R, Cirocchi R. Systematic review and meta-analysis of endoscopic submucosal dissection vs endoscopic mucosal resection for colorectal lesions. United European Gastroenterol J. 2016; 4:18–29.

259. Liggi M, Cadoni S, Gallittu P. Endoscopic submucosal dissection, endoscopic mucosal resection and hybrid techniques for large nonpedunculated colorectal tumors: a meta analysis and systematic review. J Interv Gastroenterol. 2014; 4:117–125.

260. Sato T, Fukuzawa M, Gotoda T, Moriyasu F. Comparison of clinical outcomes between colorectal EMR and ESD. J Tokyo Med Univ. 2016; 74:154–162.

261. Repici A, Hassan C, De Paula Pessoa D, et al. Efficacy and safety of endoscopic submucosal dissection for colorectal neoplasia: a systematic review. Endoscopy. 2012; 44:137–150.

262. Shiga H, Endo K, Kuroha M, et al. Endoscopic submucosal dissection for colorectal neoplasia during the clinical learning curve. Surg Endosc. 2014; 28:2120–2128.

263. Sakamoto T, Saito Y, Fukunaga S, Nakajima T, Matsuda T. Learning curve associated with colorectal endoscopic submucosal dissection for endoscopists experienced in gastric endoscopic submucosal dissection. Dis Colon Rectum. 2011; 54:1307–1312.

264. Bhurwal A, Bartel MJ, Heckman MG, et al. Endoscopic mucosal resection: learning curve for large nonpolypoid colorectal neoplasia. Gastrointest Endosc. 2016; 84:959–968.

265. Probst A, Golger D, Anthuber M, Märkl B, Messmann H. Endoscopic submucosal dissection in large sessile lesions of the rectosigmoid: learning curve in a European center. Endoscopy. 2012; 44:660–667.

266. Jeon HH, Lee HS, Youn YH, Park JJ, Park H. Learning curve analysis of colorectal endoscopic submucosal dissection (ESD) for laterally spreading tumors by endoscopists experienced in gastric ESD. Surg Endosc. 2016; 30:2422–2430.