Long-term outcomes of superficial neoplasia at the esophagogastric junction treated via endoscopic submucosal dissection and endoscopic submucosal tunnel dissection: a cohort study of a single center from China

  • Shengzhen Liu
  • Ningli Chai
  • Zhongsheng Lu
  • Huikai Li
  • Ying Xiong
  • Yaqi Zhai
  • Enqiang LinghuEmail author


Background and aims

The techniques and indications for endoscopic submucosal dissection (ESD) and endoscopic submucosal tunnel dissection (ESTD) to remove superficial neoplasia at the esophagogastric junction (EGJ) have been developed and expanded. However, the resection of superficial neoplasia at the EGJ by ESD remains challenging, and the long-term clinical outcomes of curative and non-curative resections based on histological criteria remain unclear. We conducted a retrospective analysis on the safety and efficacy of the ESD and ESTD procedure with these patients.


The records of 209 consecutive patients at the Chinese PLA General Hospital who received ESD and ESTD to treat EGJ superficial neoplasia from November 2006 to December 2016 were reviewed for this retrospective cohort study. We divided patients into two groups (curative and non-curative resection).


Of all 14 additional surgeries, 1 patient in the curative group and 13 in the non-curative group underwent surgical operation with residual tumor in 7 specimens. During a median follow-up period of 46.4 months (range 12.2–142.3 months), the 5-year survival rate was 98.6%. Two patients died 91 months and 66 months after surgery due to subarachnoid hemorrhage and lymphoma, respectively. One patient died of gastric cancer 1 year after the surgery. The 5-year disease-specific survival rate was 99.5%. Local tumor recurrence was detected in 9 of 209 cases.


In conclusion, ESD was shown to be a safe and effective treatment strategy for early EGJ neoplasia. Mucosal adhesion may increase the difficulty of piecemeal curative resection, but the superficial depth of such an invasion favors better clinical outcomes. Additional surgical resection is a good choice for non-curative ESD, and re-ESD is also an alternative, in conjunction with intensive follow-up.


Esophagogastric junction Superficial neoplasia Endoscopic submucosal dissection Long-term outcomes Non-curative resection 



This work was supported by Grants from the Beijing Science Committee Fund Program of China (D141100000414003) and the National Key R&D Program of China (2016YFC1303601). No other funding organization played a role in the design and conduct of the study, the collection, management, analysis, and interpretation of the data, or the preparation, review, and approval of the manuscript.

Compliance with ethical standards


Dr. Liu, Dr. Chai, Dr. Lu, Dr. Li, Dr. Xiong, Dr. Zhai, and Dr. Linghu have no conflicts of interest or financial ties to disclose.


  1. 1.
    Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F et al (2016) Cancer statistics in China, 2015. CA Cancer J Clin 66:115–132CrossRefGoogle Scholar
  2. 2.
    Buas MF, Vaughan TL (2013) Epidemiology and risk factors for gastroesophageal junction tumors: understanding the rising incidence of this disease. Semin Radiat Oncol 23:3–9CrossRefGoogle Scholar
  3. 3.
    Zhang XD, Shu YQ, Liang J, Zhang FC, Ma XZ, Huang JJ et al (2012) Combination chemotherapy with paclitaxel, cisplatin and fluorouracil for patients with advanced and metastatic gastric or esophagogastric junction adenocarcinoma: a multicenter prospective study. Chin J Cancer Res 24:291–298CrossRefGoogle Scholar
  4. 4.
    Hirao M, Masuda K, Asanuma T, Naka H, Noda K, Matsuura K et al (1988) Endoscopic resection of early gastric cancer and other tumors with local injection of hypertonic saline-epinephrine. Gastrointest Endosc 34:264–269CrossRefGoogle Scholar
  5. 5.
    Ohkuwa M, Hosokawa K, Boku N, Ohtu A, Tajiri H, Yoshida S (2001) New endoscopic treatment for intramucosal gastric tumors using an insulated-tip diathermic knife. Endoscopy 33:221–226CrossRefGoogle Scholar
  6. 6.
    Gong EJ, Kim DH, Ahn JY, Jung KW, Lee JH, Choi KD et al (2017) Comparison of long-term outcomes of endoscopic submucosal dissection and surgery for esophagogastric junction adenocarcinoma. Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 20:84–91Google Scholar
  7. 7.
    Yamada M, Oda I, Nonaka S, Suzuki H, Yoshinaga S, Taniguchi H et al (2013) Long-term outcome of endoscopic resection of superficial adenocarcinoma of the esophagogastric junction. Endoscopy 45:992–996CrossRefGoogle Scholar
  8. 8.
    Park CH, Kim EH, Kim HY, Roh YH, Lee YC (2015) Clinical outcomes of endoscopic submucosal dissection for early stage esophagogastric junction cancer: a systematic review and meta-analysis. Dig Liver Dis 47:37–44CrossRefGoogle Scholar
  9. 9.
    Pech O, Bollschweiler E, Manner H, Leers J, Ell C, Holscher AH (2011) Comparison between endoscopic and surgical resection of mucosal esophageal adenocarcinoma in Barrett’s esophagus at two high-volume centers. Ann Surg 254:67–72CrossRefGoogle Scholar
  10. 10.
    Das A, Singh V, Fleischer DE, Sharma VK (2008) A comparison of endoscopic treatment and surgery in early esophageal cancer: an analysis of surveillance epidemiology and end results data. Am J Gastroenterol 103:1340–1345CrossRefGoogle Scholar
  11. 11.
    Ono H, Yao K, Fujishiro M, Oda I, Nimura S, Yahagi N et al (2016) Guidelines for endoscopic submucosal dissection and endoscopic mucosal resection for early gastric cancer. Digestive Endosc Off J Jpn Gastroenterol Endosc Soc 28:3–15Google Scholar
  12. 12.
    Japanese classification of gastric carcinoma: 3rd English edition (2011). Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 14:101–112Google Scholar
  13. 13.
    Siewert JR, Stein HJ (1998) Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg 85:1457–1459CrossRefGoogle Scholar
  14. 14.
    The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002 (2003). Gastrointest Endosc 58:S3–S43Google Scholar
  15. 15.
    Wen J, Linghu E, Yang Y, Liu Q, Yang J, Wang S et al (2014) Effectiveness and safety of endoscopic submucosal dissection for intraepithelial neoplasia of the esophagogastric junction. Chin Med J 127:417–422Google Scholar
  16. 16.
    Linghu E, Feng X, Wang X, Meng J, Du H, Wang H (2013) Endoscopic submucosal tunnel dissection for large esophageal neoplastic lesions. Endoscopy 45:60–62Google Scholar
  17. 17.
    Imai K, Kakushima N, Tanaka M, Takizawa K, Matsubayashi H, Hotta K et al (2013) Validation of the application of the Japanese curative criteria for superficial adenocarcinoma at the esophagogastric junction treated by endoscopic submucosal dissection: a long-term analysis. Surg Endosc 27:2436–2445CrossRefGoogle Scholar
  18. 18.
    Yoshinaga S, Gotoda T, Kusano C, Oda I, Nakamura K, Takayanagi R (2008) Clinical impact of endoscopic submucosal dissection for superficial adenocarcinoma located at the esophagogastric junction. Gastrointest Endosc 67:202–209CrossRefGoogle Scholar
  19. 19.
    Wang SJ, Wu ML, Zhang LW, Guo XQ, Xu ZB, Er LM et al (2008) The value of endoscopic mucosal resection for dysplasia and early-stage cancer of the esophagus and gastric cardia. Zhonghua Zhong Liu Za Zhi 30:853–857Google Scholar
  20. 20.
    Jeon MY, Park JC, Hahn KY, Shin SK, Lee SK, Lee YC. Long-term outcomes after noncurative endoscopic resection of early gastric cancer: the optimal time for additional endoscopic treatment. Gastrointest Endosc. 2017Google Scholar
  21. 21.
    Suzuki H, Oda I, Abe S, Sekiguchi M, Nonaka S, Yoshinaga S et al (2017) Clinical outcomes of early gastric cancer patients after noncurative endoscopic submucosal dissection in a large consecutive patient series. Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 20:679–689Google Scholar
  22. 22.
    Japanese gastric cancer treatment guidelines 2014 (ver.) 4 (2017). Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 20:1–19Google Scholar
  23. 23.
    Ono H (2006) Early gastric cancer: diagnosis, pathology, treatment techniques and treatment outcomes. Eur J Gastroenterol Hepatol 18:863–866CrossRefGoogle Scholar
  24. 24.
    Omae M, Fujisaki J, Horiuchi Y, Yoshizawa N, Matsuo Y, Kubota M et al (2013) Safety, efficacy, and long-term outcomes for endoscopic submucosal dissection of early esophagogastric junction cancer. Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 16:147–154Google Scholar
  25. 25.
    Matsuda T, Kurokawa Y, Yoshikawa T, Kishi K, Misawa K, Ohi M et al (2016) Clinicopathological characteristics and prognostic factors of patients with Siewert Type II esophagogastric junction carcinoma: a retrospective multicenter study. World J Surg 40:1672–1679CrossRefGoogle Scholar
  26. 26.
    Hirasawa K, Kokawa A, Oka H, Yahara S, Sasaki T, Nozawa A et al (2010) Superficial adenocarcinoma of the esophagogastric junction: long-term results of endoscopic submucosal dissection. Gastrointest Endosc 72:960–966CrossRefGoogle Scholar
  27. 27.
    Hoteya S, Matsui A, Iizuka T, Kikuchi D, Yamada A, Yamashita S et al (2013) Comparison of the clinicopathological characteristics and results of endoscopic submucosal dissection for esophagogastric junction and non-junctional cancers. Digestion 87:29–33CrossRefGoogle Scholar
  28. 28.
    Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T, Repici A, Vieth M, De Ceglie A et al (2015) Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) guideline. Endoscopy 47:829–854CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of GastroenterologyChinese PLA General HospitalBeijingChina

Personalised recommendations