Surgical Endoscopy

, Volume 32, Issue 4, pp 2046–2057 | Cite as

Long-term outcomes of endoscopic submucosal dissection in comparison to surgery in undifferentiated-type intramucosal gastric cancer using propensity score analysis

  • Jun Chul ParkEmail author
  • Yong Kang Lee
  • Soon Young Kim
  • Yunho Roh
  • Kyu Yeon Hahn
  • Sung Kwan Shin
  • Sang Kil Lee
  • Yong Chan Lee
  • Hyoung-Il Kim
  • Jae-Ho Cheong
  • Woo Jin Hyung
  • Sung Hoon Noh



The treatment of intramucosal early gastric cancer with undifferentiated-type histologies (UD-EGCs) using endoscopic submucosal dissection (ESD) is controversial. This study aimed to compare the clinical and oncologic long-term outcomes of ESD and surgery for UD-EGCs.


A prospectively collected database of patients who underwent ESD or surgery between January 2006 and December 2012 was established. Patients who diagnosed with UD-EGC and satisfied the expanded indications of ESD were included. Clinical data from 111 patients treated with ESD and 382 patients underwent surgery were analyzed, and 1–1 propensity score-matched 81 pairs of patients were also compared.


In both groups, two-thirds of the UD-EGCs had signet ring cell (SRC)-type histology and about 90% of UD-EGCs were flat or depressed types. The mean size of tumors was smaller in ESD group (9.7 vs. 13.2 mm; P < 0.001). After propensity score-matched, case-matching covariates were not significantly different between the groups. Disease-free survival (DFS) was significantly shorter in the ESD group, but overall survival (OS) was not different between the two groups both in overall comparison (DFS; P < 0.001 and OS; P = 0.078) and propensity score-matched analysis (DFS; P < 0.001 and OS; P = 0.850). According to histologic type, OS of SRC histology was not different between the group, both in overall comparison and propensity score-matched analysis (P = 0.286 and P = 0.210). On the other hands, OS of poorly differentiated adenocarcinoma was significantly shorter in ESD group in overall comparison (P = 0.007), but was not as so in propensity score-matched analysis (P = 0.088).


ESD might be a complementary option for the treatment of UD-EGCs, especially in those with SRC-type histology based on strict expanded indications. Nonetheless, close endoscopic surveillance is required because of a high incidence of intragastric recurrence.


Early gastric cancer Undifferentiated histology ESD Long-term outcomes Recurrences 


Compliance with ethical standards


Jun Chul Park, Yong Kang Lee, Soon Young Kim, Yunho Roh, Kyu Yeon Hahn, Sung Kwan Shin, Sang Kil Lee, Yong Chan Lee, Hyoung-Il Kim, Jae-Ho Cheong, Woo Jin Hyung, and Sung Hoon Noh have no conflicts of interest or financial ties to disclose.


  1. 1.
    Choi JH, Kim ES, Lee YJ, Cho KB, Park KS, Jang BK, Chung WJ, Hwang JS, Ryu SW (2015) Comparison of quality of life and worry of cancer recurrence between endoscopic and surgical treatment for early gastric cancer. Gastrointest Endosc 82(2):299–307. doi: 10.1016/j.gie.2015.01.019 CrossRefPubMedGoogle Scholar
  2. 2.
    Choi IJ, Lee JH, Kim YI, Kim CG, Cho SJ, Lee JY, Ryu KW, Nam BH, Kook MC, Kim YW (2015) Long-term outcome comparison of endoscopic resection and surgery in early gastric cancer meeting the absolute indication for endoscopic resection. Gastrointest Endosc 81(2):333–341.e331. doi: 10.1016/j.gie.2014.07.047 CrossRefPubMedGoogle Scholar
  3. 3.
    Park CH, Lee H, Kim DW, Chung H, Park JC, Shin SK, Hyung WJ, Lee SK, Lee YC, Noh SH (2014) Clinical safety of endoscopic submucosal dissection compared with surgery in elderly patients with early gastric cancer: a propensity-matched analysis. Gastrointest Endosc 80(4):599–609. doi: 10.1016/j.gie.2014.04.042 CrossRefPubMedGoogle Scholar
  4. 4.
    Chiu PW, Teoh AY, To KF, Wong SK, Liu SY, Lam CC, Yung MY, Chan FK, Lau JY, Ng EK (2012) Endoscopic submucosal dissection (ESD) compared with gastrectomy for treatment of early gastric neoplasia: a retrospective cohort study. Surg Endosc 26(12):3584–3591. doi: 10.1007/s00464-012-2371-8 CrossRefPubMedGoogle Scholar
  5. 5.
    Fukunaga S, Nagami Y, Shiba M, Ominami M, Tanigawa T, Yamagami H, Tanaka H, Muguruma K, Watanabe T, Tominaga K, Fujiwara Y, Ohira M, Hirakawa K, Arakawa T (2017) Long-term prognosis of expanded-indication differentiated-type early gastric cancer treated with endoscopic submucosal dissection or surgery using propensity score analysis. Gastrointest Endosc 85(1):143–152. doi: 10.1016/j.gie.2016.06.049 CrossRefPubMedGoogle Scholar
  6. 6.
    Gotoda T, Iwasaki M, Kusano C, Seewald S, Oda I (2010) Endoscopic resection of early gastric cancer treated by guideline and expanded National Cancer Centre criteria. Br J Surg 97(6):868–871. doi: 10.1002/bjs.7033 CrossRefPubMedGoogle Scholar
  7. 7.
    Suzuki H, Oda I, Abe S, Sekiguchi M, Mori G, Nonaka S, Yoshinaga S, Saito Y (2016) High rate of 5-year survival among patients with early gastric cancer undergoing curative endoscopic submucosal dissection. Gastric Cancer 19(1):198–205. doi: 10.1007/s10120-015-0469-0 CrossRefPubMedGoogle Scholar
  8. 8.
    Tanabe S, Hirabayashi S, Oda I, Ono H, Nashimoto A, Isobe Y, Miyashiro I, Tsujitani S, Seto Y, Fukagawa T, Nunobe S, Furukawa H, Kodera Y, Kaminishi M, Katai H (2017) Gastric cancer treated by endoscopic submucosal dissection or endoscopic mucosal resection in Japan from 2004 through 2006: JGCA nationwide registry conducted in 2013. Gastric Cancer. doi: 10.1007/s10120-017-0699-4 Google Scholar
  9. 9.
    Hyung WJ, Noh SH, Lee JH, Huh JJ, Lah KH, Choi SH, Min JS (2002) Early gastric carcinoma with signet ring cell histology. Cancer 94(1):78–83CrossRefPubMedGoogle Scholar
  10. 10.
    Asakawa Y, Ohtaka M, Maekawa S, Fukasawa M, Nakayama Y, Yamaguchi T, Inoue T, Uetake T, Sakamoto M, Sato T, Kawaguchi Y, Fujii H, Mochizuki K, Hada M, Oyama T, Yasumura T, Omata K, Nishiyama A, Naito K, Hata H, Haba Y, Miyata K, Saitoh H, Yamadera Y, Miura K, Kawaoi A, Abe T, Tsunoda H, Honda Y, Kurosaki M, Enomoto N (2015) Stratifying the risk of lymph node metastasis in undifferentiated-type early gastric cancer. World J Gastroenterol 21(9):2683–2692. doi: 10.3748/wjg.v21.i9.2683 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Huh CW, Jung da H, Kim JH, Lee YC, Kim H, Kim H, Yoon SO, Youn YH, Park H, Lee SI, Choi SH, Cheong JH, Noh SH (2013) Signet ring cell mixed histology may show more aggressive behavior than other histologies in early gastric cancer. J Surg Oncol 107(2):124–129. doi: 10.1002/jso.23261 CrossRefPubMedGoogle Scholar
  12. 12.
    Tong JH, Sun Z, Wang ZN, Zhao YH, Huang BJ, Li K, Xu Y, Xu HM (2011) Early gastric cancer with signet-ring cell histologic type: risk factors of lymph node metastasis and indications of endoscopic surgery. Surgery 149(3):356–363. doi: 10.1016/j.surg.2010.07.006 CrossRefPubMedGoogle Scholar
  13. 13.
    Bang CS, Baik GH, Shin IS, Kim JB, Suk KT, Yoon JH, Kim YS, Kim DJ, Shin WG, Kim KH, Kim HY, Lim H, Kang HS, Kim JH, Kim JB, Jung SW, Kae SH, Jang HJ, Choi MH (2015) Endoscopic submucosal dissection for early gastric cancer with undifferentiated-type histology: a meta-analysis. World J Gastroenterol 21(19):6032–6043. doi: 10.3748/wjg.v21.i19.6032 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Kamada K, Tomatsuri N, Yoshida N (2012) Endoscopic submucosal dissection for undifferentiated early gastric cancer as the expanded indication lesion. Digestion 85(2):111–115. doi: 10.1159/000334681 CrossRefPubMedGoogle Scholar
  15. 15.
    Okada K, Fujisaki J, Yoshida T, Ishikawa H, Suganuma T, Kasuga A, Omae M, Kubota M, Ishiyama A, Hirasawa T, Chino A, Inamori M, Yamamoto Y, Yamamoto N, Tsuchida T, Tamegai Y, Nakajima A, Hoshino E, Igarashi M (2012) Long-term outcomes of endoscopic submucosal dissection for undifferentiated-type early gastric cancer. Endoscopy 44(2):122–127. doi: 10.1055/s-0031-1291486 CrossRefPubMedGoogle Scholar
  16. 16.
    Abe S, Oda I, Suzuki H, Nonaka S, Yoshinaga S, Odagaki T, Taniguchi H, Kushima R, Saito Y (2013) Short- and long-term outcomes of endoscopic submucosal dissection for undifferentiated early gastric cancer. Endoscopy 45(9):703–707. doi: 10.1055/s-0033-1344396 CrossRefPubMedGoogle Scholar
  17. 17.
    Ajani JA, Bentrem DJ, Besh S, D’Amico TA, Das P, Denlinger C, Fakih MG, Fuchs CS, Gerdes H, Glasgow RE, Hayman JA, Hofstetter WL, Ilson DH, Keswani RN, Kleinberg LR, Korn WM, Lockhart AC, Meredith K, Mulcahy MF, Orringer MB, Posey JA, Sasson AR, Scott WJ, Strong VE, Varghese TK Jr, Warren G, Washington MK, Willett C, Wright CD, McMillian NR, Sundar H (2013) Gastric cancer, version 2.2013: featured updates to the NCCN Guidelines. J Natl Compr Cancer Netw 11(5):531–546CrossRefGoogle Scholar
  18. 18.
    Okines A, Verheij M, Allum W, Cunningham D, Cervantes A (2010) Gastric cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 21(Suppl 5):v50–v54. doi: 10.1093/annonc/mdq164 CrossRefPubMedGoogle Scholar
  19. 19.
    Japanese Gastric Cancer A (2011) Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 14(2):113–123. doi: 10.1007/s10120-011-0042-4 CrossRefGoogle Scholar
  20. 20.
    Association JGC (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14(2):101–112CrossRefGoogle Scholar
  21. 21.
    Flejou JF (2011) WHO classification of digestive tumors: the fourth edition. Ann Pathol 31(5 Suppl):S27–S31. doi: 10.1016/j.annpat.2011.08.001 CrossRefPubMedGoogle Scholar
  22. 22.
    Lauren P (1965) The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand 64:31–49CrossRefPubMedGoogle Scholar
  23. 23.
    An JY, Heo GU, Cheong JH, Hyung WJ, Choi SH, Noh SH (2010) Assessment of open versus laparoscopy-assisted gastrectomy in lymph node-positive early gastric cancer: a retrospective cohort analysis. J Surg Oncol 102(1):77–81. doi: 10.1002/jso.21554 CrossRefPubMedGoogle Scholar
  24. 24.
    Isomoto H, Shikuwa S, Yamaguchi N, Fukuda E, Ikeda K, Nishiyama H, Ohnita K, Mizuta Y, Shiozawa J, Kohno S (2009) Endoscopic submucosal dissection for early gastric cancer: a large-scale feasibility study. Gut 58(3):331–336. doi: 10.1136/gut.2008.165381 CrossRefPubMedGoogle Scholar
  25. 25.
    Park SW, Lee H, Park CH, Jang HJ, Ahn H (2015) Endoscopic and oncologic outcomes according to indication criteria of endoscopic resection for early gastric cancer: a systematic review and meta-analysis. Surg Endosc. doi: 10.1007/s00464-015-4376-6 Google Scholar
  26. 26.
    Lee H, Yun WK, Min BH, Lee JH, Rhee PL, Kim KM, Rhee JC, Kim JJ (2011) A feasibility study on the expanded indication for endoscopic submucosal dissection of early gastric cancer. Surg Endosc 25(6):1985–1993. doi: 10.1007/s00464-010-1499-7 CrossRefPubMedGoogle Scholar
  27. 27.
    Ahn JY, Jung HY, Choi KD, Choi JY, Kim MY, Lee JH, Choi KS, Kim do H, Song HJ, Lee GH, Kim JH, Park YS (2011) Endoscopic and oncologic outcomes after endoscopic resection for early gastric cancer: 1370 cases of absolute and extended indications. Gastrointest Endosc 74(3):485–493. doi: 10.1016/j.gie.2011.04.038 CrossRefPubMedGoogle Scholar
  28. 28.
    Kim YY, Jeon SW, Kim J, Park JC, Cho KB, Park KS, Kim E, Chung YJ, Kwon JG, Jung JT, Kim EY, Kim KO, Jang B, Lee SH, Yang CH (2013) Endoscopic submucosal dissection for early gastric cancer with undifferentiated histology: could we extend the criteria beyond? Surg Endosc 27(12):4656–4662. doi: 10.1007/s00464-013-3099-9 CrossRefPubMedGoogle Scholar
  29. 29.
    Lee T, Tanaka H, Ohira M, Okita Y, Yoshii M, Sakurai K, Toyokawa T, Kubo N, Muguruma K, Tanaka S, Ohsawa M, Hirakawa K (2014) Clinical impact of the extent of lymph node micrometastasis in undifferentiated-type early gastric cancer. Int Soc Cell 86(4):244–252. doi: 10.1159/000358803 Google Scholar
  30. 30.
    Gotoda T (2007) Endoscopic resection of early gastric cancer. Gastric Cancer 10(1):1–11. doi: 10.1007/s10120-006-0408-1 CrossRefPubMedGoogle Scholar
  31. 31.
    Li C, Kim S, Lai JF, Oh SJ, Hyung WJ, Choi WH, Choi SH, Zhu ZG, Noh SH (2008) Risk factors for lymph node metastasis in undifferentiated early gastric cancer. Ann Surg Oncol 15(3):764–769. doi: 10.1245/s10434-007-9707-y CrossRefPubMedGoogle Scholar
  32. 32.
    Hirasawa T, Gotoda T, Miyata S, Kato Y, Shimoda T, Taniguchi H, Fujisaki J, Sano T, Yamaguchi T (2009) Incidence of lymph node metastasis and the feasibility of endoscopic resection for undifferentiated-type early gastric cancer. Gastric Cancer 12(3):148–152. doi: 10.1007/s10120-009-0515-x CrossRefPubMedGoogle Scholar
  33. 33.
    Kim JH, Kim YH, Jung da H, Jeon HH, Lee YC, Lee H, Lee SK, Park JC, Shin SK, Youn YH, Park H (2014) Follow-up outcomes of endoscopic resection for early gastric cancer with undifferentiated histology. Surg Endosc 28(9):2627–2633. doi: 10.1007/s00464-014-3514-x CrossRefPubMedGoogle Scholar
  34. 34.
    Inokuchi Y, Kobayashi M, Kudo K, Yamada H, Inoue S, Nishimura K, Nakayama N, Motohashi O (2015) Outcomes and precautions of endoscopic submucosal dissection for undifferentiated-type early gastric cancer. Therapeut Adv Gastroenterol 8(5):255–262. doi: 10.1177/1756283x15582139 CrossRefGoogle Scholar
  35. 35.
    Kim JH, Lee YC, Kim H, Song KH, Lee SK, Cheon JH, Kim H, Hyung WJ, Noh SH, Kim CB, Chung JB (2009) Endoscopic resection for undifferentiated early gastric cancer. Gastrointest Endosc 69(4):e1–e9. doi: 10.1016/j.gie.2008.10.040 CrossRefPubMedGoogle Scholar
  36. 36.
    Chon HJ, Hyung WJ, Kim C, Park S, Kim JH, Park CH, Ahn JB, Kim H, Chung HC, Rha SY, Noh SH, Jeung HC (2016) Differential prognostic implications of gastric signet ring cell carcinoma: stage adjusted analysis from a single high-volume center in Asia. Ann Surg. doi: 10.1097/sla.0000000000001793 Google Scholar
  37. 37.
    Lee JH, Kim JG, Jung HK, Kim JH, Jeong WK, Jeon TJ, Kim JM, Kim YI, Ryu KW, Kong SH, Kim HI, Jung HY, Kim YS, Zang DY, Cho JY, Park JO, Lim do H, Jung ES, Ahn HS, Kim HJ (2014) Synopsis on clinical practice guideline of gastric cancer in Korea: an evidence-based approach. Korean J Gastroenterol 63(2):66–81CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Jun Chul Park
    • 1
    Email author
  • Yong Kang Lee
    • 1
  • Soon Young Kim
    • 1
  • Yunho Roh
    • 2
  • Kyu Yeon Hahn
    • 1
  • Sung Kwan Shin
    • 1
  • Sang Kil Lee
    • 1
  • Yong Chan Lee
    • 1
  • Hyoung-Il Kim
    • 3
  • Jae-Ho Cheong
    • 3
  • Woo Jin Hyung
    • 3
  • Sung Hoon Noh
    • 3
  1. 1.Department of Internal Medicine and Institute of GastroenterologyYonsei University College of MedicineSeoulSouth Korea
  2. 2.Department of Biostatistics Collaboration UnitYonsei University College of MedicineSeoulSouth Korea
  3. 3.Department of SurgeryYonsei University College of MedicineSeoulSouth Korea

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