Skip to main content

Advertisement

SpringerLink
Log in

Is Additional Surgery Always Sufficient for Preventing Recurrence After Endoscopic Submucosal Dissection with Curability C-2 for Early Gastric Cancer?

  • Gastrointestinal Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

When a lesion does not meet the curative criteria of endoscopic submucosal dissection (ESD) for early gastric cancer (EGC), referred to as non-curative resection or curability C-2 in the guidelines, an additional surgery is the standard therapy because of the risk of lymph node metastasis (LNM).

Objective

This study aimed to identify high-risk patients for recurrence after additional surgery for curability C-2 ESD of EGC.

Methods

This multicenter retrospective cohort study enrolled 1064 patients who underwent additional surgery after curability C-2 ESD for EGC. We evaluated the recurrence rate and the risk factors for recurrence after additional surgery in these patients.

Results

The 5-year recurrence rate after additional surgery was 1.3%. Multivariate Cox analysis revealed that the independent risk factors for recurrence after additional surgery were LNM (hazard ratio [HR] 32.47; p < 0.001) and vascular invasion (HR 4.75; p = 0.014). Moreover, patients with both LNM and vascular invasion had a high rate of recurrence after additional surgery (24.6% in 5 years), with a high HR (119.32) compared with those with neither LNM nor vascular invasion. Among patients with no vascular invasion, a high rate of recurrence was observed in those with N2/N3 disease according to the American Joint Committee on Cancer TNM staging system (27.3% in 5 years), in contrast with no recurrence in those with N1 disease.

Conclusions

Patients with both LNM (N1–N3) and vascular invasion, as well as those with N2/N3 disease but no vascular invasion, would be candidates for adjuvant chemotherapy after additional surgery for curability C-2 ESD of EGC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T, et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy. 2015;47:829–54.

    Article  PubMed  Google Scholar 

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

  3. 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.

    Article  PubMed  Google Scholar 

  4. Japanese Gastric Cancer Association. Gastric cancer treatment guideline. 5th ed. [in Japanese]. Tokyo: Kanehara; 2018.

  5. Ito H, Inoue H, Ikeda H, et al. Surgical outcomes and clinicopathological characteristics of patients who underwent potentially noncurative endoscopic resection for gastric cancer: a report of a single-center experience. Gastroenterol Res Pract. 2013;2013:427405.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Yang HJ, Kim SG, Lim JH, et al. Predictors of lymph node metastasis in patients with non-curative endoscopic resection of early gastric cancer. Surg Endosc. 2015;29:1145–55.

    Article  PubMed  Google Scholar 

  7. Kikuchi S, Kuroda S, Nishizaki M, et al. Management of early gastric cancer that meet the indication for radical lymph node dissection following endoscopic resection: a retrospective cohort analysis. BMC Surg. 2017;17:72.

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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;31:1607–16.

    Article  PubMed  Google Scholar 

  9. 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;20:679–89.

    Article  PubMed  Google Scholar 

  10. 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;30:2404–14.

    Article  PubMed  Google Scholar 

  11. 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;24:3353–60.

    Article  PubMed  Google Scholar 

  12. 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;52:175–84.

    Article  PubMed  Google Scholar 

  13. 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;112:874–81.

    Article  Google Scholar 

  14. 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;21:481–9.

    Article  CAS  PubMed  Google Scholar 

  15. Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 2011;14:101–12.

  16. Saka M, Katai H, Fukagawa T, Nijjar R, Sano T. Recurrence in early gastric cancer with lymph node metastasis. Gastric Cancer. 2008;11:214–8.

    Article  PubMed  Google Scholar 

  17. Youn HG, An JY, Choi MG, Noh JH, Sohn TS, Kim S. Recurrence after curative resection of early gastric cancer. Ann Surg Oncol. 2010;17:448–54.

    Article  PubMed  Google Scholar 

  18. Kim SM, An JY, Lee J, Sohn TS, Kim S. Adjuvant chemotherapy versus chemoradiotherapy versus surgery alone for early gastric cancer with one or two lymph node metastasis. Ann Surg Oncol. 2018;25:1616–24.

    Article  PubMed  Google Scholar 

  19. Sano T, Sasako M, Kinoshita T, Maruyama K. Recurrence of early gastric cancer. Follow-up of 1475 patients and review of the Japanese literature. Cancer. 1993;72:3174–8.

    Article  CAS  PubMed  Google Scholar 

  20. Lee HJ, Kim YH, Kim WH, et al. Clinicopathological analysis for recurrence of early gastric cancer. Jpn J Clin Oncol. 2003;33:209–14.

    Article  PubMed  Google Scholar 

  21. Ikeda Y, Saku M, Kishihara F, Maehara Y. Effective follow-up for recurrence or a second primary cancer in patients with early gastric cancer. Br J Surg. 2005;92:235–9.

    Article  CAS  PubMed  Google Scholar 

  22. Japanese Gastric Cancer Association Registration Committee, Maruyama K, Kaminishi M, et al. Gastric cancer treated in 1991 in Japan: data analysis of nationwide registry. Gastric Cancer. 2006;9:51–66.

  23. Isobe Y, Nashimoto A, Akazawa K, et al. Gastric cancer treatment in Japan: 2008 annual report of the JGCA nationwide registry. Gastric Cancer. 2011;14:301–16.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ishida M, Morita S, Saka M, Fukagawa T, Taniguchi H, Katai H. Metachronous liver metastasis from early gastric cancer. J Gastrointest Surg. 2012;16:837–41.

    Article  PubMed  Google Scholar 

  25. Nashimoto A, Akazawa K, Isobe Y, et al. Gastric cancer treated in 2002 in Japan: 2009 annual report of the JGCA nationwide registry. Gastric Cancer. 2013;16:1–27.

    Article  PubMed  Google Scholar 

  26. Sakuramoto S, Sasako M, Yamaguchi T, et al. Adjuvant chemotherapy for gastric cancer with S-1, an oral fluoropyrimidine. N Engl J Med. 2007;357:1810–20.

    Article  CAS  PubMed  Google Scholar 

  27. National Comprehensive Cancer Network (NCCN). Clinical Practice Guidelines in Oncology (NCCN guidelines). Gastric Cancer. Version 1.2019. https://www.nccn.org/professionals/physician_gls/pdf/gastric.pdf. Accessed 4 May 2019.

Download references

Acknowledgment

The authors thank Hiroyuki Ono (Shizuoka Cancer Center), Koki Nakamura (Hiroshima City Hospital), Naohiko Harada (National Hospital Organization Kyushu Medical Center), Yasumasa Hara (Toyama Prefectural Central Hospital), and Kohei Yamanouchi (Saga Medical School) for the enrollment of patients and data collection.

Author information

Authors and Affiliations

  1. Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Japan

    Waku Hatta MD, PhD, Tooru Shimosegawa MD, PhD & Atsushi Masamune MD, PhD

  2. Division of Gastroenterology and Hepatology, Department of Medicine, Nihon University School of Medicine, Tokyo, Japan

    Takuji Gotoda MD, PhD, FASGE, FACG, FRCP & Mitsuru Esaki MD

  3. Division of Endoscopy, Saku Central Hospital Advanced Care Center, Saku, Japan

    Tsuneo Oyama MD, PhD & Akiko Takahashi MD

  4. Division of Endoscopy, Shizuoka Cancer Center, Shizuoka, Japan

    Noboru Kawata MD

  5. Department of Gastroenterology and Metabolism, Graduate School of Biomedical Sciences, Hiroshima University, Hiroshima, Japan

    Shiro Oka MD, PhD

  6. Department of Gastroenterology, Toranomon Hospital, Tokyo, Japan

    Shu Hoteya MD, PhD

  7. Department of Endoscopy, Hiroshima City Hospital, Hiroshima, Japan

    Masahiro Nakagawa MD, PhD

  8. Department of Internal Medicine, Niigata Prefectural Central Hospital, Joetsu, Japan

    Masaaki Hirano MD, PhD

  9. Department of Gastroenterology, Kitakyushu Municipal Medical Center, Kitakyushu, Japan

    Mitsuru Esaki MD

  10. Department of Internal Medicine, Toyama Prefectural Central Hospital, Toyama, Japan

    Mitsuru Matsuda MD, PhD

  11. Department of Gastroenterology and Hepatology, Nagasaki University Hospital, Nagasaki, Japan

    Ken Ohnita MD, PhD

  12. Department of Internal Medicine and Gastrointestinal Endoscopy, Saga Medical School, Saga, Japan

    Ryo Shimoda MD, PhD

  13. Department of Gastroenterology and Endocrinology and Metabolism, Nara Medical University, Nara, Japan

    Motoyuki Yoshida MD

  14. Department of Gastroenterology and Hepatology, Kyoto Prefectural University of Medicine, Kyoto, Japan

    Osamu Dohi MD, PhD

  15. Department of Gastroenterology, Gifu University Graduate School of Medicine, Gifu, Japan

    Jun Takada MD, PhD

  16. Department of Gastroenterology, Shinshu University School of Medicine, Matsumoto, Japan

    Keiko Tanaka MD

  17. Department of Gastroenterology and Hepatology, Japanese Red Cross Society Kyoto Daiichi Hospital, Kyoto, Japan

    Shinya Yamada MD, PhD

  18. Department of Gastroenterology, Akita City Hospital, Akita, Japan

    Tsuyotoshi Tsuji MD, PhD

  19. Department of Gastroenterology, Osaki Citizen Hospital, Osaki, Japan

    Hirotaka Ito MD, PhD

  20. Division of Gastroenterology, Fukui Prefectural Hospital, Fukui, Japan

    Hiroyuki Aoyagi MD, PhD

  21. Department of Preventive Medicine and Epidemiology, Tohoku Medical Megabank Organization, Sendai, Japan

    Tomohiro Nakamura PhD & Naoki Nakaya PhD

Authors
  1. Waku Hatta MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takuji Gotoda MD, PhD, FASGE, FACG, FRCP
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tsuneo Oyama MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Noboru Kawata MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Akiko Takahashi MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shiro Oka MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shu Hoteya MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Masahiro Nakagawa MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Masaaki Hirano MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Mitsuru Esaki MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mitsuru Matsuda MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ken Ohnita MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Ryo Shimoda MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Motoyuki Yoshida MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Osamu Dohi MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Jun Takada MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Keiko Tanaka MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Shinya Yamada MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Tsuyotoshi Tsuji MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Hirotaka Ito MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Hiroyuki Aoyagi MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Tomohiro Nakamura PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Naoki Nakaya PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Tooru Shimosegawa MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Atsushi Masamune MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takuji Gotoda MD, PhD, FASGE, FACG, FRCP.

Ethics declarations

Disclosures

Waku Hatta, Takuji Gotoda, Tsuneo Oyama, Noboru Kawata, Akiko Takahashi, Shiro Oka, Shu Hoteya, Masahiro Nakagawa, Masaaki Hirano, Mitsuru Esaki, Mitsuru Matsuda, Ken Ohnita, Ryo Shimoda, Motoyuki Yoshida, Osamu Dohi, Jun Takada, Keiko Tanaka, Shinya Yamada, Tsuyotoshi Tsuji, Hirotaka Ito, Hiroyuki Aoyagi, Tomohiro Nakamura, Naoki Nakaya, Tooru Shimosegawa, and Atsushi Masamune have no conflicts of interest and no financial or material support to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hatta, W., Gotoda, T., Oyama, T. et al. Is Additional Surgery Always Sufficient for Preventing Recurrence After Endoscopic Submucosal Dissection with Curability C-2 for Early Gastric Cancer?. Ann Surg Oncol 26, 3636–3643 (2019). https://doi.org/10.1245/s10434-019-07579-2

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-019-07579-2

Search

Navigation