Skip to main content

Advertisement

Log in

Prognostic risk factors associated with esophageal squamous cell carcinoma patients undergoing endoscopic submucosal dissection: a multi-center cohort study

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Long-term outcomes of endoscopic submucosal dissection (ESD) for esophageal squamous cell carcinoma (ESCC) have not been assessed in a large, multicenter cohort. We aimed to evaluate long-term outcomes of ESD for ESCC in a real-world setting.

Methods

We retrospectively recruited 659 patients who underwent ESD for ESCC at ten institutions from January 2007 to December 2015. Of these, 566 patients were analyzed and classified into three groups according to the pathologic invasion depth after ESD: epithelium/lamina propria mucosa (EP/LPM group: 454 patients), muscularis mucosa/submucosa invasion ≤ 200 μm below the inferior margin of the muscularis mucosa (MM/SM1 group: 81 patients), and submucosa invasion > 200 μm below the MM inferior margin (SM2 group: 31 patients).

Results

The 5-year overall survival rates in the EP/LPM, MM/SM1, and SM2 groups were 92.6%, 80.0%, and 62.7%, respectively, while the 5-year disease-specific survival rates were 99.7%, 96.9%, and 88.3%, respectively. Multivariate analyses revealed that the invasion depth, Charlson Comorbidity Index (CCI), and prognostic nutritional index (PNI) were independent prognostic factors. Hazard ratios in the MM/SM1 and SM2 groups were 2.25 (95% confidence interval [CI] 1.04–4.83; P = 0.038) and 3.18 (95% CI 1.08–9.34; P = 0.036), respectively, compared to those in the EP/LPM group, while those for patients with a CCI ≥ 3 and PNI ≤ 47.75 were 3.25 (95% CI 1.79–5.89; P < 0.001) and 2.42 (95% CI 1.26–4.65; P = 0.008), respectively.

Conclusions

This study identified that invasion depth, presence of comorbid diseases and preoperative nutritional status are independent prognostic risk factors associated with ESCC patients undergoing ESD.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Arnold M, Soerjomataram I, Ferlay J, Forman D (2015) Global incidence of oesophageal cancer by histological subtype in 2012. Gut 64:381–387

    Article  Google Scholar 

  2. Abnet CC, Arnold M, Wei WQ (2018) Epidemiology of esophageal squamous cell carcinoma. Gastroenterology 154:360–373

    Article  Google Scholar 

  3. Gupta B, Kumar N (2017) Worldwide incidence, mortality and time trends for cancer of the oesophagus. Eur J Cancer Prev 26:107–118

    Article  Google Scholar 

  4. Tachimori Y, Ozawa S, Numasaki H, Ishihara R, Matsubara H, Muro K, Oyama T, Toh Y, Udagawa H, Uno T (2018) Comprehensive registry of esophageal cancer in Japan, 2011. Esophagus 15:127–152

    Article  Google Scholar 

  5. Oyama T, Tomori A, Hotta K, Morita S, Kominato K, Tanaka M, Miyata Y (2005) Endoscopic submucosal dissection of early esophageal cancer. Clin Gastroenterol Hepatol 3:S67-70

    Article  Google Scholar 

  6. Fujishiro M, Yahagi N, Kakushima N, Kodashima S, Muraki Y, Ono S, Yamamichi N, Tateishi A, Shimizu Y, Oka M, Ogura K, Kawabe T, Ichinose M, Omata M (2006) Endoscopic submucosal dissection of esophageal squamous cell neoplasms. Clin Gastroenterol Hepatol 4:688–694

    Article  Google Scholar 

  7. Ishihara R, Iishi H, Uedo N, Takeuchi Y, Yamamoto S, Yamada T, Masuda E, Higashino K, Kato M, Narahara H, Tatsuta M (2008) Comparison of EMR and endoscopic submucosal dissection for en bloc resection of early esophageal cancers in Japan. Gastrointest Endosc 68:1066–1072

    Article  Google Scholar 

  8. Takahashi H, Arimura Y, Masao H, Okahara S, Tanuma T, Kodaira J, Kagaya H, Shimizu Y, Hokari K, Tsukagoshi H, Shinomura Y, Fujita M (2010) 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 72(255–264):264.e251–252

    Google Scholar 

  9. Yamashina T, Ishihara R, Nagai K, Matsuura N, Matsui F, Ito T, Fujii M, Yamamoto S, Hanaoka N, Takeuchi Y, Higashino K, Uedo N, Iishi H (2013) Long-term outcome and metastatic risk after endoscopic resection of superficial esophageal squamous cell carcinoma. Am J Gastroenterol 108:544–551

    Article  Google Scholar 

  10. Nakagawa K, Koike T, Iijima K, Shinkai H, Hatta W, Endo H, Ara N, Uno K, Asano N, Imatani A, Shimosegawa T (2014) Comparison of the long-term outcomes of endoscopic resection for superficial squamous cell carcinoma and adenocarcinoma of the esophagus in Japan. Am J Gastroenterol 109:348–356

    Article  Google Scholar 

  11. Berger A, Rahmi G, Perrod G, Pioche M, Canard JM, Cesbron-Metivier E, Boursier J, Samaha E, Vienne A, Lepilliez V, Cellier C (2019) Long-term follow-up after endoscopic resection for superficial esophageal squamous cell carcinoma: a multicenter Western study. Endoscopy 51:298–306

    Article  Google Scholar 

  12. Ono S, Fujishiro M, Niimi K, Goto O, Kodashima S, Yamamichi N, Omata M (2009) Long-term outcomes of endoscopic submucosal dissection for superficial esophageal squamous cell neoplasms. Gastrointest Endosc 70:860–866

    Article  Google Scholar 

  13. Repici A, Hassan C, Carlino A, Pagano N, Zullo A, Rando G, Strangio G, Romeo F, Nicita R, Rosati R, Malesci A (2010) Endoscopic submucosal dissection in patients with early esophageal squamous cell carcinoma: results from a prospective Western series. Gastrointest Endosc 71:715–721

    Article  Google Scholar 

  14. Joo DC, Kim GH, Park DY, Jhi JH, Song GA (2014) Long-term outcome after endoscopic submucosal dissection in patients with superficial esophageal squamous cell carcinoma: a single-center study. Gut and liver 8:612–618

    Article  Google Scholar 

  15. Tsujii Y, Nishida T, Nishiyama O, Yamamoto K, Kawai N, Yamaguchi S, Yamada T, Yoshio T, Kitamura S, Nakamura T, Nishihara A, Ogiyama H, Nakahara M, Komori M, Kato M, Hayashi Y, Shinzaki S, Iijima H, Michida T, Tsujii M, Takehara T (2015) Clinical outcomes of endoscopic submucosal dissection for superficial esophageal neoplasms: a multicenter retrospective cohort study. Endoscopy 47:775–783

    Article  Google Scholar 

  16. Nagami Y, Ominami M, Shiba M, Minamino H, Fukunaga S, Kameda N, Sugimori S, Machida H, Tanigawa T, Yamagami H, Watanabe T, Tominaga K, Fujiwara Y, Arakawa T (2017) The five-year survival rate after endoscopic submucosal dissection for superficial esophageal squamous cell neoplasia. Dig Liver Dis 49:427–433

    Article  Google Scholar 

  17. Ohashi S, Miyamoto S, Kikuchi O, Goto T, Amanuma Y, Muto M (2015) Recent advances from basic and clinical studies of esophageal squamous cell carcinoma. Gastroenterology 149:1700–1715

    Article  Google Scholar 

  18. Kitagawa Y, Uno T, Oyama T, Kato K, Kato H, Kawakubo H, Kawamura O, Kusano M, Kuwano H, Takeuchi H, Toh Y, Doki Y, Naomoto Y, Nemoto K, Booka E, Matsubara H, Miyazaki T, Muto M, Yanagisawa A, Yoshida M (2019) Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal Society: part 1. Esophagus 16:1–24

    Article  Google Scholar 

  19. Secretan B, Straif K, Baan R, Grosse Y, El Ghissassi F, Bouvard V, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V (2009) A review of human carcinogens—Part E: tobacco, areca nut, alcohol, coal smoke, and salted fish. Lancet Oncol 10:1033–1034

    Article  Google Scholar 

  20. Ishihara R, Tanaka H, Iishi H, Takeuchi Y, Higashino K, Uedo N, Tatsuta M, Yano M, Ishiguro S (2008) Long-term outcome of esophageal mucosal squamous cell carcinoma without lymphovascular involvement after endoscopic resection. Cancer 112:2166–2172

    Article  Google Scholar 

  21. Sato Y, Motoyama S, Maruyama K, Okuyama M, Ogawa J (2005) A second malignancy is the major cause of death among thoracic squamous cell esophageal cancer patients negative for lymph node involvement. J Am Coll Surg 201:188–193

    Article  Google Scholar 

  22. Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383

    Article  CAS  Google Scholar 

  23. Onodera T, Goseki N, Kosaki G (1984) Prognostic nutritional index in gastrointestinal surgery of malnourished cancer patients. Nihon Geka Gakkai zasshi 85:1001–1005

    CAS  PubMed  Google Scholar 

  24. Forrest LM, McMillan DC, McArdle CS, Angerson WJ, Dunlop DJ (2003) Evaluation of cumulative prognostic scores based on the systemic inflammatory response in patients with inoperable non-small-cell lung cancer. Br J Cancer 89:1028–1030

    Article  CAS  Google Scholar 

  25. Toiyama Y, Miki C, Inoue Y, Tanaka K, Mohri Y, Kusunoki M (2011) Evaluation of an inflammation-based prognostic score for the identification of patients requiring postoperative adjuvant chemotherapy for stage II colorectal cancer. Exp Ther Med 2:95–101

    Article  Google Scholar 

  26. Fairclough E, Cairns E, Hamilton J, Kelly C (2009) Evaluation of a modified early warning system for acute medical admissions and comparison with C-reactive protein/albumin ratio as a predictor of patient outcome. Clin Med (Lond) 9:30–33

    Article  Google Scholar 

  27. Halazun KJ, Hardy MA, Rana AA, Woodland DC, Luyten EJ, Mahadev S, Witkowski P, Siegel AB, Brown Jr. RS, Emond JC, (2009) Negative impact of neutrophil-lymphocyte ratio on outcome after liver transplantation for hepatocellular carcinoma. Ann Surg 250:141–151

    Article  Google Scholar 

  28. Nakajo K, Abe S, Oda I, Ishihara R, Tanaka M, Yoshio T, Katada C, Yano T (2019) Impact of the Charlson Comorbidity Index on the treatment strategy and survival in elderly patients after non-curative endoscopic submucosal dissection for esophageal squamous cell carcinoma: a multicenter retrospective study. J Gastroenterol 54:871–880

    Article  CAS  Google Scholar 

  29. Takahashi K, Hashimoto S, Mizuno KI, Kobayashi T, Tominaga K, Sato H, Kohisa J, Ikarashi S, Hayashi K, Takeuchi M, Yokoyama J, Kawai H, Sato Y, Kobayashi M, Terai S (2018) Management decision based on lymphovascular involvement leads to favorable outcomes after endoscopic treatment of esophageal squamous cell carcinoma. Endoscopy 50:662–670

    Article  Google Scholar 

  30. Kudou M, Shiozaki A, Fujiwara H, Konishi H, Shoda K, Arita T, Kosuga T, Morimura R, Murayama Y, Kuriu Y, Ikoma H, Kubota T, Nakanishi M, Okamoto K, Dohi O, Konishi H, Naito Y, Otsuji E (2017) Efficacy of additional surgical resection after endoscopic submucosal dissection for superficial esophageal cancer. Anticancer Res 37:5301–5307

    PubMed  Google Scholar 

  31. Suzuki G, Yamazaki H, Aibe N, Masui K, Sasaki N, Shimizu D, Kimoto T, Shiozaki A, Dohi O, Fujiwara H, Ishikawa T, Konishi H, Naito Y, Otsuji E, Yamada K (2018) Endoscopic submucosal dissection followed by chemoradiotherapy for superficial esophageal cancer: choice of new approach. Radiat Oncol 13:246

    Article  CAS  Google Scholar 

  32. Slaughter DP, Southwick HW, Smejkal W (1953) Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer 6:963–968

    Article  CAS  Google Scholar 

  33. Minashi K, Nihei K, Mizusawa J, Takizawa K, Yano T, Ezoe Y, Tsuchida T, Ono H, Iizuka T, Hanaoka N, Oda I, Morita Y, Tajika M, Fujiwara J, Yamamoto Y, Katada C, Hori S, Doyama H, Oyama T, Nebiki H, Amagai K, Kubota Y, Nishimura K, Kobayashi N, Suzuki T, Hirasawa K, Takeuchi T, Fukuda H, Muto M (2019) Efficacy of endoscopic resection and selective chemoradiotherapy for stage I esophageal squamous cell carcinoma. Gastroenterology 157(2):382–390

    Article  Google Scholar 

  34. Vashist YK, Loos J, Dedow J, Tachezy M, Uzunoglu G, Kutup A, Yekebas EF, Izbicki JR (2011) Glasgow Prognostic Score is a predictor of perioperative and long-term outcome in patients with only surgically treated esophageal cancer. Ann Surg Oncol 18:1130–1138

    Article  Google Scholar 

  35. Xu XL, Yu HQ, Hu W, Song Q, Mao WM (2015) A novel inflammation-based prognostic score, the C-reactive protein/albumin ratio predicts the prognosis of patients with operable esophageal squamous cell carcinoma. PLoS ONE 10:e0138657

    Article  Google Scholar 

  36. Sharaiha RZ, Halazun KJ, Mirza F, Port JL, Lee PC, Neugut AI, Altorki NK, Abrams JA (2011) Elevated preoperative neutrophil: lymphocyte ratio as a predictor of postoperative disease recurrence in esophageal cancer. Ann Surg Oncol 18:3362–3369

    Article  Google Scholar 

Download references

Acknowledgements

We thank all members of the KESG. We are also grateful to the following investigators: Tsugitaka Ishida, Yuka Azuma, Hiroaki Kitae, Shinya Matsumura, Kazuyuki Ogita, Shun Takayama, Naoki Mizuno (Kyoto Prefectural University of Medicine), and Takahiro Nakano (Japanese Red Cross Society Kyoto Daiichi Hospital) for their help with the data collection.

Funding

This work was partly supported by Grants-in-Aid for JFE (The Japanese Foundation for Research and Promotion of Endoscopy) Grant to Osamu Dohi and Cancer Research Grant from Kyoto Preventive Medical Center to Naoto Iwai.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Osamu Dohi.

Ethics declarations

Disclosures

Naoto Iwai, Osamu Dohi, Shinya Yamada, Akihito Harusato, Ryusuke Horie, Takeshi Yasuda, Nobuhisa Yamada, Yusuke Horii, Atsushi Majima, Keika Zen, Hiroyuki Kimura, Nobuaki Yagi, Yuji Naito, and Yoshito Itoh have no conflicts of interest or financial ties to disclose.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iwai, N., Dohi, O., Yamada, S. et al. Prognostic risk factors associated with esophageal squamous cell carcinoma patients undergoing endoscopic submucosal dissection: a multi-center cohort study. Surg Endosc 36, 2279–2289 (2022). https://doi.org/10.1007/s00464-021-08502-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-021-08502-1

Keywords

Navigation