Download PDF
Endoscopy 2019; 51(04): 298-306
DOI: 10.1055/a-0732-5317
Original article
© Georg Thieme Verlag KG Stuttgart · New York

Long-term follow-up after endoscopic resection for superficial esophageal squamous cell carcinoma: a multicenter Western study

Arthur Berger   *
1   Department of Hepatology and Gastroenterology, Angers University, Angers Teaching Hospital, Angers, France
,
Gabriel Rahmi   *
2   Department of Gastroenterology, Georges Pompidou European Hospital, Paris, France
,
Guillaume Perrod
2   Department of Gastroenterology, Georges Pompidou European Hospital, Paris, France
,
Mathieu Pioche
3   Department of Hepatology and Gastroenterology, Lyon 1 University Claude Bernard, Edouard Herriot hospital, Lyon, France
,
Jean-Marc Canard
2   Department of Gastroenterology, Georges Pompidou European Hospital, Paris, France
4   Department of Hepatogastroenterology, Trocadero Private Hospital, Paris, France
,
Elodie Cesbron-Métivier
1   Department of Hepatology and Gastroenterology, Angers University, Angers Teaching Hospital, Angers, France
,
Jérôme Boursier
1   Department of Hepatology and Gastroenterology, Angers University, Angers Teaching Hospital, Angers, France
,
Elia Samaha
2   Department of Gastroenterology, Georges Pompidou European Hospital, Paris, France
,
Ariane Vienne
2   Department of Gastroenterology, Georges Pompidou European Hospital, Paris, France
,
Vincent Lépilliez
5   Department of Hepatogastroenterology, Mermoz Private Hospital, Lyon, France
,
Christophe Cellier
2   Department of Gastroenterology, Georges Pompidou European Hospital, Paris, France
› Author Affiliations
Further Information

Publication History

submitted 26 November 2017

accepted after revision 25 July 2018

Publication Date:
27 September 2018 (online)

Also available at
    Permissions and Reprints

Referred to by:

Video Comment on Arthur Berger et al.Endoscopy 2019; 51(04): v5-v5
DOI: 10.1055/a-0806-2564

Referred to by:

Evolution of endoscopic resection for early esophageal squamous cell carcinoma in Western countriesEndoscopy 2019; 51(04): 296-297
DOI: 10.1055/a-0790-8472

Abstract

Background Endoscopic mucosal resection (EMR) and endoscopic submucosal dissection (ESD) are the first-line treatments for superficial esophageal squamous cell carcinoma (SCC). This study aimed to compare long-term clinical outcome and oncological clearance between EMR and ESD for the treatment of superficial esophageal SCC.

Methods We conducted a retrospective multicenter study in five French tertiary care hospitals. Patients treated by EMR or ESD for histologically proven superficial esophageal SCC were included consecutively.

Results Resection was performed for 148 tumors (80 EMR, 68 ESD) in 132 patients. The curative resection rate was 21.3 % in the EMR group and 73.5 % in the ESD group (P < 0.001). The recurrence rate was 23.7 % in the EMR group and 2.9 % in the ESD group (P = 0.002). The 5-year recurrence-free survival rate was 73.4 % in the EMR group and 95.2 % in the ESD group (P = 0.002). Independent factors for cancer recurrence were resection by EMR (hazard ratio [HR] 16.89, P = 0.01), tumor infiltration depth ≥ m3 (HR 3.28, P = 0.02), no complementary treatment by chemoradiotherapy (HR 7.04, P = 0.04), and no curative resection (HR 11.75, P = 0.01). Risk of metastasis strongly increased in patients with tumor infiltration depth ≥ m3, and without complementary chemoradiotherapy (P = 0.02).

Conclusion Endoscopic resection of superficial esophageal SCC was safe and efficient. Because it was associated with an increased recurrence-free survival rate, ESD should be preferred over EMR. For tumors with infiltration depths ≥ m3, chemoradiotherapy reduced the risk of nodal or distal metastasis.

* These authors contributed equally to this work.


Supplementary Table e2, Table e5, Table e6, Fig. e3 and Fig. e4

 

  • References

  • 1 Torre LA, Bray F, Siegel RL. et al. Global cancer statistics, 2012. CA Cancer J Clin 2015; 65: 87-108
    CrossrefPubMedGoogle Scholar
  • 2 Arnold M, Soerjomataram I, Ferlay J. et al. Global incidence of oesophageal cancer by histological subtype in 2012. Gut 2015; 64: 381-387
    CrossrefPubMedGoogle Scholar
  • 3 Bollschweiler E, Baldus SE, Schröder W. et al. High rate of lymph-node metastasis in submucosal esophageal squamous-cell carcinomas and adenocarcinomas. Endoscopy 2006; 38: 149-156
    Article in Thieme ConnectPubMedGoogle Scholar
  • 4 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
    CrossrefPubMedGoogle Scholar
  • 5 Tajima Y, Nakanishi Y, Tachimori Y. et al. Significance of involvement by squamous cell carcinoma of the ducts of esophageal submucosal glands. Analysis of 201 surgically resected superficial squamous cell carcinomas. Cancer 2000; 89: 248-254
    CrossrefPubMedGoogle Scholar
  • 6 Fuchs HF, Harnsberger CR, Broderick RC. et al. Mortality after esophagectomy is heavily impacted by center volume: retrospective analysis of the Nationwide Inpatient Sample. Surg Endosc 2017; 31: 2491-2497
    CrossrefPubMedGoogle Scholar
  • 7 Shimizu Y, Kato M, Yamamoto J. et al. EMR combined with chemoradiotherapy: a novel treatment for superficial esophageal squamous-cell carcinoma. Gastrointest Endosc 2004; 59: 199-204
    CrossrefPubMedGoogle Scholar
  • 8 Ishihara R, Iishi H, Takeuchi Y. et al. Local recurrence of large squamous-cell carcinoma of the esophagus after endoscopic resection. Gastrointest Endosc 2008; 67: 799-804
    CrossrefPubMedGoogle Scholar
  • 9 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
    CrossrefPubMedGoogle Scholar
  • 10 Guo H-M, Zhang X-Q, Chen M. et al. Endoscopic submucosal dissection vs endoscopic mucosal resection for superficial esophageal cancer. World J Gastroenterol 2014; 20: 5540-5547
    CrossrefPubMedGoogle Scholar
  • 11 Pioche M, Mais L, Guillaud O. et al. Endoscopic submucosal tunnel dissection for large esophageal neoplastic lesions. Endoscopy 2013; 45: 1032-1034
    Article in Thieme ConnectPubMedGoogle Scholar
  • 12 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
    Article in Thieme ConnectPubMedGoogle Scholar
  • 13 Conroy T, Piessen G, Tougeron D. et al. Cancer de l’œsophage. Thésaurus Natl Cancérologie Dig; 2016 Available at: https://www.snfge.org/sites/default/files/SNFGE/TNCD/tncd_chap-1-cancer-oesophage_2016-09-23.pdf
    PubMedGoogle Scholar
  • 14 Pech O, Gossner L, May A. et al. Endoscopic resection of superficial esophageal squamous-cell carcinomas: Western experience. Am J Gastroenterol 2004; 99: 1226-1232
    CrossrefPubMedGoogle Scholar
  • 15 Katada C, Muto M, Manabe T. et al. Local recurrence of squamous-cell carcinoma of the esophagus after EMR. Gastrointest Endosc 2005; 61: 219-225
    CrossrefPubMedGoogle Scholar
  • 16 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
    CrossrefPubMedGoogle Scholar
  • 17 Wang Z, Lu H, Wu L. et al. Long-term outcomes of endoscopic multiband mucosectomy for early esophageal squamous cell neoplasia: a retrospective, single-center study. Gastrointest Endosc 2016; 84: 893-899
    CrossrefPubMedGoogle Scholar
  • 18 Jiang D, Li X, Wang H. et al. A retrospective study of endoscopic resection for 368 patients with early esophageal squamous cell carcinoma or precancerous lesions. Surg Endosc 2017; 31: 2122-2130
    CrossrefPubMedGoogle Scholar
  • 19 Tsujii Y, Nishida T, Nishiyama O. et al. Clinical outcomes of endoscopic submucosal dissection for superficial esophageal neoplasms: a multicenter retrospective cohort study. Endoscopy 2015; 47: 775-783
    Article in Thieme ConnectPubMedGoogle Scholar
  • 20 Joo DC, Kim GH, Park DY. et al. Long-term outcome after endoscopic submucosal dissection in patients with superficial esophageal squamous cell carcinoma: a single-center study. Gut Liver 2014; 8: 612-618
    CrossrefPubMedGoogle Scholar
  • 21 Probst A, Aust D, Märkl B. et al. Early esophageal cancer in Europe: endoscopic treatment by endoscopic submucosal dissection. Endoscopy 2014; 47: 113-121
    Article in Thieme ConnectPubMedGoogle Scholar
  • 22 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
    CrossrefPubMedGoogle Scholar
  • 23 Qumseya B, Panossian AM, Rizk C. et al. Predictors of esophageal stricture formation post endoscopic mucosal resection. Clin Endosc 2014; 47: 155-161
    CrossrefPubMedGoogle Scholar
  • 24 Chung A, Bourke MJ, Hourigan LF. et al. Complete Barrett’s excision by stepwise endoscopic resection in short-segment disease: long term outcomes and predictors of stricture. Endoscopy 2011; 43: 1025-1032
    Article in Thieme ConnectPubMedGoogle Scholar
  • 25 Song BG, Min YW, Lee JH. et al. Efficacy and safety of endoscopic submucosal dissection in elderly patients with esophageal squamous cell carcinoma. Surg Endosc 2017; 31: 3905-3911
    CrossrefPubMedGoogle Scholar
  • 26 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
    CrossrefPubMedGoogle Scholar
  • 27 Mizumoto T, Hiyama T, Oka S. et al. Diagnosis of superficial esophageal squamous cell carcinoma invasion depth before endoscopic submucosal dissection. Dis Esophagus 2018; 31 DOI: 10.1093/dote/dox142.
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 29 Li C, Yamashita DT, Hawel JD. et al. Endoscopic mucosal resection versus esophagectomy for intramucosal adenocarcinoma in the setting of Barrett’s esophagus. Surg Endosc 2017; 31: 4211-4216
    CrossrefPubMedGoogle Scholar
  • 30 Kadota T, Yano T, Fujita T. et al. Submucosal invasive depth predicts lymph node metastasis and poor prognosis in submucosal invasive esophageal squamous cell carcinoma. Am J Clin Pathol 2017; 148: 416-426
    CrossrefPubMedGoogle Scholar
  • 31 Dubecz A, Kern M, Solymosi N. et al. Predictors of lymph node metastasis in surgically resected T1 esophageal cancer. Ann Thorac Surg 2015; 99: 1879-1886
    CrossrefPubMedGoogle Scholar
  • 32 Takahashi K, Hashimoto S, Mizuno K-I. et al. Management decision based on lymphovascular involvement leads to favorable outcomes after endoscopic treatment of esophageal squamous cell carcinoma. Endoscopy 2017; 72: 255-264
    PubMedGoogle Scholar
  • 33 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
    CrossrefPubMedGoogle Scholar
  • 34 Yoshii T, Ohkawa S, Tamai S. et al. Clinical outcome of endoscopic mucosal resection for esophageal squamous cell cancer invading muscularis mucosa and submucosal layer: EMR for ESCC with deeper layer. Dis Esophagus 2013; 26: 496-502
    CrossrefPubMedGoogle Scholar
  • 35 Hisano O, Nonoshita T, Hirata H. et al. Additional radiotherapy following endoscopic submucosal dissection for T1a-MM/T1b-SM esophageal squamous cell carcinoma improves locoregional control. Radiat Oncol 2018; 13: 14
    CrossrefPubMedGoogle Scholar