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Published in: Surgical Endoscopy 1/2018

01-01-2018

Clinical implication of endoscopic gross appearance in superficial esophageal squamous carcinoma: revisited

Authors: Cheal Wung Huh, Da Hyun Jung, Jie-Hyun Kim, Dae Won Ma, Young Hoon Youn, Hyojin Park

Published in: Surgical Endoscopy | Issue 1/2018

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Abstract

Background

Standard endoscopic appearance is essential for the diagnosis and treatment of superficial esophageal squamous carcinoma (SESC). The aim of this study was to investigate the association between the endoscopic gross appearance and the clinicopathologic characteristics of SESC.

Methods

We retrospectively analyzed the clinicopathologic characteristics of SESC according to gross endoscopic appearance in 275 patients with SESC that underwent esophagectomy or endoscopic resection (ER).

Results

The proportion of type I or type III gross appearance, and that of types IIa, IIb, or IIc, were 26.2 and 73.8%, respectively. Type I or type III gross appearance was significantly associated with the female sex, submucosal invasion, lymphovascular invasion (LVI), and lymph node metastasis (LNM). In addition, younger age, larger tumor size, higher proportion of circumferential extension, type I or type III endoscopic gross appearance, submucosal invasion, moderate or poorly differentiated carcinoma, and LVI were significantly associated with LNM. Multivariate logistic regression analysis determined that independent predictors of LNM in patients with SESC included endoscopic gross appearance, submucosal invasion, and presence of LVI. Additionally, type I or type III endoscopic gross appearance lesions were more likely to have submucosal invasion than types IIa, IIb, or IIc. Risk factors for submucosal invasion included a gross appearance of type I or type III, moderately or poorly differentiated tumors, and presence of LVI.

Conclusions

We found that SESC clinical features are correlated with the endoscopic appearance. Therefore, we suggest that the endoscopic gross appearance may be a candidate for additive criteria in the indications for ER.
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Literature
1.
go back to reference Li B, Chen H, Xiang J, Zhang Y, Kong Y, Garfield DH, Li H (2013) Prevalence of lymph node metastases in superficial esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg 146(5):1198–1203CrossRefPubMed Li B, Chen H, Xiang J, Zhang Y, Kong Y, Garfield DH, Li H (2013) Prevalence of lymph node metastases in superficial esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg 146(5):1198–1203CrossRefPubMed
2.
go back to reference Shimada H, Nabeya Y, Matsubara H, Okazumi S, Shiratori T, Shimizu T, Aoki T, Shuto K, Akutsu Y, Ochiai T (2006) Prediction of lymph node status in patients with superficial esophageal carcinoma: analysis of 160 surgically resected cancers. Am J Surg 191(2):250–254CrossRefPubMed Shimada H, Nabeya Y, Matsubara H, Okazumi S, Shiratori T, Shimizu T, Aoki T, Shuto K, Akutsu Y, Ochiai T (2006) Prediction of lymph node status in patients with superficial esophageal carcinoma: analysis of 160 surgically resected cancers. Am J Surg 191(2):250–254CrossRefPubMed
3.
go back to reference Spechler SJ (2005) Dysplasia in Barrett’s esophagus: limitations of current management strategies. Am J Gastroenterol 100(4):927–935CrossRefPubMed Spechler SJ (2005) Dysplasia in Barrett’s esophagus: limitations of current management strategies. Am J Gastroenterol 100(4):927–935CrossRefPubMed
4.
go back to reference 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(5):860–866CrossRefPubMed 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(5):860–866CrossRefPubMed
5.
go back to reference Muto M, Minashi K, Yano T, Saito Y, Oda I, Nonaka S, Omori T, Sugiura H, Goda K, Kaise M, Inoue H, Ishikawa H, Ochiai A, Shimoda T, Watanabe H, Tajiri H, Saito D (2010) Early detection of superficial squamous cell carcinoma in the head and neck region and esophagus by narrow band imaging: a multicenter randomized controlled trial. J Clin Oncol 28(9):1566–1572CrossRefPubMedPubMedCentral Muto M, Minashi K, Yano T, Saito Y, Oda I, Nonaka S, Omori T, Sugiura H, Goda K, Kaise M, Inoue H, Ishikawa H, Ochiai A, Shimoda T, Watanabe H, Tajiri H, Saito D (2010) Early detection of superficial squamous cell carcinoma in the head and neck region and esophagus by narrow band imaging: a multicenter randomized controlled trial. J Clin Oncol 28(9):1566–1572CrossRefPubMedPubMedCentral
6.
go back to reference Yoshida T, Inoue H, Usui S, Satodate H, Fukami N, Kudo SE (2004) Narrow-band imaging system with magnifying endoscopy for superficial esophageal lesions. Gastrointest Endosc 59(2):288–295CrossRefPubMed Yoshida T, Inoue H, Usui S, Satodate H, Fukami N, Kudo SE (2004) Narrow-band imaging system with magnifying endoscopy for superficial esophageal lesions. Gastrointest Endosc 59(2):288–295CrossRefPubMed
7.
go back to reference Ebi M, Shimura T, Yamada T, Mizushima T, Itoh K, Tsukamoto H, Tsuchida K, Hirata Y, Murakami K, Kanie H, Nomura S, Iwasaki H, Kitagawa M, Takahashi S, Joh T (2015) Multicenter, prospective trial of white-light imaging alone versus white-light imaging followed by magnifying endoscopy with narrow-band imaging for the real-time imaging and diagnosis of invasion depth in superficial esophageal squamous cell carcinoma. Gastrointest Endosc 81(6):1355–1361 e1352 CrossRefPubMed Ebi M, Shimura T, Yamada T, Mizushima T, Itoh K, Tsukamoto H, Tsuchida K, Hirata Y, Murakami K, Kanie H, Nomura S, Iwasaki H, Kitagawa M, Takahashi S, Joh T (2015) Multicenter, prospective trial of white-light imaging alone versus white-light imaging followed by magnifying endoscopy with narrow-band imaging for the real-time imaging and diagnosis of invasion depth in superficial esophageal squamous cell carcinoma. Gastrointest Endosc 81(6):1355–1361 e1352 CrossRefPubMed
8.
go back to reference Jung DH, Park YM, Kim JH, Lee YC, Youn YH, Park H, Lee SI, Kim JW, Choi SH, Hyung WJ, Noh SH (2013) Clinical implication of endoscopic gross appearance in early gastric cancer: revisited. Surg Endosc 27(10):3690–3695CrossRefPubMed Jung DH, Park YM, Kim JH, Lee YC, Youn YH, Park H, Lee SI, Kim JW, Choi SH, Hyung WJ, Noh SH (2013) Clinical implication of endoscopic gross appearance in early gastric cancer: revisited. Surg Endosc 27(10):3690–3695CrossRefPubMed
9.
go back to reference Soetikno R, Kaltenbach T, Yeh R, Gotoda T (2005) Endoscopic mucosal resection for early cancers of the upper gastrointestinal tract. J Clin Oncol 23(20):4490–4498CrossRefPubMed Soetikno R, Kaltenbach T, Yeh R, Gotoda T (2005) Endoscopic mucosal resection for early cancers of the upper gastrointestinal tract. J Clin Oncol 23(20):4490–4498CrossRefPubMed
10.
go back to reference Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14(2):101–112CrossRef Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14(2):101–112CrossRef
11.
go back to reference Kuwano H, Nishimura Y, Oyama T, Kato H, Kitagawa Y, Kusano M, Shimada H, Takiuchi H, Toh Y, Doki Y, Naomoto Y, Matsubara H, Miyazaki T, Muto M, Yanagisawa A (2015) Guidelines for diagnosis and treatment of carcinoma of the esophagus April 2012 edited by the Japan Esophageal Society. Esophagus 12:1–30CrossRefPubMed Kuwano H, Nishimura Y, Oyama T, Kato H, Kitagawa Y, Kusano M, Shimada H, Takiuchi H, Toh Y, Doki Y, Naomoto Y, Matsubara H, Miyazaki T, Muto M, Yanagisawa A (2015) Guidelines for diagnosis and treatment of carcinoma of the esophagus April 2012 edited by the Japan Esophageal Society. Esophagus 12:1–30CrossRefPubMed
12.
go back to reference Shima I, Sasaguri Y, Kakegawa T, Fujita H, Yamana H, Irie K, Morimatsu M (1994) Treatment for superficial esophageal cancer based on histological features and gross appearance. Int J Oncol 5(2):315–320PubMed Shima I, Sasaguri Y, Kakegawa T, Fujita H, Yamana H, Irie K, Morimatsu M (1994) Treatment for superficial esophageal cancer based on histological features and gross appearance. Int J Oncol 5(2):315–320PubMed
13.
go back to reference Oda I, Abe S, Kusano C, Suzuki H, Nonaka S, Yoshinaga S, Taniguchi H, Shimoda T, Gotoda T (2011) Correlation between endoscopic macroscopic type and invasion depth for early esophagogastric junction adenocarcinomas. Gastric Cancer 14(1):22–27CrossRefPubMed Oda I, Abe S, Kusano C, Suzuki H, Nonaka S, Yoshinaga S, Taniguchi H, Shimoda T, Gotoda T (2011) Correlation between endoscopic macroscopic type and invasion depth for early esophagogastric junction adenocarcinomas. Gastric Cancer 14(1):22–27CrossRefPubMed
14.
go back to reference Moon JY, Kim GH, Kim JH, Kim HH, Ryu KD, Park SO, Lee BE, Song GA (2014) Clinicopathologic factors predicting lymph node metastasis in superficial esophageal squamous cell carcinoma. Scand J Gastroenterol 49(5):589–594CrossRefPubMed Moon JY, Kim GH, Kim JH, Kim HH, Ryu KD, Park SO, Lee BE, Song GA (2014) Clinicopathologic factors predicting lymph node metastasis in superficial esophageal squamous cell carcinoma. Scand J Gastroenterol 49(5):589–594CrossRefPubMed
15.
go back to reference Choi JY, Park YS, Jung HY, Ahn JY, Kim MY, Lee JH, Choi KS, Kim DH, Choi KD, Song HJ, Lee GH, Cho KJ, Kim JH (2011) Feasibility of endoscopic resection in superficial esophageal squamous carcinoma. Gastrointest Endosc 73(5):881–889 889 e881-882 CrossRefPubMed Choi JY, Park YS, Jung HY, Ahn JY, Kim MY, Lee JH, Choi KS, Kim DH, Choi KD, Song HJ, Lee GH, Cho KJ, Kim JH (2011) Feasibility of endoscopic resection in superficial esophageal squamous carcinoma. Gastrointest Endosc 73(5):881–889 889 e881-882 CrossRefPubMed
16.
go back to reference (2003) The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc 58(6 Suppl):S3-43 (2003) The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc 58(6 Suppl):S3-43
17.
go back to reference Ajani JA, Barthel JS, Bentrem DJ, D’Amico TA, Das P, Denlinger CS, Fuchs CS, Gerdes H, Glasgow RE, Hayman JA (2011) Esophageal and esophagogastric junction cancers. J Natl Compr Canc Netw 9(8):830–887CrossRefPubMed Ajani JA, Barthel JS, Bentrem DJ, D’Amico TA, Das P, Denlinger CS, Fuchs CS, Gerdes H, Glasgow RE, Hayman JA (2011) Esophageal and esophagogastric junction cancers. J Natl Compr Canc Netw 9(8):830–887CrossRefPubMed
18.
go back to reference Endoscopic Classification Review Group (2005) Update on the paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy 37(6):570–578CrossRef Endoscopic Classification Review Group (2005) Update on the paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy 37(6):570–578CrossRef
19.
go back to reference Rampado S, Bocus P, Battaglia G, Ruol A, Portale G, Ancona E (2008) Endoscopic ultrasound: accuracy in staging superficial carcinomas of the esophagus. Ann Thorac Surg 85(1):251–256CrossRefPubMed Rampado S, Bocus P, Battaglia G, Ruol A, Portale G, Ancona E (2008) Endoscopic ultrasound: accuracy in staging superficial carcinomas of the esophagus. Ann Thorac Surg 85(1):251–256CrossRefPubMed
20.
go back to reference Vazquez-Sequeiros E, Wiersema MJ (2002) High-frequency US catheter-based staging of early esophageal tumors. Gastrointest Endosc 55(1):95–99CrossRefPubMed Vazquez-Sequeiros E, Wiersema MJ (2002) High-frequency US catheter-based staging of early esophageal tumors. Gastrointest Endosc 55(1):95–99CrossRefPubMed
21.
go back to reference Qin X, He S, Zhang Y, Xue L, Lu N, Wang G (2014) Diagnosis and staging of superficial esophageal precursor based on pre-endoscopic resection system comparable to endoscopic resection. BMC Cancer 14:774CrossRefPubMedPubMedCentral Qin X, He S, Zhang Y, Xue L, Lu N, Wang G (2014) Diagnosis and staging of superficial esophageal precursor based on pre-endoscopic resection system comparable to endoscopic resection. BMC Cancer 14:774CrossRefPubMedPubMedCentral
22.
go back to reference Fujishiro M, Kodashima S, Goto O, Ono S, Niimi K, Yamamichi N, Oka M, Ichinose M, Omata M (2009) Endoscopic submucosal dissection for esophageal squamous cell neoplasms. Dig Endosc 21(2):109–115CrossRefPubMed Fujishiro M, Kodashima S, Goto O, Ono S, Niimi K, Yamamichi N, Oka M, Ichinose M, Omata M (2009) Endoscopic submucosal dissection for esophageal squamous cell neoplasms. Dig Endosc 21(2):109–115CrossRefPubMed
23.
go back to reference Motoyama S, Jin M, Matsuhashi T, Nanjo H, Ishiyama K, Sato Y, Yoshino K, Sasaki T, Wakita A, Saito H, Minamiya Y, Ohnishi H, Ogawa J (2013) Outcomes of patients receiving additional esophagectomy after endoscopic resection for clinically mucosal, but pathologically submucosal, squamous cell carcinoma of the esophagus. Surg Today 43(6):638–642CrossRefPubMed Motoyama S, Jin M, Matsuhashi T, Nanjo H, Ishiyama K, Sato Y, Yoshino K, Sasaki T, Wakita A, Saito H, Minamiya Y, Ohnishi H, Ogawa J (2013) Outcomes of patients receiving additional esophagectomy after endoscopic resection for clinically mucosal, but pathologically submucosal, squamous cell carcinoma of the esophagus. Surg Today 43(6):638–642CrossRefPubMed
24.
go back to reference Akutsu Y, Uesato M, Shuto K, Kono T, Hoshino I, Horibe D, Sazuka T, Takeshita N, Maruyama T, Isozaki Y, Akanuma N, Matsubara H (2013) The overall prevalence of metastasis in T1 esophageal squamous cell carcinoma: a retrospective analysis of 295 patients. Ann Surg 257(6):1032–1038CrossRefPubMed Akutsu Y, Uesato M, Shuto K, Kono T, Hoshino I, Horibe D, Sazuka T, Takeshita N, Maruyama T, Isozaki Y, Akanuma N, Matsubara H (2013) The overall prevalence of metastasis in T1 esophageal squamous cell carcinoma: a retrospective analysis of 295 patients. Ann Surg 257(6):1032–1038CrossRefPubMed
25.
go back to reference 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(4):544–551CrossRefPubMed 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(4):544–551CrossRefPubMed
26.
go back to reference Eguchi T, Nakanishi Y, Shimoda T, Iwasaki M, Igaki H, Tachimori Y, Kato H, Yamaguchi H, Saito D, Umemura S (2006) Histopathological criteria for additional treatment after endoscopic mucosal resection for esophageal cancer: analysis of 464 surgically resected cases. Mod Pathol 19(3):475–480CrossRefPubMed Eguchi T, Nakanishi Y, Shimoda T, Iwasaki M, Igaki H, Tachimori Y, Kato H, Yamaguchi H, Saito D, Umemura S (2006) Histopathological criteria for additional treatment after endoscopic mucosal resection for esophageal cancer: analysis of 464 surgically resected cases. Mod Pathol 19(3):475–480CrossRefPubMed
27.
go back to reference Uchinami Y, Myojin M, Takahashi H, Harada K, Shimizu S, Hosokawa M (2016) Prognostic factors in clinical T1N0M0 thoracic esophageal squamous cell carcinoma invading the muscularis mucosa or submucosa. Radiat Oncol 11:84CrossRefPubMedPubMedCentral Uchinami Y, Myojin M, Takahashi H, Harada K, Shimizu S, Hosokawa M (2016) Prognostic factors in clinical T1N0M0 thoracic esophageal squamous cell carcinoma invading the muscularis mucosa or submucosa. Radiat Oncol 11:84CrossRefPubMedPubMedCentral
Metadata
Title
Clinical implication of endoscopic gross appearance in superficial esophageal squamous carcinoma: revisited
Authors
Cheal Wung Huh
Da Hyun Jung
Jie-Hyun Kim
Dae Won Ma
Young Hoon Youn
Hyojin Park
Publication date
01-01-2018
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 1/2018
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-017-5685-8

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