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Published in: Surgical Endoscopy 5/2024

11-03-2024

Efficacy of endoscopic surveillance for pharyngeal mucosa during endoscopic resection for pharyngeal carcinoma: a multicenter prospective study

Authors: Yuki Kimura, Yuichi Shimizu, Masanobu Taniguchi, Suguru Ito, Akira Dobashi, Kenichi Goda, Yusuke Nishimura, Keiko Yamamoto, Shin Ichihara, Akihito Watanabe

Published in: Surgical Endoscopy | Issue 5/2024

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Abstract

Introduction

Since patients with pharyngeal squamous cell carcinoma (SCC) often have multiple pharyngeal lesions, evaluation of pharyngeal lesions before endoscopic resection (ER) is important. However, detailed endoscopic observation of the entire pharyngeal mucosa under conscious sedation is difficult. We examined the usefulness of endoscopic surveillance with narrow band imaging (NBI) and lugol staining for detection of pharyngeal sublesions during ER for pharyngeal SCC under general anesthesia (endoscopic surveillance during treatment; ESDT).

Methods

From January 2021 through June 2022, we examined 78 patients who were diagnosed with superficial pharyngeal SCC and underwent ER. They underwent the ESDT and for patients who were diagnosed with new lesions of pharyngeal SCC or high-grade dysplasia (HGD) that were not detected in the endoscopic examination before treatment, ER were performed simultaneously for new lesions and the main lesions. The primary endpoint of this study was the detection rate of new lesions of pharyngeal SCC or HGD in the ESDT.

Results

Fifteen of the 78 patients were diagnosed as having undetected new pharyngeal lesions in the ESDT and 10 (12.8%) (95% CI 6.9–22.2%) were histopathologically confirmed to have new lesions of pharyngeal SCC or HGD. Among the 13 lesions of SCC or HGD, 8 were found by NBI observation; however, 5 were undetectable using NBI but detectable by lugol staining. All of the 13 lesions had endoscopic findings of pink color sign on lugol staining.

Conclusions

Endoscopic surveillance for pharyngeal sublesions during ER for pharyngeal SCC is feasible and useful.
Literature
1.
go back to reference Muto M, Nakane M, Katada C, Sano Y, Ohtsu A, Esumi H, Ebihara S, Yoshida S (2004) Squamous cell carcinoma in situ at oropharyngeal and hypopharyngeal mucosal sites. Cancer 101:1375–1381CrossRefPubMed Muto M, Nakane M, Katada C, Sano Y, Ohtsu A, Esumi H, Ebihara S, Yoshida S (2004) Squamous cell carcinoma in situ at oropharyngeal and hypopharyngeal mucosal sites. Cancer 101:1375–1381CrossRefPubMed
2.
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 28:1566–1572CrossRefPubMedPubMedCentral 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 28:1566–1572CrossRefPubMedPubMedCentral
3.
go back to reference Katada C, Tanabe S, Koizumi W, Higuchi K, Sasaki T, Azuma M, Katada N, Masaki T, Nakayama M, Okamoto M, Muto M (2010) Narrow band imaging for detecting superficial squamous cell carcinoma of the head and neck in patients with esophageal squamous cell carcinoma. Endoscopy 42:185–190CrossRefPubMed Katada C, Tanabe S, Koizumi W, Higuchi K, Sasaki T, Azuma M, Katada N, Masaki T, Nakayama M, Okamoto M, Muto M (2010) Narrow band imaging for detecting superficial squamous cell carcinoma of the head and neck in patients with esophageal squamous cell carcinoma. Endoscopy 42:185–190CrossRefPubMed
4.
go back to reference Nakanishi H, Doyama H, Takemura K, Yoshida N, Tsuji K, Takeda Y, Asahina Y, Kito Y, Ito R, Hayashi T, Hirano K, Goto Y, Tominaga K, Inagaki S, Waseda Y, Tsuji S, Miwa K, Kaneko Y, Yamada S, Kurumaya H, Sakumoto M, Okada T (2014) Detection of pharyngeal cancer in the overall population undergoing upper GI endoscopy by using narrow-band imaging: a single-center experience, 2009–2012. Gastrointest Endosc 79:558–564CrossRefPubMed Nakanishi H, Doyama H, Takemura K, Yoshida N, Tsuji K, Takeda Y, Asahina Y, Kito Y, Ito R, Hayashi T, Hirano K, Goto Y, Tominaga K, Inagaki S, Waseda Y, Tsuji S, Miwa K, Kaneko Y, Yamada S, Kurumaya H, Sakumoto M, Okada T (2014) Detection of pharyngeal cancer in the overall population undergoing upper GI endoscopy by using narrow-band imaging: a single-center experience, 2009–2012. Gastrointest Endosc 79:558–564CrossRefPubMed
5.
go back to reference Shimizu Y, Yamamoto J, Kato M, Yoshida T, Hirota J, Ono Y, Nakagawa M, Nakagawa S, Oridate N, Asaka M (2006) Endoscopic submucosal dissection for treatment of early stage hypopharyngeal carcinoma. Gastrointest Endosc 64:255–259CrossRefPubMed Shimizu Y, Yamamoto J, Kato M, Yoshida T, Hirota J, Ono Y, Nakagawa M, Nakagawa S, Oridate N, Asaka M (2006) Endoscopic submucosal dissection for treatment of early stage hypopharyngeal carcinoma. Gastrointest Endosc 64:255–259CrossRefPubMed
6.
go back to reference Iizuka T, Kikuchi D, Hoteya S, Nakamura M, Yamashita S, Mitani T, Takeda H, Yahagi N (2011) Clinical advantage of endoscopic submucosal dissection over endoscopic mucosal resection for early mesopharyngeal and hypopharyngeal cancers. Endoscopy 43:839–843CrossRefPubMed Iizuka T, Kikuchi D, Hoteya S, Nakamura M, Yamashita S, Mitani T, Takeda H, Yahagi N (2011) Clinical advantage of endoscopic submucosal dissection over endoscopic mucosal resection for early mesopharyngeal and hypopharyngeal cancers. Endoscopy 43:839–843CrossRefPubMed
7.
go back to reference Kuwabara T, Hiyama T, Oka S, Urabe Y, Tanaka S, Yoshihara M, Arihiro K, Shimamoto F, Chayama K (2012) Clinical features of pharyngeal intraepithelial neoplasias and outcomes of treatment by endoscopic submucosal dissection. Gastrointest Endosc 76:1095–1103CrossRefPubMed Kuwabara T, Hiyama T, Oka S, Urabe Y, Tanaka S, Yoshihara M, Arihiro K, Shimamoto F, Chayama K (2012) Clinical features of pharyngeal intraepithelial neoplasias and outcomes of treatment by endoscopic submucosal dissection. Gastrointest Endosc 76:1095–1103CrossRefPubMed
8.
go back to reference Satake H, Yano T, Muto M, Minashi K, Yoda Y, Kojima T, Oono Y, Ikematsu H, Aoyama I, Morita S, Miyamoto S, Fujii S, Yoshizawa A, Ochiai A, Hayashi R, Kaneko K (2015) Clinical outcome after endoscopic resection for superficial pharyngeal squamous cell carcinoma invading the subepithelial layer. Endoscopy 47:11–18PubMed Satake H, Yano T, Muto M, Minashi K, Yoda Y, Kojima T, Oono Y, Ikematsu H, Aoyama I, Morita S, Miyamoto S, Fujii S, Yoshizawa A, Ochiai A, Hayashi R, Kaneko K (2015) Clinical outcome after endoscopic resection for superficial pharyngeal squamous cell carcinoma invading the subepithelial layer. Endoscopy 47:11–18PubMed
9.
go back to reference Hanaoka N, Ishihara R, Takeuchi Y, Suzuki M, Otozai S, Kida K, Yoshii T, Fujii T, Yoshino K, Sugawa T, Kitamura K, Kanemura R, Koike R, Uedo N, Higashino K, Akasaka T, Yamashina T, Kanesaka T, Matsuura N, Aoi K, Yamasaki Y, Hamada K, Iishi H, Tomita Y (2015) Endoscopic submucosal dissection as minimally invasive treatment for superficial pharyngeal cancer: a phase II study (with video). Gastrointest Endosc 82:1002–1008CrossRefPubMed Hanaoka N, Ishihara R, Takeuchi Y, Suzuki M, Otozai S, Kida K, Yoshii T, Fujii T, Yoshino K, Sugawa T, Kitamura K, Kanemura R, Koike R, Uedo N, Higashino K, Akasaka T, Yamashina T, Kanesaka T, Matsuura N, Aoi K, Yamasaki Y, Hamada K, Iishi H, Tomita Y (2015) Endoscopic submucosal dissection as minimally invasive treatment for superficial pharyngeal cancer: a phase II study (with video). Gastrointest Endosc 82:1002–1008CrossRefPubMed
10.
go back to reference Muto M, Satake H, Yano T, Minashi K, Hayashi R, Fujii S, Ochiai A, Ohtsu A, Morita S, Horimatsu T, Ezoe Y, Miyamoto S, Asato R, Tateya I, Yoshizawa A, Chiba T (2011) Long-term outcome of transoral organ-preserving pharyngeal endoscopic resection for superficial pharyngeal cancer. Gastrointest Endosc 74:477–484CrossRefPubMed Muto M, Satake H, Yano T, Minashi K, Hayashi R, Fujii S, Ochiai A, Ohtsu A, Morita S, Horimatsu T, Ezoe Y, Miyamoto S, Asato R, Tateya I, Yoshizawa A, Chiba T (2011) Long-term outcome of transoral organ-preserving pharyngeal endoscopic resection for superficial pharyngeal cancer. Gastrointest Endosc 74:477–484CrossRefPubMed
11.
go back to reference Tateya I, Muto M, Morita S, Miyamoto S, Hayashi T, Funakoshi M, Aoyama I, Higuchi H, Hirano S, Kitamura M, Ishikawa S, Kishimoto Y, Morita M, Ito J (2016) Endoscopic laryngo-pharyngeal surgery for superficial laryngo-pharyngeal cancer. Surg Endosc 30:323–329CrossRefPubMed Tateya I, Muto M, Morita S, Miyamoto S, Hayashi T, Funakoshi M, Aoyama I, Higuchi H, Hirano S, Kitamura M, Ishikawa S, Kishimoto Y, Morita M, Ito J (2016) Endoscopic laryngo-pharyngeal surgery for superficial laryngo-pharyngeal cancer. Surg Endosc 30:323–329CrossRefPubMed
12.
go back to reference Watanabe A, Taniguchi M, Kimura Y, Hosokawa M, Ito S, Tsukamoto S, Sasaki S (2017) Synopsis transoral endoscopic laryngopharyngeal surgery for superficial pharyngeal cancers. Head Neck 39:1779–1787CrossRefPubMed Watanabe A, Taniguchi M, Kimura Y, Hosokawa M, Ito S, Tsukamoto S, Sasaki S (2017) Synopsis transoral endoscopic laryngopharyngeal surgery for superficial pharyngeal cancers. Head Neck 39:1779–1787CrossRefPubMed
13.
go back to reference Iizuka T, Kikuchi D, Suzuki Y, Tanaka M, Takeda H (2021) Clinical relevance of endoscopic treatment for superficial pharyngeal cancer: feasibility of techniques corresponding to each location and long-term outcomes. Gastrointest Endosc 93:818–827CrossRefPubMed Iizuka T, Kikuchi D, Suzuki Y, Tanaka M, Takeda H (2021) Clinical relevance of endoscopic treatment for superficial pharyngeal cancer: feasibility of techniques corresponding to each location and long-term outcomes. Gastrointest Endosc 93:818–827CrossRefPubMed
14.
go back to reference Sakaguchi Y, Saito Y, Ando M, Yoshida M, Fukuoka O, Kobayashi K, Kubota D, Ohki D, Mizutani H, Niimi K, Tsuji Y, Fujishiro M, Yamasoba T (2023) Risk factors for incomplete resection with pharyngeal endoscopic submucosal dissection and long-term prognosis after resection. Surg Endosc 37:3593–3601CrossRefPubMedPubMedCentral Sakaguchi Y, Saito Y, Ando M, Yoshida M, Fukuoka O, Kobayashi K, Kubota D, Ohki D, Mizutani H, Niimi K, Tsuji Y, Fujishiro M, Yamasoba T (2023) Risk factors for incomplete resection with pharyngeal endoscopic submucosal dissection and long-term prognosis after resection. Surg Endosc 37:3593–3601CrossRefPubMedPubMedCentral
15.
go back to reference Takahashi M, Shimizu Y, Ono M, Suzuki M, Omori S, Yoshida T, Mori Y, Nakagawa M, Ono S, Nakagawa S, Mabe K, Kato M, Hatanaka K, Asaka M, Sakamoto N (2014) Endoscopic diagnosis of early neoplasia of the esophagus with narrow band imaging: correlations among background coloration and iodine staining findings. J Gastroenterol Hepatol 29:762–768CrossRefPubMed Takahashi M, Shimizu Y, Ono M, Suzuki M, Omori S, Yoshida T, Mori Y, Nakagawa M, Ono S, Nakagawa S, Mabe K, Kato M, Hatanaka K, Asaka M, Sakamoto N (2014) Endoscopic diagnosis of early neoplasia of the esophagus with narrow band imaging: correlations among background coloration and iodine staining findings. J Gastroenterol Hepatol 29:762–768CrossRefPubMed
16.
go back to reference Shimizu Y, Omori T, Yokoyama A, Yoshida T, Hirota J, Ono Y, Yamamoto J, Kato M, Asaka M (2008) Endoscopic diagnosis of early squamous neoplasia of the esophagus with iodine staining: high-grade intra-epithelial neoplasia turns pink within a few minutes. J Gastroenterol Hepatol 23:546–550CrossRefPubMed Shimizu Y, Omori T, Yokoyama A, Yoshida T, Hirota J, Ono Y, Yamamoto J, Kato M, Asaka M (2008) Endoscopic diagnosis of early squamous neoplasia of the esophagus with iodine staining: high-grade intra-epithelial neoplasia turns pink within a few minutes. J Gastroenterol Hepatol 23:546–550CrossRefPubMed
17.
go back to reference Bugter O, Ven SEM, Hardillo JA, Bruno MJ, Koch AD, Baatenburg de Jong RJ (2019) Early detection of esophageal second primary tumors using lugol chromoendoscopy in patients with head and neck cancer: a systematic review and meta-analysis. Head Neck 41:1122–1130CrossRefPubMed Bugter O, Ven SEM, Hardillo JA, Bruno MJ, Koch AD, Baatenburg de Jong RJ (2019) Early detection of esophageal second primary tumors using lugol chromoendoscopy in patients with head and neck cancer: a systematic review and meta-analysis. Head Neck 41:1122–1130CrossRefPubMed
18.
go back to reference Liu M, Zhou R, Guo C, Xu R, Liu A, Yang H, Li F, Duan L, Shen L, Wu Q, Liu Z, Liu F, Liu Y, Pan Y, Cai H, Weiss NS, He Z, Ke Y (2021) Size of lugol-unstained lesions as a predictor for risk of progression in premalignant lesions of the esophagus. Gastrointest Endosc 93:1074–1076CrossRef Liu M, Zhou R, Guo C, Xu R, Liu A, Yang H, Li F, Duan L, Shen L, Wu Q, Liu Z, Liu F, Liu Y, Pan Y, Cai H, Weiss NS, He Z, Ke Y (2021) Size of lugol-unstained lesions as a predictor for risk of progression in premalignant lesions of the esophagus. Gastrointest Endosc 93:1074–1076CrossRef
19.
go back to reference Kanzaki H, Ishihara R, Ishiguro S, Nagai K, Matsui F, Yamashina T, Ohta T, Yamamoto S, Hanaoka N, Hanafusa M, Takeuchi Y, Higashino K, Uedo N, Iishi H, Tomita Y (2013) Histological features responsible for brownish epithelium in squamous neoplasia of the esophagus by narrow band imaging. J Gastroenterol Hepatol 28:274–278CrossRefPubMed Kanzaki H, Ishihara R, Ishiguro S, Nagai K, Matsui F, Yamashina T, Ohta T, Yamamoto S, Hanaoka N, Hanafusa M, Takeuchi Y, Higashino K, Uedo N, Iishi H, Tomita Y (2013) Histological features responsible for brownish epithelium in squamous neoplasia of the esophagus by narrow band imaging. J Gastroenterol Hepatol 28:274–278CrossRefPubMed
20.
go back to reference Ishihara R, Yamada T, Iishi H, Kato M, Yamamoto S, Yamamoto S, Masuda E, Tatsumi K, Takeuchi Y, Higashino K, Uedo N, Tatsuta M, Ishiguro S (2009) Quantitative analysis of the color change after iodine staining for diagnosing esophageal high-grade intraepithelial neoplasia and invasive cancer. Gastrointest Endosc 69:213–218CrossRefPubMed Ishihara R, Yamada T, Iishi H, Kato M, Yamamoto S, Yamamoto S, Masuda E, Tatsumi K, Takeuchi Y, Higashino K, Uedo N, Tatsuta M, Ishiguro S (2009) Quantitative analysis of the color change after iodine staining for diagnosing esophageal high-grade intraepithelial neoplasia and invasive cancer. Gastrointest Endosc 69:213–218CrossRefPubMed
21.
go back to reference Gale N, Hille J, Jordan RC (2017) Precursor lesions. In: El-Naggar AK, Chan JKC, Grandis JR et al (eds) WHO classification of head and neck tumours, 4th edn. IARC, Lyon, pp 91–95 Gale N, Hille J, Jordan RC (2017) Precursor lesions. In: El-Naggar AK, Chan JKC, Grandis JR et al (eds) WHO classification of head and neck tumours, 4th edn. IARC, Lyon, pp 91–95
22.
go back to reference Slaughter DP, Southwick HW, Smejkal W (1953) “Field cancerization” in oral stratified epithelium. Cancer 6:963–968CrossRefPubMed Slaughter DP, Southwick HW, Smejkal W (1953) “Field cancerization” in oral stratified epithelium. Cancer 6:963–968CrossRefPubMed
23.
go back to reference Lee YC, Wang HP, Wang CP, Ko JY, Lee JM, Chiu HM, Lin JT, Yamashita S, Oka D, Watanabe N, Matsuda Y, Ushijima T, Wu MS (2011) Revisit of field cancerization in squamous cell carcinoma of upper aerodigestive tract: better risk assessment with epigenetic markers. Cancer Prev Res 4:1982–1992CrossRef Lee YC, Wang HP, Wang CP, Ko JY, Lee JM, Chiu HM, Lin JT, Yamashita S, Oka D, Watanabe N, Matsuda Y, Ushijima T, Wu MS (2011) Revisit of field cancerization in squamous cell carcinoma of upper aerodigestive tract: better risk assessment with epigenetic markers. Cancer Prev Res 4:1982–1992CrossRef
24.
go back to reference Katada C, Yokoyama T, Yano T, Kaneko K, Oda I, Shimizu Y, Doyama H, Koike T, Takizawa K, Hirao M, Okada H, Yoshii T, Konishi K, Yamanouchi T, Tsuda T, Omori T, Kobayashi N, Shimoda T, Ochiai A, Amanuma Y, Ohashi S, Matsuda T, Ishikawa H, Yokoyama A, Muto M (2016) Alcohol consumption and multiple dysplastic lesions increase risk of squamous cell carcinoma in the esophagus, head, and neck. Gastroenterology 151:860–869CrossRefPubMed Katada C, Yokoyama T, Yano T, Kaneko K, Oda I, Shimizu Y, Doyama H, Koike T, Takizawa K, Hirao M, Okada H, Yoshii T, Konishi K, Yamanouchi T, Tsuda T, Omori T, Kobayashi N, Shimoda T, Ochiai A, Amanuma Y, Ohashi S, Matsuda T, Ishikawa H, Yokoyama A, Muto M (2016) Alcohol consumption and multiple dysplastic lesions increase risk of squamous cell carcinoma in the esophagus, head, and neck. Gastroenterology 151:860–869CrossRefPubMed
25.
go back to reference Takenaka R, Kawahara Y, Okada H, Hori K, Inoue M, Kawano S, Tanioka D, Tsuzuki T, Uemura M, Ohara N, Tominaga S, Onoda T, Yamamoto K (2009) Narrow-band imaging provides reliable screening for esophageal malignancy in patients with head and neck cancers. Am J Gastroenterol 104:2942–2948CrossRefPubMed Takenaka R, Kawahara Y, Okada H, Hori K, Inoue M, Kawano S, Tanioka D, Tsuzuki T, Uemura M, Ohara N, Tominaga S, Onoda T, Yamamoto K (2009) Narrow-band imaging provides reliable screening for esophageal malignancy in patients with head and neck cancers. Am J Gastroenterol 104:2942–2948CrossRefPubMed
26.
go back to reference Kawada K, Arima M, Miyahara R, Tsunomiya M, Kikuchi M, Yamamoto F, Hoshino A, Nakajima Y, Kinugasa Y, Kawano T (2021) Effect of adding magnifying BLI, magnifying NBI, and iodine staining to white light imaging in diagnosis of early esophageal cancer. Endosc Int Open 09:E1877-1885CrossRef Kawada K, Arima M, Miyahara R, Tsunomiya M, Kikuchi M, Yamamoto F, Hoshino A, Nakajima Y, Kinugasa Y, Kawano T (2021) Effect of adding magnifying BLI, magnifying NBI, and iodine staining to white light imaging in diagnosis of early esophageal cancer. Endosc Int Open 09:E1877-1885CrossRef
27.
go back to reference Ono S, Dobashi A, Furuhashi H, Koizumi A, Matsui H, Hara Y, Sumiyama K (2021) Characteristics of superficial esophageal squamous cell carcinomas undetectable with narrow-band imaging endoscopy. Gastroenterol Rep 9:402–407CrossRef Ono S, Dobashi A, Furuhashi H, Koizumi A, Matsui H, Hara Y, Sumiyama K (2021) Characteristics of superficial esophageal squamous cell carcinomas undetectable with narrow-band imaging endoscopy. Gastroenterol Rep 9:402–407CrossRef
Metadata
Title
Efficacy of endoscopic surveillance for pharyngeal mucosa during endoscopic resection for pharyngeal carcinoma: a multicenter prospective study
Authors
Yuki Kimura
Yuichi Shimizu
Masanobu Taniguchi
Suguru Ito
Akira Dobashi
Kenichi Goda
Yusuke Nishimura
Keiko Yamamoto
Shin Ichihara
Akihito Watanabe
Publication date
11-03-2024
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 5/2024
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-024-10747-5

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