Narrow-band imaging versus Lugol chromoendoscopy for esophageal squamous cell cancer screening in normal endoscopic practice: randomized controlled trial

Abstract

Background Narrow-band imaging (NBI) is as sensitive as Lugol chromoendoscopy to detect esophageal squamous cell carcinoma (SCC) but its specificity, which appears higher than that of Lugol chromoendoscopy in expert centers, remains to be established in general practice. This study aimed to prove the superiority of NBI specificity over Lugol chromoendoscopy in the detection of esophageal SCC and high grade dysplasia (HGD) in current general practice (including tertiary care centers, local hospitals, and private clinics).

Methods This prospective randomized multicenter trial included consecutive patients with previous or current SCC of the upper aerodigestive tract who were scheduled for gastroscopy. Patients were randomly allocated to either the Lugol or NBI group. In the Lugol group, examination with white light and Lugol chromoendoscopy were successively performed. In the NBI group, NBI examination was performed after white-light endoscopy. We compared the diagnostic characteristics of NBI and Lugol chromoendoscopy in a per-patient analysis.

Results 334 patients with history of SCC were included and analyzed (intention-to-treat) from 15 French institutions between March 2011 and December 2015. In per-patient analysis, sensitivity, specificity, positive and negative likelihood values were 100 %, 66.0 %, 21.2 %, and 100 %, respectively, for Lugol chromoendoscopy vs. 100 %, 79.9 %, 37.5 %, and 100 %, respectively, for NBI. Specificity was greater with NBI than with Lugol (P = 0.002).

Conclusions As previously demonstrated in expert centers, NBI was more specific than Lugol in current gastroenterology practice for the detection of early SCC, but combined approaches with both NBI and Lugol could improve the detection of squamous neoplasia.

Publication History

Received: 28 January 2020

Accepted: 22 July 2020

Accepted Manuscript online:
22 July 2020

Article published online:
01 October 2020

• References

• 1 Anderson LA, Tavilla A, Brenner H. et al. Survival for oesophageal, stomach and small intestine cancers in Europe 1999–2007: results from EUROCARE-5. Eur J Cancer 2015; 51: 2144-2157
• 2 Torre LA, Siegel RL, Ward EM. et al. Global cancer incidence and mortality rates and trends – an update. Cancer Epidemiol Prev Biomark 2016; 25: 16-27
• 3 Zhang Y. Epidemiology of esophageal cancer. World J Gastroenterol 2013; 19: 5598-5606
• 4 Dubuc J, Legoux J-L, Winnock M. et al. Endoscopic screening for esophageal squamous-cell carcinoma in high-risk patients: a prospective study conducted in 62 French endoscopy centers. Endoscopy 2006; 38: 690-695
• 5 Ina H, Shibuya H, Ohashi I. et al. The frequency of a concomitant early esophageal cancer in male patients with oral and oropharyngeal cancer. Screening results using Lugol dye endoscopy. Cancer 1994; 73: 2038-2041
• 6 Ribeiro U, Posner MC, Safatle-Ribeiro AV. et al. Risk factors for squamous cell carcinoma of the oesophagus. Br J Surg 1996; 83: 1174-1185
• 7 Petit T, Georges C, Jung GM. et al. Systematic esophageal endoscopy screening in patients previously treated for head and neck squamous-cell carcinoma. Ann Oncol 2001; 12: 643-646
• 8 Muto M, Hironaka S, Nakane M. et al. Association of multiple Lugol-voiding lesions with synchronous and metachronous esophageal squamous cell carcinoma in patients with head and neck cancer. Gastrointest Endosc 2002; 56: 517-521
• 9 Hirota WK, Zuckerman MJ, Adler DG. et al. Standards of Practice Committee, American Society for Gastrointestinal Endoscopy. ASGE guideline: the role of endoscopy in the surveillance of premalignant conditions of the upper GI tract. Gastrointest Endosc 2006; 63: 570-580
• 10 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
• 11 Bisschops R, Areia M, Coron E. et al. Performance measures for upper gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative. Endoscopy 2016; 48: 843-864
• 12 Kandiah K, Chedgy FJQ, Subramaniam S. et al. Early squamous neoplasia of the esophagus: the endoscopic approach to diagnosis and management. Saudi J Gastroenterol 2017; 23: 75-81
• 13 Trivedi PJ, Braden B. Indications, stains and techniques in chromoendoscopy. QJM 2013; 106: 117-131
• 14 Morita FHA, Bernardo WM, Ide E. et al. Narrow band imaging versus Lugol chromoendoscopy to diagnose squamous cell carcinoma of the esophagus: a systematic review and meta-analysis. BMC Cancer 2017; 17: 54
• 15 Nagami Y, Tominaga K, Machida H. et al. Usefulness of non-magnifying narrow-band imaging in screening of early esophageal squamous cell carcinoma: a prospective comparative study using propensity score matching. Am J Gastroenterol 2014; 109: 845-854
• 16 Ide E, Maluf-Filho F, Chaves DM. et al. Narrow-band imaging without magnification for detecting early esophageal squamous cell carcinoma. World J Gastroenterol 2011; 17: 4408-4413
• 17 Canard JM, Arpurt JP, Boustière C. et al. la Lettre de la SFED. Deux jours d’endoscopie en France. Résultats de l’enquête 2006. 2007 http://www.sfed.org/files/documents_sfed/files/lettresfed/Lettre_SFED_No36.pdf
• 18 Ponchon T, Lapalus MG, Saurin JC. et al. Could narrow band imaging (NBI) replace Lugol staining for the detection of esophageal squamous cell carcinoma?. Gastrointest Endosc 2007; 65: AB343
• 19 Tincani AJ, Brandalise N, Altemani A. et al. Diagnosis of superficial esophageal cancer and dysplasia using endoscopic screening with a 2% Lugol dye solution in patients with head and neck cancer. Head Neck 2000; 22: 170-174
• 20 Ishihara R, Takeuchi Y, Chatani R. et al. Prospective evaluation of narrow-band imaging endoscopy for screening of esophageal squamous mucosal high-grade neoplasia in experienced and less experienced endoscopists. Dis Esophagus 2010; 23: 480-486
• 21 The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc 2003; 58: S3-43
• 22 Shimizu Y, Omori T, Yokoyama A. et al. 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 2008; 23: 546-550
• 23 Takenaka R, Kawahara Y, Okada H. et al. Narrow-band imaging provides reliable screening for esophageal malignancy in patients with head and neck cancers. Am J Gastroenterol 2009; 104: 2942-2948
• 24 Casagrande JT, Pike MC. An improved approximate formula for calculating sample sizes for comparing two binomial distributions. Biometrics 1978; 34: 483-486
• 25 Dixon MF. Gastrointestinal epithelial neoplasia: Vienna revisited. Gut 2002; 51: 130-131
• 26 Muto M, Minashi K, Yano T. et al. 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 2010; 28: 1566-1572
• 27 Inoue H, Kaga M, Ikeda H. et al. Magnification endoscopy in esophageal squamous cell carcinoma: a review of the intrapapillary capillary loop classification. Ann Gastroenterol 2015; 28: 41-48
• 28 Jin D, Wang J, Zhan Q. et al. The safety and efficacy of 2% vitamin C solution spray for relief of mucosal irritation caused by Lugol chromoendoscopy: a multicenter, randomized, double-blind, parallel trial. Gastrointest Endosc 2019; DOI: 10.1016/j.gie.2019.11.028.
• 29 Bories E, Barret M, Chaussade S. Endoscopic treatment of superficial oesophageal squamous cell cancers. Acta Endosc 2017; 47: 192-194