Can optical evaluation distinguish between T1a and T1b esophageal adenocarcinoma: an international expert interobserver agreement study

Abstract

Background Piecemeal endoscopic mucosal resection (EMR) is an acceptable technique for T1a esophageal adenocarcinoma, but en bloc R0 excision is advocated for T1b disease as it may offer a potential cure and mitigate recurrence. Thus, distinguishing between T1a and T1b disease is imperative under current treatment paradigms. We investigated whether expert Barrett’s endoscopists could make this distinction based on optical evaluation.

Methods Endoscopic images of histologically confirmed high grade dysplasia (HGD), T1a, and T1b disease (20 sets for each) were compiled from consecutive patients at a single institution. Each set contained four images including an overview, a close-up in high definition white light, a near-focus magnification image, and a narrow-band image. Experts predicted the histology for each set.

Results 19 experts from 8 countries (Australia, USA, Italy, Netherlands, Germany, Canada, Belgium, and Portugal) participated. The majority had been practicing for > 20 years, with a median (interquartile range) annual case volume of 50 (18–75) for Barrett’s EMR and 25 (10–45) for Barrett’s endoscopic submucosal dissection. Esophageal adenocarcinoma (T1a/b) could be distinguished from HGD with a pooled sensitivity of 89.1 % (95 %CI 84.7–93.4). T1b adenocarcinoma could be predicted with a pooled sensitivity of 43.8 % (95 %CI 29.9–57.7). Fleiss’ kappa was 0.421 (95 %CI 0.399–0.442; P < 0.001), indicating fair-to-moderate agreement.

Conclusions Expert Barrett’s endoscopists could reliably differentiate T1a/T1b esophageal adenocarcinoma from HGD. Despite fair-to-moderate agreement for T staging, T1b disease could not be reliably distinguished from T1a disease. This may impact clinical decision making and selection of endoscopic techniques.

• References

• 1 Rice TW, Rusch VW, Ishwaran H. et al. Cancer of the esophagus and esophagogastric junction: data‐driven staging for the seventh edition of the American Joint Committee on Cancer/International Union Against Cancer Cancer Staging Manuals. Cancer 2010; 116: 3763-3773
• 2 Wani S, Drahos J, Cook MB. et al. Comparison of endoscopic therapies and surgical resection in patients with early esophageal cancer: a population-based study. Gastrointest Endosc 2014; 79: 224-232.e1
• 3 Bennett C, Vakil N, Bergman J. et al. Consensus statements for management of Barrett’s dysplasia and early-stage esophageal adenocarcinoma, based on a Delphi process. Gastroenterology 2012; 143: 336-346
• 4 McLarty AJ, Deschamps C, Trastek VF. et al. Esophageal resection for cancer of the esophagus: long-term function and quality of life. Ann Thorac Surg 1997; 63: 1568-1572
• 5 Bahin FF, Jayanna M, Hourigan LF. et al. Long-term outcomes of a primary complete endoscopic resection strategy for short-segment Barrett’s esophagus with high-grade dysplasia and/or early esophageal adenocarcinoma. Gastrointest Endosc 2016; 83: 68-77
• 6 Chung A, Bourke MJ, Hourigan L. 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
• 7 Moss A, Bourke MJ, Hourigan LF. et al. Endoscopic resection for Barrett’s high-grade dysplasia and early esophageal adenocarcinoma: an essential staging procedure with long-term therapeutic benefit. Am J Gastroenterol 2010; 105: 1276-1283
• 8 Van Vilsteren FG, Pouw RE, Seewald S. et al. Stepwise radical endoscopic resection versus radiofrequency ablation for Barrett’s oesophagus with high-grade dysplasia or early cancer: a multicentre randomised trial. Gut 2011; 60: 765-773
• 9 Pouw RE, Van Vilsteren FG, Peters FP. et al. Randomized trial on endoscopic resection-cap versus multiband mucosectomy for piecemeal endoscopic resection of early Barrett’s neoplasia. Gastrointest Endosc 2011; 74: 35-43
• 10 Dunbar KB, Spechler SJ. The risk of lymph node metastases in patients with high grade dysplasia or intramucosal carcinoma in Barrett’s esophagus: a systematic review. Am J Gastroenterol 2012; 107: 850
• 11 Kagemoto K, Oka S, Tanaka S. et al. Clinical outcomes of endoscopic submucosal dissection for superficial Barrett’s adenocarcinoma. Gastrointest Endosc 2014; 80: 239-245
• 12 Parikh MP, Thota PN, Raja S. et al. Outcomes of endoscopic submucosal dissection in esophageal adenocarcinoma staged T1bN0 by endoscopic ultrasound in non-surgical patients. J Gastrointest Oncol 2019; 10: 362
• 13 Schölvinck D, Künzli H, Meijer S. et al. Management of patients with T1b esophageal adenocarcinoma: a retrospective cohort study on patient management and risk of metastatic disease. Surg Endosc 2016; 30: 4102-4113
• 14 Chan MW, Nieuwenhuis E, Jansen M. et al. Endoscopic follow-up of radically resected submucosal adenocarcinoma in Barrett’s esophagus: interim results of an ongoing prospective, international, multicenter cohort registry (PREFER trial). Gastrointest Endosc 2023; 97 (Suppl. 06) AB1017-AB1018
• 15 Werbrouck E, De Hertogh G, Sagaert X. et al. Oesophageal biopsies are insufficient to predict final histology after endoscopic resection in early Barrett’s neoplasia. United European Gastroenterol J 2016; 4: 663-668
• 16 Qumseya BJ, Brown J, Abraham M. et al. Diagnostic performance of EUS in predicting advanced cancer among patients with Barrett’s esophagus and high-grade dysplasia/early adenocarcinoma: systematic review and meta-analysis. Gastrointest Endosc 2015; 81: 865-874.e2
• 17 Harris P, Taylor B, Minor B. et al. The REDCap consortium: building an international community of software partners. J Biomed Inform 2019; 95: 103208
• 18 Harris PA, Taylor R, Thielke R. et al. A metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform 2009; 42: 377-381
• 19 Genders TS, Spronk S, Stijnen T. et al. Methods for calculating sensitivity and specificity of clustered data: a tutorial. Radiology 2012; 265: 910-916
• 20 Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33: 159-174
• 21 Kastelein F, van Olphen S, Steyerberg E. et al. Surveillance in patients with long-segment Barrett’s oesophagus: a cost-effectiveness analysis. Gut 2015; 64: 864-871
• 22 Raman V, Jawitz OK, Voigt SL. et al. The effect of age on survival after endoscopic resection versus surgery for T1a esophageal cancer. J Thorac Cardiovasc Surg 2020; 160: 295-302.e3
• 23 Pimentel-Nunes P, Libânio D, Bastiaansen BA. et al. Endoscopic submucosal dissection for superficial gastrointestinal lesions: European Society of Gastrointestinal Endoscopy (ESGE) Guideline – update 2022. Endoscopy 2022; 54: 591-622
• 24 Forbes N, Elhanafi SE, Al-Haddad MA. et al. American Society for Gastrointestinal Endoscopy guideline on endoscopic submucosal dissection for the management of early esophageal and gastric cancers: summary and recommendations. Gastrointest Endosc 2023; 98: 271-284
• 25 Peters FP, Brakenhoff KP, Curvers WL. et al. Histologic evaluation of resection specimens obtained at 293 endoscopic resections in Barrett’s esophagus. Gastrointest Endosc 2008; 67: 604-609
• 26 Yamasaki A, Shimizu T, Kawachi H. et al. Endoscopic features of esophageal adenocarcinoma derived from short‐segment versus long‐segment Barrett’s esophagus. J Gastroenterol Hepatol 2020; 35: 211-217
• 27 Shaheen NJ, Falk GW, Iyer PG. et al. Diagnosis and management of Barrett’s esophagus: an updated ACG guideline. Am J Gastroenterol 2022; 117: 559
• 28 Gono K, Obi T, Yamaguchi M. et al. Appearance of enhanced tissue features in narrow-band endoscopic imaging. J Biomed Optics 2004; 9: 568-577
• 29 Kara M, Bergman J. Autofluorescence imaging and narrow-band imaging for the detection of early neoplasia in patients with Barrett’s esophagus. Endoscopy 2006; 38: 627-631
• 30 Sharma P, Bergman JJ, Goda K. et al. Development and validation of a classification system to identify high-grade dysplasia and esophageal adenocarcinoma in Barrett’s esophagus using narrow-band imaging. Gastroenterology 2016; 150: 591-598
• 31 Ancona E, Rampado S, Cassaro M. et al. Prediction of lymph node status in superficial esophageal carcinoma. Ann Surg Oncol 2008; 15: 3278-3288
• 32 Badreddine RJ, Prasad GA, Lewis JT. et al. Depth of submucosal invasion does not predict lymph node metastasis and survival of patients with esophageal carcinoma. Clin Gastroenterol Hepatol 2010; 8: 248-253
• 33 Pennathur A, Farkas A, Krasinskas AM. et al. Esophagectomy for T1 esophageal cancer: outcomes in 100 patients and implications for endoscopic therapy. Ann Thorac Surg 2009; 87: 1048-1055
• 34 Westerterp M, Koppert LB, Buskens CJ. et al. Outcome of surgical treatment for early adenocarcinoma of the esophagus or gastro-esophageal junction. Virchows Archiv 2005; 446: 497-504
• 35 Benech N, O’Brien JM, Barret M. et al. Endoscopic resection of Barrett’s adenocarcinoma: intramucosal and low‐risk tumours are not associated with lymph node metastases. UEG J 2021; 9: 362-369
• 36 Pouw R, Nieuwenhuis E, Jansen M. et al. Endoscopic follow-up of radically resected submucosal esophageal adenocarcinoma: preliminary results of an ongoing prospective, international, multicenter cohort registry (PREFER trial). Dis Esophagus 2023; 36 (Suppl. 02) doad052.126
• 37 Bennett C, Vakil N, Bergman J. et al. Consensus statements for management of Barrett’s dysplasia and early-stage esophageal adenocarcinoma, based on a Delphi process. Gastroenterology 2012; 143: 336-346
• 38 Sinonquel P, Haidry RJ, Bergman JJ. et al. MP028 Single wavelength endoscopy for the assessment of Barrett’s oesophagus: expert and non-expert optical diagnosis using different imaging techniques. United European Gastroenterology Journal 2022; 10 (Suppl. 08) 204
• 39 Ebigbo A, Mendel R, Rückert T. et al. Endoscopic prediction of submucosal invasion in Barrett’s cancer with the use of artificial intelligence: a pilot study. Endoscopy 2021; 53: 878-883