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  • Review Article
  • Published:

Role of endoscopy in early oesophageal cancer

Nature Reviews Gastroenterology & Hepatology volume 13, pages 720–730 (2016)Cite this article

Subjects

Key Points

  • Current generation high-definition endoscopy enables detection of early oesophageal neoplasia

  • Detailed examination and image enhancement techniques enable characterization and improved delineation of early neoplasia to inform endoscopic therapy

  • Endoscopic resection is now standard of care for the treatment of early oesophageal neoplasia confined to the mucosa, and in selected cases of adenocarcinoma with superficial submucosal invasion

  • Radiofrequency ablation is the preferred ablative technique and adjuvant treatment to endoscopic resection in Barrett dysplasia

Abstract

Incidence of oesophageal adenocarcinoma has increased exponentially in the West over the past few decades. Following detection of advanced cancers, 5-year survival rates remain bleak, making identification of early neoplasia, which has a better outcome, important. Detection of subtle oesophageal lesions during endoscopy can be challenging, and advanced imaging techniques might improve their detection. High-definition endoscopy has become a standard in most endoscopy centres, and this technology probably provides better delineation of mucosal features than standard-definition endoscopy. Various image enhancement techniques are now available with the development of new electronics and software systems. Image enhancement with chromoendoscopy using dyes has been a cost-effective option for many years, yet these techniques have been replaced in some contexts by electronic chromoendoscopy, which can be used with the press of a button. However, Lugol's chromoendoscopy remains the gold standard to identify squamous dysplasia. Identification and characterization of subtle neoplastic lesions could help to target biopsies and perform endoscopic resection for better local staging and definitive therapy. In vivo histology with techniques such as confocal endomicroscopy could make endotherapy feasible within a shorter timescale than when relying on histology on tissue samples. Once early neoplasia is identified, treatments include endoscopic resection, endoscopic submucosal dissection or various ablative techniques. Endotherapy has the advantage of being a less invasive technique than oesophagectomy, and is associated with lower mortality and morbidity. Endoscopic ablation therapies have evolved over the past few years, with radiofrequency ablation showing the best results in terms of success rates and complications in Barrett dysplasia.

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Figure 1: Lugol's iodine dye is the gold-standard for detecting SCC.
Figure 2: Acetowhitening and high-magnification endoscopy can visualize early neoplasia.
Figure 3: Enhanced imaging techniques.
Figure 4: Endoscopic resection
Figure 5: RFA ablation in Barrett oesophagus.
Figure 6: Algorithm for the management of Barrett early neoplasia.
Figure 7: Investigation of Barrett oesophagus using optical enhancement imaging.
Figure 8: Blue laser imaging of Barrett oesophagus.

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References

  1. Devesa, S. S., Blot, W. J. & Fraumeni, J. F. Jr. Changing patterns in the incidence of esophageal and gastric carcinoma in the United States. Cancer 83, 2049–2053 (1998).

    CAS  PubMed  Google Scholar 

  2. Enzinger, P. C. & Mayer, R. J. Esophageal cancer. N. Engl. J. Med. 349, 2241–2252 (2003).

    CAS  PubMed  Google Scholar 

  3. Jankowski, J. A., Provenzale, D. & Moayyedi, P. Esophageal adenocarcinoma arising from Barrett's metaplasia has regional variations in the west. Gastroenterology 122, 588–590 (2002).

    PubMed  Google Scholar 

  4. Abrams, J. A., Sharaiha, R. Z., Gonsalves, L., Lightdale, C. J. & Neugut, A. I. Dating the rise of esophageal adenocarcinoma: analysis of Connecticut Tumor Registry data, 1940–2007. Cancer Epidemiol. Biomarkers Prev. 20, 183–186 (2011).

    PubMed  Google Scholar 

  5. El-Serag, H. B., Mason, A. C., Petersen, N. & Key, C. R. Epidemiological differences between adenocarcinoma of the oesophagus and adenocarcinoma of the gastric cardia in the USA. Gut 50, 368–372 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Castro, C. et al. Patterns and trends in esophageal cancer mortality and incidence in Europe (1980–2011) and predictions to 2015. Ann. Oncol. 25, 283–290 (2014).

    CAS  PubMed  Google Scholar 

  7. Boys, J. A. et al. Can the risk of lymph node metastases be gauged in endoscopically resected submucosal esophageal adenocarcinomas? A multi-center study. J. Gastrointest. Surg. 20, 6–12 (2016).

    PubMed  Google Scholar 

  8. Liu, L. et al. Significance of the depth of tumor invasion and lymph node metastasis in superficially invasive (T1) esophageal adenocarcinoma. Am. J. Surg. Pathol. 29, 1079–1085 (2005).

    PubMed  Google Scholar 

  9. Westerterp, M. et al. Outcome of surgical treatment for early adenocarcinoma of the esophagus or gastro-esophageal junction. Virchows Arch. 446, 497–504 (2005).

    PubMed  Google Scholar 

  10. Siewert, J. R. et al. Histologic tumor type is an independent prognostic parameter in esophageal cancer: lessons from more than 1,000 consecutive resections at a single center in the Western world. Ann. Surg. 234, 360–367 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Pennathur, A., Gibson, M. K., Jobe, B. A. & Luketich, J. D. et al. Oesophageal carcinoma. Lancet 381, 400–412 (2013).

    PubMed  Google Scholar 

  12. Singh, S. et al. Incidence of esophageal adenocarcinoma in Barrett's esophagus with low-grade dysplasia: a systematic review and meta-analysis. Gastrointest. Endosc. 79, 897–909 (2014).

    PubMed  Google Scholar 

  13. Verbeek, R. E. et al. Surveillance and follow-up strategies in patients with high-grade dysplasia in Barrett's esophagus: a Dutch population-based study. Am. J. Gastroenterol. 107, 534–542 (2012).

    PubMed  Google Scholar 

  14. Sami, S. S. et al. High definition versus standard definition white light endoscopy for detecting dysplasia in patients with Barrett's esophagus. Dis. Esophagus 28, 742–749 (2014).

    PubMed  Google Scholar 

  15. Marvik, R. & Lango, T. High-definition television in medicine. Surg. Endosc. 20, 349–350 (2006).

    CAS  PubMed  Google Scholar 

  16. Hurlstone, D. P. & Fujii, T. Practical uses of chromoendoscopy and magnification at colonoscopy. Gastrointest. Endosc. Clin. N. Am. 15, 687–702 (2005).

    PubMed  Google Scholar 

  17. Tanaka, K. et al. Features of early gastric cancer and gastric adenoma by enhanced-magnification endoscopy. J. Gastroenterol. 41, 332–338 (2006).

    PubMed  Google Scholar 

  18. Togashi, K. et al. The use of acetic acid in magnification chromocolonoscopy for pit pattern analysis of small polyps. Endoscopy 38, 613–616 (2006).

    CAS  PubMed  Google Scholar 

  19. Yao, K. et al. Magnification endoscopy outlines the microvascular architecture and extent of Barrett's intramucosal carcinoma prior to endoscopic resection. Gastrointest. Endosc. 63, 1064–1065 (2006).

    PubMed  Google Scholar 

  20. Singh, R. et al. Preliminary feasibility study using a novel narrow-band imaging system with dual focus magnification capability in Barrett's esophagus: is the time ripe to abandon random biopsies? Dig. Endosc. 25 (Suppl. 2), 151–156 (2013).

    PubMed  Google Scholar 

  21. Bennett, C. et al. Consensus statements for management of Barrett's dysplasia and early-stage esophageal adenocarcinoma, based on a Delphi process. Gastroenterology 143, 336–346 (2012).

    PubMed  PubMed Central  Google Scholar 

  22. Canto, M. I. et al. Methylene blue-directed biopsies improve detection of intestinal metaplasia and dysplasia in Barrett's esophagus. Gastrointest. Endosc. 51, 560–568 (2000).

    CAS  PubMed  Google Scholar 

  23. Gossner, L. et al. Comparison of methylene blue-directed biopsies and four-quadrant biopsies in the detection of high-grade intraepithelial neoplasia and early cancer in Barrett's oesophagus. Dig. Liver Dis. 38, 724–729 (2006).

    CAS  PubMed  Google Scholar 

  24. Ragunath, K., Krasner, N., Raman, V. S., Haqqani, M. T. & Cheung, W. Y. A randomized, prospective cross-over trial comparing methylene blue-directed biopsy and conventional random biopsy for detecting intestinal metaplasia and dysplasia in Barrett's esophagus. Endoscopy 35, 998–1003 (2003).

    CAS  PubMed  Google Scholar 

  25. Ngamruengphong, S., Sharma, V. K. & Das, A. Diagnostic yield of methylene blue chromoendoscopy for detecting specialized intestinal metaplasia and dysplasia in Barrett's esophagus: a meta-analysis. Gastrointest. Endosc. 69, 1021–1028 (2009).

    PubMed  Google Scholar 

  26. Sharma, P. et al. Non-biopsy detection of intestinal metaplasia and dysplasia in Barrett's esophagus: a prospective multicenter study. Endoscopy 38, 1206–1212 (2006).

    CAS  PubMed  Google Scholar 

  27. Kara, M. A. et al. High-resolution endoscopy plus chromoendoscopy or narrow-band imaging in Barrett's esophagus: a prospective randomized crossover study. Endoscopy 37, 929–936 (2005).

    CAS  PubMed  Google Scholar 

  28. Guelrud, M., Herrera, I., Essenfeld, H. & Castro, J. Enhanced magnification endoscopy: a new technique to identify specialized intestinal metaplasia in Barrett's esophagus. Gastrointest. Endosc. 53, 559–565 (2001).

    CAS  PubMed  Google Scholar 

  29. Fortun, P. J. et al. Acetic acid-enhanced magnification endoscopy in the diagnosis of specialized intestinal metaplasia, dysplasia and early cancer in Barrett's oesophagus. Aliment. Pharmacol. Ther. 23, 735–742 (2006).

    CAS  PubMed  Google Scholar 

  30. Pohl, J. et al. Incidence of macroscopically occult neoplasias in Barrett's esophagus: are random biopsies dispensable in the era of advanced endoscopic imaging? Am. J. Gastroenterol. 105, 2350–2356 (2010).

    PubMed  Google Scholar 

  31. Longcroft-Wheaton, G., Duku, M., Mead, R., Poller, D. & Bhandari, P. Acetic acid spray is an effective tool for the endoscopic detection of neoplasia in patients with Barrett's esophagus. Clin. Gastroenterol. Hepatol. 8, 843–847 (2010).

    PubMed  Google Scholar 

  32. Tholoor, S., Bhattacharyya, R., Tsagkournis, O., Longcroft-Wheaton, G. & Bhandari, P. Acetic acid chromoendoscopy in Barrett's esophagus surveillance is superior to the standardized random biopsy protocol: results from a large cohort study (with video). Gastrointest. Endosc. 80, 417–424 (2014).

    PubMed  Google Scholar 

  33. Coletta, M. et al. Acetic acid chromoendoscopy for the diagnosis of early neoplasia and specialized intestinal metaplasia in Barrett's esophagus: a meta-analysis. Gastrointest. Endosc. 83, 57–67 (2016).

    PubMed  Google Scholar 

  34. Longcroft-Wheaton, G. et al. Duration of acetowhitening as a novel objective tool for diagnosing high risk neoplasia in Barrett's esophagus: a prospective cohort trial. Endoscopy 45, 426–432 (2013).

    CAS  PubMed  Google Scholar 

  35. Bhandari, P., Kandaswamy, P., Cowlishaw, D. & Longcroft-Wheaton, G. Acetic acid-enhanced chromoendoscopy is more cost-effective than protocol-guided biopsies in a high-risk Barrett's population. Dis. Esophagus. 25, 386–392 (2012).

    CAS  PubMed  Google Scholar 

  36. Lopes, A. B. & Fagundes, R. B. Esophageal squamous cell carcinoma - precursor lesions and early diagnosis. World J. Gastrointest. Endosc. 4, 9–16 (2012).

    PubMed  PubMed Central  Google Scholar 

  37. Boller, D. et al. Lugol chromoendoscopy combined with brush cytology in patients at risk for esophageal squamous cell carcinoma. Surg. Endosc. 23, 2748–2754 (2009).

    CAS  PubMed  Google Scholar 

  38. Lecleire, S. et al. Lugol chromo-endoscopy versus narrow band imaging for endoscopic screening of esophageal squamous-cell carcinoma in patients with a history of cured esophageal cancer: a feasibility study. Dis. Esophagus. 24, 418–422 (2011).

    CAS  PubMed  Google Scholar 

  39. Urabe, Y. et al. Metachronous multiple esophageal squamous cell carcinomas and Lugol-voiding lesions after endoscopic mucosal resection. Endoscopy 41, 304–309 (2009).

    CAS  PubMed  Google Scholar 

  40. Gono, K. et al. Appearance of enhanced tissue features in narrow-band endoscopic imaging. J. Biomed. Opt. 9, 568–577 (2004).

    PubMed  Google Scholar 

  41. Wolfsen, H. C. et al. Prospective, controlled tandem endoscopy study of narrow band imaging for dysplasia detection in Barrett's Esophagus. Gastroenterology 135, 24–31 (2008).

    PubMed  Google Scholar 

  42. Singh, R. et al. Narrow-band imaging with magnification in Barrett's esophagus: validation of a simplified grading system of mucosal morphology patterns against histology. Endoscopy 40, 457–463 (2008).

    CAS  PubMed  Google Scholar 

  43. Mannath, J., Subramanian, V., Hawkey, C. J. & Ragunath, K. Narrow band imaging for characterization of high grade dysplasia and specialized intestinal metaplasia in Barrett's esophagus: a meta-analysis. Endoscopy 42, 351–359 (2010).

    CAS  PubMed  Google Scholar 

  44. Levine, D. S. et al. An endoscopic biopsy protocol can differentiate high-grade dysplasia from early adenocarcinoma in Barrett's esophagus. Gastroenterology 105, 40–50 (1993).

    CAS  PubMed  Google Scholar 

  45. Sharma, P. et al. Standard endoscopy with random biopsies versus narrow band imaging targeted biopsies in Barrett's oesophagus: a prospective, international, randomised controlled trial. Gut 62, 15–21 (2013).

    PubMed  Google Scholar 

  46. Qumseya, B. J. et al. Advanced imaging technologies increase detection of dysplasia and neoplasia in patients with Barrett's esophagus: a meta-analysis and systematic review. Clin. Gastroenterol. Hepatol. 11, 1562–1570 (2013).

    PubMed  PubMed Central  Google Scholar 

  47. Singh, R. et al. Narrow-band imaging and white-light endoscopy with optical magnification in the diagnosis of dysplasia in Barrett's esophagus: results of the Asia-Pacific Barrett's Consortium. Endosc. Int. Open 3, E14–E18 (2015).

    PubMed  Google Scholar 

  48. Sharma, P. 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 150, 591–598 (2015).

    PubMed  Google Scholar 

  49. Yoshida, T. et al. Narrow-band imaging system with magnifying endoscopy for superficial esophageal lesions. Gastrointest. Endosc. 59, 288–295 (2004).

    PubMed  Google Scholar 

  50. Muto, M. et al. Squamous cell carcinoma in situ at oropharyngeal and hypopharyngeal mucosal sites. Cancer 101, 1375–1381 (2004).

    PubMed  Google Scholar 

  51. Inoue, H. et al. Magnification endoscopy in esophageal squamous cell carcinoma: a review of the intrapapillary capillary loop classification. Ann. Gastroenterol. 28, 41–48 (2015).

    PubMed  PubMed Central  Google Scholar 

  52. Sato, H. et al. Utility of intrapapillary capillary loops seen on magnifying narrow-band imaging in estimating invasive depth of esophageal squamous cell carcinoma. Endoscopy 47, 122–128 (2015).

    PubMed  Google Scholar 

  53. Ide, E., Maluf-Filho, F., Chaves, D. M., Matuguma, S. E. & Sakai, P. Narrow-band imaging without magnification for detecting early esophageal squamous cell carcinoma. World J. Gastroenterol. 17, 4408–4413 (2011).

    PubMed  PubMed Central  Google Scholar 

  54. Lee, C. T. et al. Narrow-band imaging with magnifying endoscopy for the screening of esophageal cancer in patients with primary head and neck cancers. Endoscopy 42, 613–619 (2010).

    CAS  PubMed  Google Scholar 

  55. Goda, K. et al. Narrow-band imaging magnifying endoscopy versus lugol chromoendoscopy with pink-color sign assessment in the diagnosis of superficial esophageal squamous neoplasms: a randomised noninferiority trial. Gastroenterol. Res. Pract. 2015, 639462 (2015).

    PubMed  PubMed Central  Google Scholar 

  56. Nagami, Y. 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. 109, 845–854 (2014).

    PubMed  PubMed Central  Google Scholar 

  57. Kodashima, S. & Fujishiro, M. Novel image-enhanced endoscopy with i-scan technology. World J. Gastroenterol. 16, 1043–1049 (2010).

    PubMed  PubMed Central  Google Scholar 

  58. Coriat, R. et al. Computed virtual chromoendoscopy system (FICE): a new tool for upper endoscopy? Gastroenterol. Clin. Biol. 32, 363–369 (2008).

    CAS  PubMed  Google Scholar 

  59. Camus, M. et al. Helpfulness of the combination of acetic acid and FICE in the detection of Barrett's epithelium and Barrett's associated neoplasias. World J. Gastroenterol. 18, 1921–1925 (2012).

    PubMed  PubMed Central  Google Scholar 

  60. Osawa, H. et al. Diagnosis of endoscopic Barrett's esophagus by transnasal flexible spectral imaging color enhancement. J. Gastroenterol. 44, 1125–1132 (2009).

    PubMed  Google Scholar 

  61. Hoffman, A. et al. Acetic acid compared with i-scan imaging for detecting Barrett's esophagus: a randomized, comparative trial. Gastrointest. Endosc. 79, 46–54 (2014).

    PubMed  Google Scholar 

  62. Verna, C. et al. I-SCAN targeted versus random biopsies in Barrett's oesophagus. Dig. Liver Dis. 46, 131–134 (2014).

    PubMed  Google Scholar 

  63. Kara, M. A. et al. Endoscopic video autofluorescence imaging may improve the detection of early neoplasia in patients with Barrett's esophagus. Gastrointest. Endosc. 61, 679–685 (2005).

    PubMed  Google Scholar 

  64. Kara, M. A., Peters, F. P., Fockens, P., ten Kate, F. J. & Bergman, J. J. Endoscopic video-autofluorescence imaging followed by narrow band imaging for detecting early neoplasia in Barrett's esophagus. Gastrointest. Endosc. 64, 176–185 (2006).

    PubMed  Google Scholar 

  65. Borovicka, J. et al. Autofluorescence endoscopy in surveillance of Barrett's esophagus: a multicenter randomized trial on diagnostic efficacy. Endoscopy 38, 867–872 (2006).

    CAS  PubMed  Google Scholar 

  66. Curvers, W. L. et al. Endoscopic tri-modal imaging for detection of early neoplasia in Barrett's oesophagus: a multi-centre feasibility study using high-resolution endoscopy, autofluorescence imaging and narrow band imaging incorporated in one endoscopy system. Gut 57, 167–172 (2008).

    CAS  PubMed  Google Scholar 

  67. Mannath, J. et al. An inter-observer agreement study of autofluorescence endoscopy in Barrett's esophagus among expert and non-expert endoscopists. Dig. Dis. Sci. 58, 465–470 (2013).

    CAS  PubMed  Google Scholar 

  68. Curvers, W. L. et al. Endoscopic tri-modal imaging is more effective than standard endoscopy in identifying early-stage neoplasia in Barrett's esophagus. Gastroenterology 139, 1106–1114 (2010).

    PubMed  Google Scholar 

  69. Curvers, W. L. et al. Endoscopic trimodal imaging versus standard video endoscopy for detection of early Barrett's neoplasia: a multicenter, randomized, crossover study in general practice. Gastrointest. Endosc. 73, 195–203 (2011).

    PubMed  Google Scholar 

  70. Di, P. M. et al. The combination of autofluorescence endoscopy and molecular biomarkers is a novel diagnostic tool for dysplasia in Barrett's oesophagus. Gut 64, 49–56 (2015).

    Google Scholar 

  71. Wang, T. D. Confocal microscopy from the bench to the bedside. Gastrointest. Endosc. 62, 696–697 (2005).

    PubMed  PubMed Central  Google Scholar 

  72. Kiesslich, R. et al. In vivo histology of Barrett's esophagus and associated neoplasia by confocal laser endomicroscopy. Clin. Gastroenterol. Hepatol. 4, 979–987 (2006).

    PubMed  Google Scholar 

  73. Dunbar, K. B., Okolo, P., I. I. I., Montgomery, E. & Canto, M. I. Confocal laser endomicroscopy in Barrett's esophagus and endoscopically inapparent Barrett's neoplasia: a prospective, randomized, double-blind, controlled, crossover trial. Gastrointest. Endosc. 70, 645–654 (2009).

    PubMed  PubMed Central  Google Scholar 

  74. Xiong, Y. Q., Ma, S. J., Zhou, J. H., Zhong, X. S. & Chen, Q. A meta-analysis of confocal laser endomicroscopy for the detection of neoplasia in patients with Barrett's esophagus. J. Gastroenterol. Hepatol. 31, 1102–1110 (2015).

    Google Scholar 

  75. Sharma, P. et al. Real-time increased detection of neoplastic tissue in Barrett's esophagus with probe-based confocal laser endomicroscopy: final results of an international multicenter, prospective, randomized, controlled trial. Gastrointest. Endosc. 74, 465–472 (2011).

    PubMed  PubMed Central  Google Scholar 

  76. Bertani, H. et al. Improved detection of incident dysplasia by probe-based confocal laser endomicroscopy in a Barrett's esophagus surveillance program. Dig. Dis. Sci. 58, 188–193 (2013).

    PubMed  Google Scholar 

  77. Jayasekera, C., Taylor, A. C., Desmond, P. V., Macrae, F. & Williams, R. Added value of narrow band imaging and confocal laser endomicroscopy in detecting Barrett's esophagus neoplasia. Endoscopy 44, 1089–1095 (2012).

    CAS  PubMed  Google Scholar 

  78. Pohl, H. et al. Miniprobe confocal laser microscopy for the detection of invisible neoplasia in patients with Barrett's oesophagus. Gut 57, 1648–1653 (2008).

    CAS  PubMed  Google Scholar 

  79. Pech, O. et al. Confocal laser endomicroscopy for in vivo diagnosis of early squamous cell carcinoma in the esophagus. Clin. Gastroenterol. Hepatol. 6, 89–94 (2008).

    PubMed  Google Scholar 

  80. Isenberg, G. et al. Accuracy of endoscopic optical coherence tomography in the detection of dysplasia in Barrett's esophagus: a prospective, double-blinded study. Gastrointest. Endosc. 62, 825–831 (2005).

    PubMed  Google Scholar 

  81. Cobb, M. J. et al. Imaging of subsquamous Barrett's epithelium with ultrahigh-resolution optical coherence tomography: a histologic correlation study. Gastrointest. Endosc. 71, 223–230 (2010).

    PubMed  Google Scholar 

  82. Evans, J. A. et al. Optical coherence tomography to identify intramucosal carcinoma and high-grade dysplasia in Barrett's esophagus. Clin. Gastroenterol. Hepatol. 4, 38–43 (2006).

    PubMed  PubMed Central  Google Scholar 

  83. Suter, M. J. et al. Comprehensive microscopy of the esophagus in human patients with optical frequency domain imaging. Gastrointest. Endosc. 68, 745–753 (2008).

    PubMed  PubMed Central  Google Scholar 

  84. Hatta, W. et al. Optical coherence tomography for the staging of tumor infiltration in superficial esophageal squamous cell carcinoma. Gastrointest. Endosc. 71, 899–906 (2010).

    PubMed  Google Scholar 

  85. Fitzgerald, R. C. et al. British Society of Gastroenterology guidelines on the diagnosis and management of Barrett's oesophagus. Gut 63, 7–42 (2014).

    PubMed  Google Scholar 

  86. Manner, H. et al. The frequency of lymph node metastasis in early-stage adenocarcinoma of the esophagus with incipient submucosal invasion (pT1b sm1) depending on histological risk patterns. Surg. Endosc. 29, 1888–1896 (2015).

    PubMed  Google Scholar 

  87. Pech, O. et al. Long-term results and risk factor analysis for recurrence after curative endoscopic therapy in 349 patients with high-grade intraepithelial neoplasia and mucosal adenocarcinoma in Barrett's oesophagus. Gut 57, 1200–1206 (2008).

    CAS  PubMed  Google Scholar 

  88. Shimizu, Y. et al. Metachronous squamous cell carcinoma of the esophagus arising after endoscopic mucosal resection. Gastrointest. Endosc. 54, 190–194 (2001).

    CAS  PubMed  Google Scholar 

  89. Pouw, R. E., Peters, F. P., Sempoux, C., Piessevaux, H. & Deprez, P. H. Stepwise radical endoscopic resection for Barrett's esophagus with early neoplasia: report on a Brussels' cohort. Endoscopy 40, 892–898 (2008).

    CAS  PubMed  Google Scholar 

  90. van Vilsteren, F. G. 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 60, 765–773 (2011).

    PubMed  Google Scholar 

  91. Pouw, R. E. et al. Randomized trial on endoscopic resection-cap versus multiband mucosectomy for piecemeal endoscopic resection of early Barrett's neoplasia. Gastrointest. Endosc. 74, 35–43 (2011).

    PubMed  Google Scholar 

  92. Peters, F. P. et al. Multiband mucosectomy for endoscopic resection of Barrett's esophagus: feasibility study with matched historical controls. Eur. J. Gastroenterol. Hepatol. 19, 311–315 (2007).

    PubMed  Google Scholar 

  93. van Vilsteren, F. G. et al. Learning to perform endoscopic resection of esophageal neoplasia is associated with significant complications even within a structured training program. Endoscopy 44, 4–12 (2012).

    CAS  PubMed  Google Scholar 

  94. Ono, S. et al. Long-term outcomes of endoscopic submucosal dissection for superficial esophageal squamous cell neoplasms. Gastrointest. Endosc. 70, 860–866 (2009).

    PubMed  Google Scholar 

  95. Repici, A. et al. Endoscopic submucosal dissection in patients with early esophageal squamous cell carcinoma: results from a prospective Western series. Gastrointest. Endosc. 71, 715–721 (2010).

    PubMed  Google Scholar 

  96. Yoshinaga, S. et al. Clinical impact of endoscopic submucosal dissection for superficial adenocarcinoma located at the esophagogastric junction. Gastrointest. Endosc. 67, 202–209 (2008).

    PubMed  Google Scholar 

  97. Park, C. H., Kim, E. H., Kim, H. Y., Roh, Y. H. & Lee, Y. C. Clinical outcomes of endoscopic submucosal dissection for early stage esophagogastric junction cancer: a systematic review and meta-analysis. Dig. Liver Dis. 47, 37–44 (2015).

    PubMed  Google Scholar 

  98. Komeda, Y., Bruno, M. & Koch, A. EMR is not inferior to ESD for early Barrett's and EGJ neoplasia: an extensive review on outcome, recurrence and complication rates. Endosc. Int. Open 2, E58–E64 (2014).

    PubMed  PubMed Central  Google Scholar 

  99. Terheggen, G. et al. A randomised trial of endoscopic submucosal dissection versus endoscopic mucosal resection for early Barrett's neoplasia. Gut http://dx.doi.org/10.1136/gutjnl-2015-310126 (2016).

  100. Hammad, H., Kaltenbach, T. & Soetikno, R. Endoscopic submucosal dissection for malignant esophageal lesions. Curr. Gastroenterol. Rep. 16, 386 (2014).

    PubMed  Google Scholar 

  101. Montes, C. G., Brandalise, N. A., Deliza, R., Novais de Magalhaes, A. F. & Ferraz, J. G. Antireflux surgery followed by bipolar electrocoagulation in the treatment of Barrett's esophagus. Gastrointest. Endosc. 50, 173–177 (1999).

    CAS  PubMed  Google Scholar 

  102. Sampliner, R. E. et al. Effective and safe endoscopic reversal of nondysplastic Barrett's esophagus with thermal electrocoagulation combined with high-dose acid inhibition: a multicenter study. Gastrointest. Endosc. 53, 554–558 (2001).

    CAS  PubMed  Google Scholar 

  103. Menon, D., Stafinski, T., Wu, H., Lau, D. & Wong, C. Endoscopic treatments for Barrett's esophagus: a systematic review of safety and effectiveness compared to esophagectomy. BMC Gastroenterol. 10, 111 (2010).

    PubMed  PubMed Central  Google Scholar 

  104. Sharma, P. et al. A randomised controlled trial of ablation of Barrett's oesophagus with multipolar electrocoagulation versus argon plasma coagulation in combination with acid suppression: long term results. Gut 55, 1233–1239 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Barr, H., Kendall, C. & Stone, N. Photodynamic therapy for esophageal cancer: a useful and realistic option. Technol. Cancer Res. Treat. 2, 65–76 (2003).

    PubMed  Google Scholar 

  106. Barr, H., Dix, A. J., Kendall, C. & Stone, N. Review article: the potential role for photodynamic therapy in the management of upper gastrointestinal disease. Aliment. Pharmacol. Ther. 15, 311–321 (2001).

    CAS  PubMed  Google Scholar 

  107. Overholt, B. F. & Panjehpour, M. Photodynamic therapy in Barrett's esophagus. J. Clin. Laser Med. Surg. 14, 245–249 (1996).

    CAS  PubMed  Google Scholar 

  108. Overholt, B. F. & Panjehpour, M. Photodynamic therapy for Barrett's esophagus: clinical update. Am. J. Gastroenterol. 91, 1719–1723 (1996).

    CAS  PubMed  Google Scholar 

  109. Overholt, B. F. et al. Five-year efficacy and safety of photodynamic therapy with Photofrin in Barrett's high-grade dysplasia. Gastrointest. Endosc. 66, 460–468 (2007).

    PubMed  Google Scholar 

  110. Hage, M. et al. 5-Aminolevulinic acid photodynamic therapy versus argon plasma coagulation for ablation of Barrett's oesophagus: a randomised trial. Gut 53, 785–790 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Kelty, C. J. et al. Endoscopic ablation of Barrett's oesophagus: a randomized-controlled trial of photodynamic therapy versus argon plasma coagulation. Aliment. Pharmacol. Ther. 20, 1289–1296 (2004).

    CAS  PubMed  Google Scholar 

  112. Van Laethem, J. L., Jagodzinski, R., Peny, M. O., Cremer, M. & Deviere, J. Argon plasma coagulation in the treatment of Barrett's high-grade dysplasia and in situ adenocarcinoma. Endoscopy 33, 257–261 (2001).

    CAS  PubMed  Google Scholar 

  113. Attwood, S. E., Lewis, C. J., Caplin, S., Hemming, K. & Armstrong, G. Argon beam plasma coagulation as therapy for high-grade dysplasia in Barrett's esophagus. Clin. Gastroenterol. Hepatol. 1, 258–263 (2003).

    PubMed  Google Scholar 

  114. Manner, H. et al. Efficacy and safety of Hybrid-APC for the ablation of Barrett's esophagus. Surg. Endosc. 30, 1364–1370 (2015).

    PubMed  Google Scholar 

  115. Pouw, R. E., Sharma, V. K., Bergman, J. J. & Fleischer, D. E. Radiofrequency ablation for total Barrett's eradication: a description of the endoscopic technique, its clinical results and future prospects. Endoscopy 40, 1033–1040 (2008).

    CAS  PubMed  Google Scholar 

  116. Shaheen, N. J. et al. Radiofrequency ablation in Barrett's esophagus with dysplasia. N. Engl. J. Med. 360, 2277–2288 (2009).

    CAS  PubMed  Google Scholar 

  117. Fleischer, D. E. et al. Endoscopic ablation of Barrett's esophagus: a multicenter study with 2.5-year follow-up. Gastrointest. Endosc. 68, 867–876 (2008).

    PubMed  Google Scholar 

  118. Pouw, R. E. et al. Eradication of Barrett esophagus with early neoplasia by radiofrequency ablation, with or without endoscopic resection. J. Gastrointest. Surg. 12, 1627–1636 (2008).

    PubMed  Google Scholar 

  119. Semlitsch, T. et al. A systematic review of the evidence for radiofrequency ablation for Barrett's esophagus. Surg. Endosc. 24, 2935–2943 (2010).

    PubMed  Google Scholar 

  120. Haidry, R. J. et al. Radiofrequency ablation and endoscopic mucosal resection for dysplastic barrett's esophagus and early esophageal adenocarcinoma: outcomes of the UK National Halo RFA Registry. Gastroenterology 145, 87–95 (2013).

    PubMed  Google Scholar 

  121. Haidry, R. J. et al. Improvement over time in outcomes for patients undergoing endoscopic therapy for Barrett's oesophagus-related neoplasia: 6-year experience from the first 500 patients treated in the UK patient registry. Gut 64, 1192–1199 (2015).

    CAS  PubMed  Google Scholar 

  122. Phoa, K. N. et al. Multimodality endoscopic eradication for neoplastic Barrett oesophagus: results of an European multicentre study (EURO-II). Gut 64, 555–562 (2015).

    Google Scholar 

  123. Phoa, K. N. et al. Radiofrequency ablation versus endoscopic surveillance for patients with Barrett esophagus and low-grade dysplasia: a randomized clinical trial. JAMA 311, 1209–1217 (2014).

    CAS  PubMed  Google Scholar 

  124. He, S. et al. Endoscopic radiofrequency ablation for early esophageal squamous cell neoplasia: report of safety and effectiveness from a large prospective trial. Endoscopy 47, 398–408 (2015).

    PubMed  PubMed Central  Google Scholar 

  125. Haidry, R. J. et al. Radiofrequency ablation for early oesophageal squamous neoplasia: outcomes form United Kingdom registry. World J. Gastroenterol. 19, 6011–6019 (2013).

    PubMed  PubMed Central  Google Scholar 

  126. Xue, H. B. et al. A pilot study of endoscopic spray cryotherapy by pressurized carbon dioxide gas for Barrett's esophagus. Endoscopy 43, 379–385 (2011).

    CAS  PubMed  Google Scholar 

  127. Greenwald, B. D., Dumot, J. A., Horwhat, J. D., Lightdale, C. J. & Abrams, J. A. Safety, tolerability, and efficacy of endoscopic low-pressure liquid nitrogen spray cryotherapy in the esophagus. Dis. Esophagus. 23, 13–19 (2010).

    PubMed  Google Scholar 

  128. Chen, A. M. & Pasricha, P. J. Cryotherapy for Barrett's esophagus: who, how, and why? Gastrointest. Endosc. Clin. N. Am. 21, 111–118 (2011).

    PubMed  Google Scholar 

  129. Canto, M. I. et al. Safety and efficacy of carbon dioxide cryotherapy for treatment of neoplastic Barrett's esophagus. Endoscopy 47, 582–591 (2015).

    PubMed  Google Scholar 

  130. Gosain, S., Mercer, K., Twaddell, W. S., Uradomo, L. & Greenwald, B. D. Liquid nitrogen spray cryotherapy in Barrett's esophagus with high-grade dysplasia: long-term results. Gastrointest. Endosc. 78, 260–265 (2013).

    PubMed  Google Scholar 

  131. Verbeek, R. E., Vleggaar, F. P., ten Kate, F. J., van Baal, J. W. & Siersema, P. D. Cryospray ablation using pressurized CO2 for ablation of Barrett's esophagus with early neoplasia: early termination of a prospective series. Endosc. Int. Open. 3, E107–E112 (2015).

    PubMed  PubMed Central  Google Scholar 

  132. Goda, K. et al. Dual-focus versus conventional magnification endoscopy for the diagnosis of superficial squamous neoplasms in the pharynx and esophagus: a randomized trial. Endoscopy 48, 321–329 (2016).

    PubMed  Google Scholar 

  133. Kodashima, S. et al. Evaluation of a new image-enhanced endoscopic technology using band-limited light for detection of esophageal squamous cell carcinoma. Dig. Endosc. 26, 164–171 (2014).

    PubMed  Google Scholar 

  134. Osawa, H. & Yamamoto, H. Present and future status of flexible spectral imaging color enhancement and blue laser imaging technology. Dig. Endosc. 26 (Suppl. 1), 105–115 (2014).

    PubMed  Google Scholar 

  135. Sturm, M. B. & Wang, T. D. Emerging optical methods for surveillance of Barrett's oesophagus. Gut 64, 1816–1823 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Bird-Lieberman, E. L. et al. Molecular imaging using fluorescent lectins permits rapid endoscopic identification of dysplasia in Barrett's esophagus. Nat. Med. 18, 315–321 (2012).

    CAS  PubMed  Google Scholar 

  137. Sturm, M. B. et al. In vivo molecular imaging of Barrett's esophagus with confocal laser endomicroscopy. Gastroenterology 145, 56–58 (2013).

    PubMed  Google Scholar 

  138. Scholvinck, D. W. et al. Treatment of Barrett's esophagus with a novel focal cryoablation device: a safety and feasibility study. Endoscopy 47, 1106–1112 (2015).

    PubMed  Google Scholar 

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Authors and Affiliations

  1. University Hospitals Coventry and Warwickshire NHS Trust, Clifford Bridge Road, Coventry, CV2 2DX, UK

    Jayan Mannath

  2. NIHR Nottingham Digestive Diseases Biomedical Research Unit, Queens Medical Centre, Nottingham University Hospitals NHS Trust, Derby Road, NG7 2UH, Nottingham, UK

    Krish Ragunath

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  1. Jayan Mannath
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K.R. and J.M. researched data for article, discussed content and wrote the article. K.R. reviewed and edited the manuscript before submission.

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Correspondence to Krish Ragunath.

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Competing interests

K.R. has received speaker honoraria, consultancy fees, research and educational grants from Boston Scientific, Cook Medical, Covidien, ERBE, Olympus and Pentax Medical. J.M. reports no competing interest.

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Mannath, J., Ragunath, K. Role of endoscopy in early oesophageal cancer. Nat Rev Gastroenterol Hepatol 13, 720–730 (2016). https://doi.org/10.1038/nrgastro.2016.148

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