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What Constitutes Optimal Management of T1N0 Esophageal Adenocarcinoma?

  • Fariha H. Ramay
  • Ashley A. Vareedayah
  • Kavel Visrodia
  • Prasad G. Iyer
  • Kenneth K. Wang
  • Swathi Eluri
  • Nicholas J. Shaheen
  • Rishindra Reddy
  • Linda W. Martin
  • Bruce D. Greenwald
  • Melanie A. Edwards
Gastrointestinal Oncology
  • 46 Downloads

Abstract

Purpose and Design

Esophageal adenocarcinoma (EAC) develops as a consequence of gastroesophageal reflux disease and Barrett’s esophagus (BE). While combination therapy with chemotherapy or concurrent chemoradiotherapy followed by esophagectomy improves survival in more advanced tumors, the optimal treatment strategy for early-stage EAC is undefined. Endoscopic eradication therapy, consisting of endoscopic resection and mucosal ablation, has revolutionized therapy for superficial (T1a) EAC in BE and allows for esophageal preservation in appropriate patients at low risk for lymph node metastasis (LNM). This review critically examines the literature regarding evaluation, treatment, and outcomes in patients with T1 EAC.

Methods

The literature was queried via the PubMed database to include articles published between 1990 and 2017. Search terms were generated from the key statements “Endoscopic eradication therapy results in equivalent overall survival when compared to esophagectomy for clinical T1aN0 EAC” and “Esophagectomy provides better overall survival than endoscopic eradication therapy for cT1b EAC”. Abstracts were reviewed and included according to predefined selection and exclusion criteria, and were then assessed according to the GRADE system.

Results and Conclusions

In patients with T1aN0 EAC, overall survival with endoscopic eradication therapy is equal to esophagectomy. Given the substantial risk of LNM in patients with submucosal (T1b) EAC, esophagectomy remains the standard of care for surgical candidates. In the case of inoperability or low-risk lesions, endoscopic resection may be considered adequate therapy. Chemotherapy and radiation can be offered as primary therapy for non-surgical candidates with lesions not amenable to endoscopic therapy, but does not have a clear role in the adjuvant setting after either endoscopic or surgical resection.

Notes

Funding

Research reported in this publication was supported by the University of Maryland under Award No. T32DK067872 (FR). The content is solely the responsibility of the authors and does not necessarily reflect the views of the National Institutes of Health.

DISCLOSURE

Fariha H. Ramay, Ashley A. Vareedayah, Kavel Visrodia, Prasad G. Iyer, Kenneth K. Wang, Swathi Eluri, Nicholas J. Shaheen, Rishindra Reddy, Linda W. Martin, Bruce D. Greenwald, and Melanie A. Edwards have no conflicts of interest to disclose.

References

  1. 1.
    Cunningham D, Allum WH, Stenning SP, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006;355(1):11–20.Google Scholar
  2. 2.
    Shapiro J, van Lanschot JJ, Hulshof MC, et al. Neoadjuvant chemoradiotherapy plus surgery versus surgery alone for oesophageal or junctional cancer (CROSS): long-term results of a randomised controlled trial. Lancet Oncol. 2015;16(9):1090–98.Google Scholar
  3. 3.
    Pech O, May A, Manner H, et al. Long-term efficacy and safety of endoscopic resection for patients with mucosal adenocarcinoma of the esophagus. Gastroenterology. 2014;146(3):652–660 e651.Google Scholar
  4. 4.
    Ancona E, Rampado S, Cassaro M, et al. Prediction of lymph node status in superficial esophageal carcinoma. Ann Surg Oncol. 2008;15(11):3278–88.Google Scholar
  5. 5.
    Bogoevski D, Bockhorn M, Koenig A, et al. How radical should surgery be for early esophageal cancer? World J Surg. 2011;35(6):1311–20.Google Scholar
  6. 6.
    Bolton WD, Hofstetter WL, Francis AM, et al. Impact of tumor length on long-term survival of pT1 esophageal adenocarcinoma. J Thorac Cardiovasc Surg. 2009;138(4):831–36.Google Scholar
  7. 7.
    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(6):850–62 (quiz 863).Google Scholar
  8. 8.
    Estrella JS, Hofstetter WL, Correa AM, et al. Duplicated muscularis mucosae invasion has similar risk of lymph node metastasis and recurrence-free survival as intramucosal esophageal adenocarcinoma. Am J Surg Pathol. 2011;35(7):1045–53.Google Scholar
  9. 9.
    Leers JM, DeMeester SR, Oezcelik A, et al. The prevalence of lymph node metastases in patients with T1 esophageal adenocarcinoma a retrospective review of esophagectomy specimens. Ann Surg. 2011;253(2):271–78.Google Scholar
  10. 10.
    Lorenz D, Origer J, Pauthner M, et al. Prognostic risk factors of early esophageal adenocarcinomas. Ann Surg. 2014;259(3):469–76.Google Scholar
  11. 11.
    Rice TW, Blackstone EH, Goldblum JR, et al. Superficial adenocarcinoma of the esophagus. J Thorac Cardiovasc Surg. 2001;122(6):1077–90.Google Scholar
  12. 12.
    Sepesi B, Watson TJ, Zhou D, et al. Are endoscopic therapies appropriate for superficial submucosal esophageal adenocarcinoma? An analysis of esophagectomy specimens. J Am Coll Surg. 2010;210(4):418–27.Google Scholar
  13. 13.
    Stein HJ, Feith M, Bruecher BL, Naehrig J, Sarbia M, Siewert JR. Early esophageal cancer: pattern of lymphatic spread and prognostic factors for long-term survival after surgical resection. Ann Surg. 2005;242(4):566–73 (discussion 573–565).Google Scholar
  14. 14.
    Stein HJ, Feith M, Mueller J, Werner M, Siewert JR. Limited resection for early adenocarcinoma in Barrett’s esophagus. Ann Surg. 2000;232(6):733–42.Google Scholar
  15. 15.
    Westerterp M, Koppert LB, Buskens CJ, et al. Outcome of surgical treatment for early adenocarcinoma of the esophagus or gastro-esophageal junction. Virchows Arch. 2005;446(5):497–04.Google Scholar
  16. 16.
    Dhupar R, Rice RD, Correa AM, et al. endoscopic ultrasound estimates for tumor depth at the gastroesophageal junction are inaccurate: implications for the liberal use of endoscopic resection. Ann Thorac Surg. 2015;100(5):1812–16.Google Scholar
  17. 17.
    McDonough PB, Jones DR, Shen KR, et al. Does FDG-PET add information to EUS and CT in the initial management of esophageal cancer? A prospective single center study. Am J Gastroenterol. 2008;103(3):570–74.Google Scholar
  18. 18.
    Pouw RE, Heldoorn N, Alvarez Herrero L, et al. Do we still need EUS in the workup of patients with early esophageal neoplasia? A retrospective analysis of 131 cases. Gastrointest Endosc. 2011;73(4):662–68.Google Scholar
  19. 19.
    Rampado S, Bocus P, Battaglia G, Ruol A, Portale G, Ancona E. Endoscopic ultrasound: accuracy in staging superficial carcinomas of the esophagus. Ann Thorac Surg. 2008;85(1):251–56.Google Scholar
  20. 20.
    Prasad GA, Wu TT, Wigle DA, et al. Endoscopic and surgical treatment of mucosal (T1a) esophageal adenocarcinoma in Barrett’s esophagus. Gastroenterology. 2009;137(3):815–23.Google Scholar
  21. 21.
    Schunemann HJ, Oxman AD, Brozek J, et al. Grading quality of evidence and strength of recommendations for diagnostic tests and strategies. BMJ. 2008;336(7653):1106–10.Google Scholar
  22. 22.
    Zehetner J, DeMeester SR, Hagen JA, et al. Endoscopic resection and ablation versus esophagectomy for high-grade dysplasia and intramucosal adenocarcinoma. J Thorac Cardiovasc Surg. 2011;141(1):39–47.Google Scholar
  23. 23.
    Barbour AP, Jones M, Brown I, et al. Risk stratification for early esophageal adenocarcinoma: analysis of lymphatic spread and prognostic factors. Ann Surg Oncol. 2010;17(9):2494–02.Google Scholar
  24. 24.
    Kaneshiro DK, Post JC, Rybicki L, Rice TW, Goldblum JR. Clinical significance of the duplicated muscularis mucosae in Barrett esophagus-related superficial adenocarcinoma. Am J Surg Pathol. 2011;35(5):697–700.Google Scholar
  25. 25.
    Kauppi J, Gockel I, Rantanen T, et al. Cause of death during long-term follow-up for superficial esophageal adenocarcinoma. Ann Surg Oncol. 2013;20(7):2428–33.Google Scholar
  26. 26.
    Ngamruengphong S, Wolfsen HC, Wallace MB. Survival of patients with superficial esophageal adenocarcinoma after endoscopic treatment vs surgery. Clin Gastroenterol Hepatol. 2013;11(11):1424–1429 e1422 (quiz e1481).Google Scholar
  27. 27.
    Nurkin SJ, Nava HR, Yendamuri S, et al. Outcomes of endoscopic resection for high-grade dysplasia and esophageal cancer. Surg Endosc. 2014;28(4):1090–95.Google Scholar
  28. 28.
    Oh DS, Hagen JA, Chandrasoma PT, et al. Clinical biology and surgical therapy of intramucosal adenocarcinoma of the esophagus. J Am Coll Surg. 2006;203(2):152–61.Google Scholar
  29. 29.
    Pech O, Bollschweiler E, Manner H, Leers J, Ell C, Holscher AH. Comparison between endoscopic and surgical resection of mucosal esophageal adenocarcinoma in Barrett’s esophagus at two high-volume centers. Ann Surg. 2011;254(1):67–72.Google Scholar
  30. 30.
    Peyre CG, DeMeester SR, Rizzetto C, et al. Vagal-sparing esophagectomy: the ideal operation for intramucosal adenocarcinoma and barrett with high-grade dysplasia. Ann Surg. 2007;246(4):665–71 (discussion 671–664).Google Scholar
  31. 31.
    Saha AK, Sutton CD, Sue-Ling H, Dexter SP, Sarela AI. Comparison of oncological outcomes after laparoscopic transhiatal and open esophagectomy for T1 esophageal adenocarcinoma. Surg Endosc. 2009;23(1):119–24.Google Scholar
  32. 32.
    Wu J, Pan YM, Wang TT, Gao DJ, Hu B. Endotherapy versus surgery for early neoplasia in Barrett’s esophagus: a meta-analysis. Gastrointest Endosc. 2014;79(2):233–241 e232.Google Scholar
  33. 33.
    Manner H, Wetzka J, May A, et al. Early-stage adenocarcinoma of the esophagus with mid to deep submucosal invasion (pT1b sm2-3): the frequency of lymph-node metastasis depends on macroscopic and histological risk patterns. Dis Esophagus. 2017;30(3):1–11.Google Scholar
  34. 34.
    Cummings LC, Kou TD, Schluchter MD, Chak A, Cooper GS. Outcomes after endoscopic versus surgical therapy for early esophageal cancers in an older population. Gastrointest Endosc. 2016;84(2):232–240.e1.Google Scholar
  35. 35.
    Schmidt HM, Mohiuddin K, Bodnar AM, et al. Multidisciplinary treatment of T1a adenocarcinoma in Barrett’s esophagus: contemporary comparison of endoscopic and surgical treatment in physiologically fit patients. Surg Endosc. 2016;30(8):3391–01.Google Scholar
  36. 36.
    Pech O, Gossner L, May A, et al. Long-term results of photodynamic therapy with 5-aminolevulinic acid for superficial Barrett’s cancer and high-grade intraepithelial neoplasia. Gastrointest Endosc. 2005;62(1):24–30.Google Scholar
  37. 37.
    Sgourakis G, Gockel I, Lang H. Endoscopic and surgical resection of T1a/T1b esophageal neoplasms: a systematic review. World J Gastroenterol. 2013;19(9):1424–37.Google Scholar
  38. 38.
    Pech O, Behrens A, May A, 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. 2008;57(9):1200–06.Google Scholar
  39. 39.
    Shaheen NJ, Falk GW, Iyer PG, Gerson LB, American College of Gastroenterology. ACG clinical guideline: diagnosis and management of Barrett’s esophagus. Am J Gastroenterol. 2016;111(1):30–50 (quiz 51).Google Scholar
  40. 40.
    Ramay FH, Cui Q, Greenwald BD. Outcomes after liquid nitrogen spray cryotherapy in Barrett’s esophagus-associated high-grade dysplasia and intramucosal adenocarcinoma: 5-year follow-up. Gastrointest Endosc. 2017;86(4):626–32.Google Scholar
  41. 41.
    Tsai FC, Ghorbani S, Greenwald BD, et al. Safety and efficacy of endoscopic spray cryotherapy for esophageal cancer. Dis Esophagus. 2017;30(11):1–7.Google Scholar
  42. 42.
    Neuhaus H, Terheggen G, Rutz EM, Vieth M, Schumacher B. Endoscopic submucosal dissection plus radiofrequency ablation of neoplastic Barrett’s esophagus. Endoscopy. 2012;44(12):1105–13.Google Scholar
  43. 43.
    Probst A, Aust D, Markl B, Anthuber M, Messmann H. Early esophageal cancer in Europe: endoscopic treatment by endoscopic submucosal dissection. Endoscopy. 2015;47(2):113–21.Google Scholar
  44. 44.
    Chevaux JB, Piessevaux H, Jouret-Mourin A, Yeung R, Danse E, Deprez PH. Clinical outcome in patients treated with endoscopic submucosal dissection for superficial Barrett’s neoplasia. Endoscopy. 2015;47(2):103–12.Google Scholar
  45. 45.
    Hobel S, Dautel P, Baumbach R, et al. Single center experience of endoscopic submucosal dissection (ESD) in early Barrett’s adenocarcinoma. Surg Endosc. 2015;29(6):1591–97.Google Scholar
  46. 46.
    Barret M, Cao DT, Beuvon F, et al. Endoscopic submucosal dissection for early Barrett’s neoplasia. United European Gastroenterol J. 2016;4(2):207–15.Google Scholar
  47. 47.
    Yang D, Coman RM, Kahaleh M, et al. Endoscopic submucosal dissection for Barrett’s early neoplasia: a multicenter study in the United States. Gastrointest Endosc. 2017;86(4):600–07.Google Scholar
  48. 48.
    Coman RM, Gotoda T, Forsmark CE, Draganov PV. Prospective evaluation of the clinical utility of endoscopic submucosal dissection (ESD) in patients with Barrett’s esophagus: a Western center experience. Endosc Int Open. 2016;4(6):E715–721.Google Scholar
  49. 49.
    Terheggen G, Horn EM, Vieth M, et al. A randomised trial of endoscopic submucosal dissection versus endoscopic mucosal resection for early Barrett’s neoplasia. Gut. 2017;66(5):783–93.Google Scholar
  50. 50.
    Cao Y, Liao C, Tan A, Gao Y, Mo Z, Gao F. Meta-analysis of endoscopic submucosal dissection versus endoscopic mucosal resection for tumors of the gastrointestinal tract. Endoscopy. 2009;41(9):751–57.Google Scholar
  51. 51.
    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(3):248–53.Google Scholar
  52. 52.
    Sihag S, Kosinski AS, Gaissert HA, Wright CD, Schipper PH. Minimally invasive versus open esophagectomy for esophageal cancer: a comparison of early surgical outcomes from the society of thoracic surgeons national database. Ann Thorac Surg. 2016;101(4):1281–89.Google Scholar
  53. 53.
    Manner H, Pech O, Heldmann Y, et al. Efficacy, safety, and long-term results of endoscopic treatment for early stage adenocarcinoma of the esophagus with low-risk sm1 invasion. Clin Gastroenterol Hepatol. 2013;11(6):630–35 (quiz e645).Google Scholar
  54. 54.
    Tian J, Prasad GA, Lutzke LS, Lewis JT, Wang KK. Outcomes of T1b esophageal adenocarcinoma patients. Gastrointest Endosc. 2011;74(6):1201–06.Google Scholar
  55. 55.
    The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc. 2003;58(6 Suppl):S3–43.Google Scholar
  56. 56.
    Gaur P, Sepesi B, Hofstetter WL, et al. A clinical nomogram predicting pathologic lymph node involvement in esophageal cancer patients. Ann Surg. 2010;252(4):611–17.Google Scholar
  57. 57.
    Gertler R, Stein HJ, Schuster T, Rondak IC, Hofler H, Feith M. Prevalence and topography of lymph node metastases in early esophageal and gastric cancer. Ann Surg. 2014;259(1):96–01.Google Scholar
  58. 58.
    Lee L, Ronellenfitsch U, Hofstetter WL, et al. Predicting lymph node metastases in early esophageal adenocarcinoma using a simple scoring system. J Am Coll Surg. 2013;217(2):191–99.Google Scholar
  59. 59.
    The National Comprehensive Cancer Network (NCCN) Clinical Practice Guidelines in Oncology-Esophageal and Esophagogastric Junction Cancers. 2017; Version 1.2017.Google Scholar

Copyright information

© Society of Surgical Oncology 2019

Authors and Affiliations

  • Fariha H. Ramay
    • 1
  • Ashley A. Vareedayah
    • 2
  • Kavel Visrodia
    • 3
  • Prasad G. Iyer
    • 3
  • Kenneth K. Wang
    • 3
  • Swathi Eluri
    • 4
  • Nicholas J. Shaheen
    • 4
  • Rishindra Reddy
    • 5
  • Linda W. Martin
    • 6
  • Bruce D. Greenwald
    • 1
  • Melanie A. Edwards
    • 7
  1. 1.Division of Gastroenterology and Hepatology, Department of MedicineUniversity of Maryland School of MedicineBaltimoreUSA
  2. 2.Division of Gastroenterology and Hepatology, Department of MedicineSaint Louis University School of MedicineSt. LouisUSA
  3. 3.Division of Gastroenterology and HepatologyMayo ClinicRochesterUSA
  4. 4.Division of Gastroenterology and HepatologyUniversity of North Carolina at Chapel HillChapel HillUSA
  5. 5.Department of Thoracic SurgeryUniversity of Michigan Medical CenterAnn ArborUSA
  6. 6.Division of Thoracic Surgery, Department of SurgeryUniversity of VirginiaCharlottesvilleUSA
  7. 7.Cardiovascular and Thoracic SurgeryIntegrated Health AssociatesYpsilantiUSA

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