Journal of Gastrointestinal Surgery

, Volume 13, Issue 12, pp 2104–2112 | Cite as

Transoral Endoscopic Inner Layer Esophagectomy: Management of High-Grade Dysplasia and Superficial Cancer with Organ Preservation

  • Bart P. L. Witteman
  • Tyler J. Foxwell
  • Sandy Monsheimer
  • Andres Gelrud
  • George M. Eid
  • Alejandro Nieponice
  • Robert W. O’Rourke
  • Toshitaka Hoppo
  • Nicole D. Bouvy
  • Stephen F. Badylak
  • Blair A. JobeEmail author
2009 SSAT Plenary Presentation



Limitations of endoscopic therapies for Barrett’s esophagus and superficial cancer include a compromised histological assessment, the need for surveillance, subsequent procedures, and stricture formation. Circumferential en bloc resection of the mucosa–submucosa complex followed by deployment of a biologic scaffold onto the remaining muscularis propria may address these concerns. The objective of this study was to determine technical feasibility of transoral resection of the esophageal lining.

Materials and Methods

Transoral endoscopic inner layer esophagectomy was performed in ten swine. Endpoints included procedure duration, hemorrhage, number of perforations, and adequacy of resection length and depth.


Procedures were successfully completed in all animals without perioperative mortality. Procedure times averaged 179 min (range 125–320). No perforations were found, and a mean of 1.7 (0–4) interventions for hemorrhage was required. Complete longitudinal resection was achieved in nine of ten animals. Resection depth included all mucosal layers in 100% of tissue sections, the submucosal layers, SM1 in 100%, and SM2 in 96%. A portion of SM3 was adherent to the muscularis propria in 70%.


Transoral endoscopic resection of the inner esophageal layers was feasible and reproducible. This technique may facilitate a single-step definitive treatment and staging tool for early neoplastic lesions, obviating the need for esophagectomy.


Endoscopy Esophagus Barrett’s esophagus High-grade dysplasia Esophagectomy Cancer Transoral Incisionless 



Transoral endoscopic inner layer esophagectomy


Mucosa–submucosa complex


Conflict of Interest

The authors report that there are no disclosures relevant to this publication.


This study was supported by the Robert Anthony McHugh Research Fund for the Prevention and Early Detection of Esophageal Cancer, an American Surgical Association Foundation Fellowship Award (RWO), and National Institutes of Health grants K23 DK066165-01 (BAJ) and K08 DK074397 (RWO).

Supplementary material

ESM Video 1

(WMV 14.3 MB)

ESM Video 2

(WMV 11.5 MB)

ESM Video 3

(WMV 356 MB)


  1. 1.
    DeMeester SR. New options for the therapy of Barrett’s high-grade dysplasia and intramucosal adenocarcinoma: endoscopic mucosal resection and ablation versus vagal-sparing esophagectomy. Ann Thorac Surg 2008;85:S747–750.CrossRefPubMedGoogle Scholar
  2. 2.
    Shaheen NJ, Sharma P, Overholt BF, Wolfsen HC, Sampliner RE, Wang KK, Galanko JA, Bronner MP, Goldblum JR, Bennett AE, Jobe BA, Eisen GM, Fennerty MB, Hunter JG, Fleischer DE, Sharma VK, Hawes RH, Hoffman BJ, Rothstein RI, Gordon SR, Mashimo H, Chang KJ, Muthusamy VR, Edmundowicz SA, Spechler SJ, Siddiqui AA, Souza RF, Infantolino A, Falk GW, Kimmey MB, Madanick RD, Chak A, Lightdale CJ. Radiofrequency ablation in Barrett’s esophagus with dysplasia. N Engl J Med 2009;360:2277–2288.CrossRefPubMedGoogle Scholar
  3. 3.
    Thomas P, Doddoli C, Neville P, Pons J, Lienne P, Giudicelli R, Giovannini M, Seitz JF, Fuentes P. Esophageal cancer resection in the elderly. Eur J Cardiothorac Surg 1996;10:941–946.CrossRefPubMedGoogle Scholar
  4. 4.
    Ell C, May A, Pech O, Gossner L, Guenter E, Behrens A, Nachbar L, Huijsmans J, Vieth M, Stolte M. Curative endoscopic resection of early esophageal adenocarcinomas (Barrett’s cancer). Gastrointest Endosc 2007;65:3–10.CrossRefPubMedGoogle Scholar
  5. 5.
    Holscher AH, Bollschweiler E, Schneider PM, Siewert JR. Early adenocarcinoma in Barrett’s oesophagus. Br J Surg 1997;84:1470–1473.CrossRefPubMedGoogle Scholar
  6. 6.
    Oh DS, Hagen JA, Chandrasoma PT, Dunst CM, Demeester SR, Alavi M, Bremner CG, Lipham J, Rizzetto C, Cote R, Demeester TR. Clinical biology and surgical therapy of intramucosal adenocarcinoma of the esophagus. J Am Coll Surg 2006;203:152–161.CrossRefPubMedGoogle Scholar
  7. 7.
    Rice TW, Blackstone EH, Adelstein DJ, Zuccaro G Jr., Vargo JJ, Goldblum JR, Murthy SC, DeCamp MM, Rybicki LA. Role of clinically determined depth of tumor invasion in the treatment of esophageal carcinoma. J Thorac Cardiovasc Surg 2003;125:1091–1102.CrossRefPubMedGoogle Scholar
  8. 8.
    Rice TW, Zuccaro G Jr., Adelstein DJ, Rybicki LA, Blackstone EH, Goldblum JR. Esophageal carcinoma: depth of tumor invasion is predictive of regional lymph node status. Ann Thorac Surg 1998;65:787–792.CrossRefPubMedGoogle Scholar
  9. 9.
    Farrell JJ, Lauwers GY, Brugge WR. Endoscopic mucosal resection using a cap-fitted endoscope improves tissue resection and pathology interpretation: an animal study. Gastric Cancer 2006;9:3–8.CrossRefPubMedGoogle Scholar
  10. 10.
    Ahmadi A, Draganov P. Endoscopic mucosal resection in the upper gastrointestinal tract. World J Gastroenterol 2008;14:1984–1989.CrossRefPubMedGoogle Scholar
  11. 11.
    Kakushima N, Yahagi N, Fujishiro M, Kodashima S, Nakamura M, Omata M. Efficacy and safety of endoscopic submucosal dissection for tumors of the esophagogastric junction. Endoscopy 2006;38:170–174.CrossRefPubMedGoogle Scholar
  12. 12.
    Yoshinaga S, Gotoda T, Kusano C, Oda I, Nakamura K, Takayanagi R. Clinical impact of endoscopic submucosal dissection for superficial adenocarcinoma located at the esophagogastric junction. Gastrointest Endosc 2008;67:202–209.CrossRefPubMedGoogle Scholar
  13. 13.
    Oyama T, Tomori A, Hotta K, Morita S, Kominato K, Tanaka M, Miyata Y. Endoscopic submucosal dissection of early esophageal cancer. Clin Gastroenterol Hepatol 2005;3:S67–70.CrossRefPubMedGoogle Scholar
  14. 14.
    Kamler JP, Borsatto R, Binmoeller KF. Circumferential endoscopic mucosal resection in the swine esophagus assisted by a cap attachment. Gastrointest Endosc 2002;55:923–928.CrossRefPubMedGoogle Scholar
  15. 15.
    Katada C, Muto M, Manabe T, Boku N, Ohtsu A, Yoshida S. Esophageal stenosis after endoscopic mucosal resection of superficial esophageal lesions. Gastrointest Endosc 2003;57:165–169.CrossRefPubMedGoogle Scholar
  16. 16.
    Conio M, Sorbi D, Batts KP, Gostout CJ. Endoscopic circumferential esophageal mucosectomy in a porcine model: an assessment of technical feasibility, safety, and outcome. Endoscopy 2001;33:791–794.CrossRefPubMedGoogle Scholar
  17. 17.
    Kudo S. Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy 1993;25:455–461.CrossRefPubMedGoogle Scholar
  18. 18.
    Ono H, Kondo H, Gotoda T, Shirao K, Yamaguchi H, Saito D, Hosokawa K, Shimoda T, Yoshida S. Endoscopic mucosal resection for treatment of early gastric cancer. Gut 2001;48:225–229.CrossRefPubMedGoogle Scholar
  19. 19.
    Endo M, Yoshino K, Kawano T, Nagai K, Inoue H. Clinicopathologic analysis of lymph node metastasis in surgically resected superficial cancer of the thoracic esophagus. Dis Esophagus 2000;13:125–129.CrossRefPubMedGoogle Scholar
  20. 20.
    Ries LA, Wingo PA, Miller DS, Howe HL, Weir HK, Rosenberg HM, Vernon SW, Cronin K, Edwards BK. The annual report to the nation on the status of cancer, 1973–1997, with a special section on colorectal cancer. Cancer 2000;88:2398–2424.CrossRefPubMedGoogle Scholar
  21. 21.
    Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med 2003;349:2241–2252.CrossRefPubMedGoogle Scholar
  22. 22.
    Fitzgerald RC, Saeed IT, Khoo D, Farthing MJ, Burnham WR. Rigorous surveillance protocol increases detection of curable cancers associated with Barrett’s esophagus. Dig Dis Sci 2001;46:1892–1898.CrossRefPubMedGoogle Scholar
  23. 23.
    van Sandick JW, van Lanschot JJ, Kuiken BW, Tytgat GN, Offerhaus GJ, Obertop H. Impact of endoscopic biopsy surveillance of Barrett’s oesophagus on pathological stage and clinical outcome of Barrett’s carcinoma. Gut 1998;43:216–222.PubMedCrossRefGoogle Scholar
  24. 24.
    Overholt BF, Panjehpour M, Halberg DL. Photodynamic therapy for Barrett’s esophagus with dysplasia and/or early stage carcinoma: long-term results. Gastrointest Endosc 2003;58:183–188.CrossRefPubMedGoogle Scholar
  25. 25.
    Prasad GA, Wang KK, Buttar NS, Wongkeesong LM, Krishnadath KK, Nichols FC 3rd, Lutzke LS, Borkenhagen LS. Long-term survival following endoscopic and surgical treatment of high-grade dysplasia in Barrett’s esophagus. Gastroenterology 2007;132:1226–1233.CrossRefPubMedGoogle Scholar
  26. 26.
    Ganz RA, Overholt BF, Sharma VK, Fleischer DE, Shaheen NJ, Lightdale CJ, Freeman SR, Pruitt RE, Urayama SM, Gress F, Pavey DA, Branch MS, Savides TJ, Chang KJ, Muthusamy VR, Bohorfoush AG, Pace SC, DeMeester SR, Eysselein VE, Panjehpour M, Triadafilopoulos G. Circumferential ablation of Barrett’s esophagus that contains high-grade dysplasia: a U.S. multicenter registry. Gastrointest Endosc 2008;68:35–40.CrossRefPubMedGoogle Scholar
  27. 27.
    Giovannini M, Bories E, Pesenti C, Moutardier V, Monges G, Danisi C, Lelong B, Delpero JR. Circumferential endoscopic mucosal resection in Barrett’s esophagus with high-grade intraepithelial neoplasia or mucosal cancer. Preliminary results in 21 patients. Endoscopy 2004;36:782–787.CrossRefPubMedGoogle Scholar
  28. 28.
    Lopes CV, Hela M, Pesenti C, Bories E, Caillol F, Monges G, Giovannini M. Circumferential endoscopic resection of Barrett’s esophagus with high-grade dysplasia or early adenocarcinoma. Surg Endosc 2007;21:820–824.CrossRefPubMedGoogle Scholar
  29. 29.
    Ishihara R, Iishi H, Uedo N, Takeuchi Y, Yamamoto S, Yamada T, Masuda E, Higashino K, Kato M, Narahara H, Tatsuta M. Comparison of EMR and endoscopic submucosal dissection for en bloc resection of early esophageal cancers in Japan. Gastrointest Endosc 2008;68:1066–1072.CrossRefPubMedGoogle Scholar
  30. 30.
    von Delius S, Feussner H, Henke J, Schneider A, Hollweck R, Rosch T, Prinz C, Schmid RM, Frimberger E. Submucosal endoscopy: a novel approach to en bloc endoscopic mucosal resection (with videos). Gastrointest Endosc 2007;66:753–756.CrossRefGoogle Scholar
  31. 31.
    Willingham FF, Gee DW, Sylla P, Lauwers GY, Rattner DW, Brugge WR. En bloc esophageal mucosectomy for concentric circumferential mucosal resection (with video). Gastrointest Endosc 2009;69:147–151.CrossRefPubMedGoogle Scholar
  32. 32.
    Akiyama H, Tsurumaru M, Ono Y, Udagawa H, Kajiyama Y. Esophagectomy without thoracotomy with vagal preservation. J Am Coll Surg 1994;178:83–85.PubMedGoogle Scholar
  33. 33.
    Nigro JJ, Hagen JA, DeMeester TR, DeMeester SR, Peters JH, Oberg S, Theisen J, Kiyabu M, Crookes PF, Bremner CG. Prevalence and location of nodal metastases in distal esophageal adenocarcinoma confined to the wall: implications for therapy. J Thorac Cardiovasc Surg 1999;117:16–23. discussion 23–15.CrossRefPubMedGoogle Scholar
  34. 34.
    Nieponice A, Gilbert TW, Badylak SF. Reinforcement of esophageal anastomoses with an extracellular matrix scaffold in a canine model. Ann Thorac Surg 2006;82:2050–2058.CrossRefPubMedGoogle Scholar
  35. 35.
    Nieponice A, McGrath K, Qureshi I, Beckman EJ, Luketich JD, Gilbert TW, Badylak SF. An extracellular matrix scaffold for esophageal stricture prevention after circumferential EMR. Gastrointest Endosc 2008;69:289–296.CrossRefPubMedGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2009

Authors and Affiliations

  • Bart P. L. Witteman
    • 1
  • Tyler J. Foxwell
    • 1
  • Sandy Monsheimer
    • 1
  • Andres Gelrud
    • 2
  • George M. Eid
    • 3
  • Alejandro Nieponice
    • 3
    • 4
  • Robert W. O’Rourke
    • 5
  • Toshitaka Hoppo
    • 1
  • Nicole D. Bouvy
    • 6
  • Stephen F. Badylak
    • 3
    • 4
  • Blair A. Jobe
    • 1
    • 7
    Email author
  1. 1.Division of Thoracic and Foregut Surgery, Heart, Lung and Esophageal Surgery InstituteUniversity of PittsburghPittsburghUSA
  2. 2.Department of Medicine, Division of GastroenterologyUniversity of PittsburghPittsburghUSA
  3. 3.Department of SurgeryUniversity of PittsburghPittsburghUSA
  4. 4.McGowan Institute for Regenerative MedicineUniversity of PittsburghPittsburghUSA
  5. 5.Department of SurgeryOregon Health & Science UniversityPortlandUSA
  6. 6.Department of SurgeryMaastricht University Medical CentreMaastrichtThe Netherlands
  7. 7.Shadyside Medical CenterPittsburghUSA

Personalised recommendations