Skip to main content

Advertisement

Log in

Salvage Surgery for Esophageal Cancer: How to Improve Outcomes?

  • Thoracic Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Locoregional recurrence rates after definitive chemoradiotherapy (dCRT) for locally advanced esophageal cancer (EC) are high. Salvage surgery (SALV) is considered the best treatment option in case of persistent or recurrent disease for operable patients, but SALV has been associated with increased morbidity and mortality. The aim of this study is to identify factors linked to outcomes after SALV to better select candidates and to optimize perioperative care.

Study Design

We retrospectively analyzed data from 308 consecutive SALV patients from a large multicenter European cohort. Univariate and multivariate analyses were performed to identify factors associated with in-hospital postoperative morbidity, anastomotic leakage (AL), and overall survival (OS).

Results

The in-hospital postoperative mortality and morbidity rates were 8.4 and 34.7%, respectively. Squamous cell histology (p = 0.040) and radiation dose ≥ 55 Gy (p = 0.047) were independently associated with major morbidity. The AL rate was 12.7%, and cervical anastomosis was independently associated with AL (p = 0.002). OS at 5 years was 34.0%. Radiation dose ≥ 55 Gy (p = 0.003), occurrence of postoperative complications (p = 0.006), ypTNM stage 3 (p = 0.019), and positive surgical margins (p < 0.001) were linked to poor prognosis.

Conclusions

SALV is a valuable option for patients with persistent or recurrent disease after dCRT and offers long-term survival. Factors such as radiation dose and anastomosis location identified here will help to optimize outcomes after SALV, which may be considered a standard treatment in the EC therapeutic armamentarium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Siegel R, DeSantis C, Virgo K, et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin. 2012;62:220–41.

    Article  PubMed  Google Scholar 

  2. Mariette C, Piessen G, Briez N, et al. Oesophagogastric junction adenocarcinoma: which therapeutic approach? Lancet Oncol. 2011;12:296–305.

    Article  PubMed  Google Scholar 

  3. Stahl M, Stuschke M, Lehmann N, et al. Chemoradiation with and without surgery in patients with locally advanced squamous cell carcinoma of the esophagus. J Clin Oncol. 2005;23:2310–17.

    Article  PubMed  Google Scholar 

  4. Bedenne L, Michel P, Bouche O, et al. Randomized phase III trial in locally advanced esophageal cancer: radiochemotherapy followed by surgery versus radiochemotherapy alone (FFCD 9102). J Clin Oncol. 2007;25:1160–8.

    Article  CAS  PubMed  Google Scholar 

  5. Stahl M, Mariette C, Haustermans K, et al. Oesophageal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2013;24 Suppl 6:vi52–56.

  6. Thésaurus National de Cancerologie Digestive. Société nationale française de gastroenterologie. Chapitre 1: Cancer de l’oesophage. http://www.tncd.org. Accessed 21 Aug 21 2015.

  7. Gardner-Thorpe J, Hardwick R, Dwerryhouse S. Salvage esophagectomy after local failure of definitive chemoradiotherapy. Br J Surg. 2007;94:1059–66.

    Article  CAS  PubMed  Google Scholar 

  8. Jamel S, Markar S. Salvage esophagectomy: safe therapeutic strategy? J Thorac Dis. 2017;9:S799–808.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Rice TW. Esophageal nightmare: cancer recurrence after definitive chemoradiation. Is salvage esophagectomy possible? Semin Thorac Cardiovasc Surg. 2013;25:83–6.

    Article  PubMed  Google Scholar 

  10. Piessen G, Messager M, Mirabel X, et al. Is there a role for surgery for patients with a complete clinical response after chemoradiation for esophageal cancer? An intention to-treat case-control study. Ann Surg. 2013;258:793–9.

    Article  PubMed  Google Scholar 

  11. Mariette C, Piessen G, Briez N, Triboulet JP. The number of metastatic lymph nodes and the ratio between metastatic and examined lymph nodes are independent prognostic factors in esophageal cancer regardless of neoadjuvant chemoradiation or lymphadenectomy extent. Ann Surg. 2008;247:365–71.

    Article  PubMed  Google Scholar 

  12. Briez N, Piessen G, Bonnetain F, et al. Open versus laparoscopically-assisted oesophagectomy for cancer: a multicenter randomized controlled phase III trial-the MIRO trial. BMC Cancer. 2011;11:310.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Edge SB, Byrd DR, Compton CC, eds. AJCC Cancer Staging Manual. 7th ed. New York: Springer; 2010:103–115.

  15. Akutsu Y, Kono T, Uesato M, et al. Is outcome of salvage surgery for T4 thoracic esophageal squamous cell carcinoma really poor? World J Surg. 2014;38:2891–7.

    Article  PubMed  Google Scholar 

  16. Borghesi S, Hawkins M, Tait D. Esophagectomy after definitive chemoradiation in patients with locally advanced esophageal cancer. Clin Oncol. 2008;20:221–6.

    Article  CAS  Google Scholar 

  17. Yoo C, Park JH, Yoon DH, et al. Salvage esophagectomy for locoregional failure after chemoradiotherapy in patients with advanced esophageal cancer. Ann Thorac Surg. 2012;94:1862–8.

    Article  PubMed  Google Scholar 

  18. Chao YK, Chan SC, Chang HK, et al. Salvage surgery after failed chemoradiotherapy in squamous cell carcinoma of the esophagus. Eur J Surg Oncol. 2009;35:289–94.

    Article  CAS  PubMed  Google Scholar 

  19. Chen Y, Lu Y, Wang Y, et al. Comparison of salvage chemoradiation versus salvage surgery for recurrent esophageal squamous cell carcinoma after definitive radiochemotherapy or radiotherapy alone. Dis Esophagus. 2014;27:134–40.

    Article  CAS  PubMed  Google Scholar 

  20. D’Journo XB, Michelet P, Dahan L, et al. Indications and outcome of salvage surgery for esophageal cancer. Eur J Cardiothorac Surg. 2008;33:1117–23.

    Article  PubMed  Google Scholar 

  21. Farinella E, Safar A, Nasser H, et al. Salvage esophagectomy after failure of definitive radiochemotherapy for esophageal cancer. J Surg Oncol. 2016; 114:833–7.

    Article  PubMed  Google Scholar 

  22. Marks J, Hofstetter W, Correa A, et al. Salvage esophagectomy after failed definitive chemoradiation for esophageal adenocarcinoma. Ann Thorac Surg. 2012;94:1126–33.

    Article  PubMed  Google Scholar 

  23. Miyata R, Yamasaki M, Takiguchi S, et al. Salvage esophagectomy after definitive chemoradiotherapy for thoracic esophageal cancer. J Surg Oncol. 2009;100:442–6.

    Article  CAS  PubMed  Google Scholar 

  24. Morita M, Kumashiro R, Hisamatsu Y, et al. Clinical significance of salvage esophagectomy for remnant or recurrent cancer following definitive chemoradiotherapy. J Gastroenterol. 2011;46:1284–91.

    Article  CAS  PubMed  Google Scholar 

  25. Nakamura T, Hayashi K, Ota M, et al. Salvage esophagectomy after definitive chemotherapy and radiotherapy for advanced esophageal cancer. Am J Surg. 2004;188:261–6.

    Article  PubMed  Google Scholar 

  26. Oki E, Morita M, Kakeji Y, et al. Salvage esophagectomy after definitive chemoradiotherapy for esophageal cancer. Dis Esophagus. 2007;20:301–4.

    Article  CAS  PubMed  Google Scholar 

  27. Piessen G, Briez N, Triboulet JP, Mariette C. Patients with locally advanced esophageal carcinoma nonresponder to radiochemotherapy: who will benefit from surgery? Ann Surg Oncol. 2007;14:2036–44.

    Article  PubMed  Google Scholar 

  28. Pinto CE, de Souza Fernandes D, Moura Sà E, Mello ELR. Salvage esophagectomy after exclusive chemoradiotherapy: results at the Brazilian Cancer Institute. Dis Esophagus. 2009;22:682–6.

    Article  CAS  PubMed  Google Scholar 

  29. Schieman C, Wigle DA, Deschamps C, et al. Salvage resections for recurrent or persistent cancer of the proximal esophagus after chemoradiotherapy. Ann Thorac Surg. 2013;95:459–63.

    Article  PubMed  Google Scholar 

  30. Smithers BM, Cullinan M, Thomas JM, et al. Outcomes from salvage esophagectomy post definitive chemoradiotherapy compared with resection following preoperative neoadjuvant chemoradiotherapy. Dis Esophagus. 2007;20:471–7.

    Article  CAS  PubMed  Google Scholar 

  31. Sohda M, Kumakura Y, Saito H, et al. Clinical significance of salvage esophagectomy for patients with esophageal cancer and factors of influencing long-term survival. Anticancer Res. 2017;37:5045–51.

    PubMed  Google Scholar 

  32. Swisher SG, Wynn P, Putnam JB, et al. Salvage esophagectomy for recurrent tumors after definitive chemotherapy and radiotherapy. J Thorac Cardiovasc Surg. 2002;123:175–83.

    Article  PubMed  Google Scholar 

  33. Tachimori Y, Kanamori N, Uemura N, et al. Salvage esophagectomy after high-dose chemoradiotherapy for esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg. 2009;137:49–54.

    Article  PubMed  Google Scholar 

  34. Takeuchi H, Saikawa Y, Oyama T, et al. Factors influencing the long-term survival in patients with esophageal cancer who underwent esophagectomy after chemoradiotherapy. World J Surg. 2010;34:277–84.

    Article  PubMed  Google Scholar 

  35. Tomimaru Y, Yano M, Takachi K, et al. Factors affecting the prognosis of patients with esophageal cancer undergoing salvage surgery after definitive chemoradiotherapy. J Surg Oncol. 2006;93:422–8.

    Article  PubMed  Google Scholar 

  36. Wang S, Tachimori Y, Hokamura N, et al. Prognosis analysis of salvage esophagectomy following definitive chemoradiotherapy for esophageal squamous cell carcinoma: the importance of lymphadenectomy. J Thorac Cardiovasc Surg. 2014;147:1805–11.

    Article  PubMed  Google Scholar 

  37. Watanabe M, Mine S, Nishida K et al. Salavage esophagectomy after definitive chemoradiotherapy for patients with esophageal squamous cell carcinoma: who really benefits from this high risk surgery? Ann Surg Oncol. 2015;22:4438–44.

    Article  PubMed  Google Scholar 

  38. Ghaly G, Kamel M, Nasar A, et al. Locally advanced esophageal cancer: what becomes of 5-year survivors? J Thorac Cardiovasc Surg. 2016;151:726–32.

    Article  PubMed  Google Scholar 

  39. Gronnier C, Tréchot B, Duhamel A, et al. Impact of neoadjuvant chemoradiotherapy on postoperative outcomes after esophageal cancer resection: results of a European multicenter study. Ann Surg. 2014;260:764–70.

    Article  PubMed  Google Scholar 

  40. Minsky BD, Pajak TF, Ginsberg RJ, et al. INT 0123 (Radiation Therapy Oncology Group 94-05) phase III trial of combined-modality therapy for esophageal cancer: high-dose versus standard-dose radiation therapy. J Clin Oncol. 2002;20:1167–74.

    Article  CAS  PubMed  Google Scholar 

  41. NCCN esophageal cancer guidelines. http://www.nccn.org/professionals/physician_gls/pdf/esophageal.pdf. Accessed 20 Aug 2015.

  42. Girard E, Messager M, Sauvanet A, et al. Anastomotic leakage after gastrointestinal surgery: diagnosis and management. J Visc Surg. 2014;151:441–50.

    Article  CAS  PubMed  Google Scholar 

  43. Markar S, Gronnier C, Duhamel A, et al. Salvage surgery after chemotherapy in the management of esophageal cancer: is it a viable therapeutic option? J Clin Oncol. 2015; 33:3866–73.

    Article  CAS  PubMed  Google Scholar 

  44. Vincent J, Mariette C, Pezet D, et al. Early surgery for failure after chemoradiation in operable thoracic oesophageal cancer. Analysis of the non-randomised patients in FFCD 9102 phase III trial: Chemoradiation followed by surgery versus chemoradiation alone. Eur J Cancer. 2015;51:1683–93.

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

Collaborators for the FREGAT (French Eso-Gastric Tumors working group) – FRENCH (Fédération de Recherche en Chirurgie) – AFC (Association Française de Chirurgie) Working Groups

Abdennahceur Dhahri, MD, PhD, Delphine Lignier, MD, Cyril Cossé, MD, Jean-Marc Regimbeau, MD, PhD, Department of Digestive Surgery, Amiens, France; Guillaume Luc, MD, Department of Digestive Surgery, Bordeaux, France; Magalie Cabau, MD, Jacques Jougon MD, PhD, Department of Thoracic Surgery, Bordeaux, France; Bogdan Badic, MD, Patrick Lozach, MD, Jean Pierre Bail, MD, Department of Digestive Surgery, Brest, France; Serge Cappeliez, MD, PhD, Issam El Nakadi, MD, PhD, Department of Digestive Surgery, Brussel ULB, Erasme Bordet University, Brussel, Belgium; Gil Lebreton, MD, Arnaud Alves, MD, PhD, Department of Digestive Surgery, Caen, France; Renaud Flamein, MD, Denis Pezet, MD, PhD, Department of Digestive Surgery, Clermont-Ferrand, France; Federica Pipitone, MD, Bogdan Stan-Iuga, MD, Nicolas Contival, MD, Eric Pappalardo, MD, Xaviera Coueffe, MD, Simon Msika, MD, PhD, Department of Digestive Surgery, Louis Mourier University Hospital, Colombes, France; Styliani Mantziari, MD, Nicolas Demartines, MD, Department of Digestive Surgery, Lausanne University Hospital, Lausanne, Switzerland; Flora Hec, MD, Marguerite Vanderbeken, MD, Nicolas Briez, MD, Department of Digestive Surgery, Lille, France; Fabien Fredon, MD, Alain Gainant, MD, Muriel Mathonnet, MD, PhD, Department of Digestive Surgery, Limoges, France; Jean Marc Bigourdan, MD, Salim Mezoughi, MD, Christian Ducerf, MD, Jacques Baulieux, MD, Jean-Yves Mabrut, MD, PhD, Department of Digestive Surgery, Croix Rousse University Hospital, Lyon, France; Oussama Baraket, MD, Gilles Poncet, MD, Mustapha Adam, MD, PhD, Department of Digestive Surgery, Edouard Herriot University Hospital, Lyon, France; Delphine Vaudoyer, MD, Peggy Jourdan Enfer, MD, Laurent Villeneuve, MD, Olivier Glehen, MD, PhD, Department of Digestive Surgery, Lyon Sud University Hospital, Lyon, France; Thibault Coste, MD, Jean-Michel Fabre, MD, Department of Digestive Surgery, Montpellier, France; Frédéric Marchal, MD, Department of Digestive Surgery, Institut de cancérologie de Lorraine, Nancy, France; Romain Frisoni, MD, Ahmet Ayav, MD, PhD, Laurent Brunaud, MD, PhD, Laurent Bresler, MD, Department of Digestive Surgery, Nancy, France; Olivier Aze, MD, Nicolas Venissac, MD, Daniel Pop, MD, Jérôme Mouroux, MD, Department of Thoracic Surgery, Nice, France; Ion Donici, MD, Michel Prudhomme, MD, PhD, Department of Digestive Surgery, Nîmes, France; Emanuele Felli, MD, Stéphanie Lisunfui, MD, Marie Seman, MD, Gaelle Godiris Petit, MD, Mehdi Karoui, MD, PhD, Christophe Tresallet, MD, PhD, Fabrice Ménégaux, MD, PhD, Jean-Christophe Vaillant, MD, Laurent Hannoun, MD, Department of Digestive Surgery, Pitié-Salpétrière University Hospital, Paris, France; Brice Malgras, MD, Denis Lantuas, MD, Karine Pautrat, MD, Marc Pocard, MD, PhD, Patrice Valleur, MD, Department of Digestive Surgery, Lariboisière University Hospital, Paris, France; Jérémie H Lefevre, MD, PhD, Najim Chafai, MD, Pierre Balladur, MD, Magalie Lefrançois, MD, Yann Parc, MD, PhD, François Paye, MD, PhD Emmanuel Tiret, MD Department of Digestive Surgery, Saint-Antoine University Hospital, Paris, France; Marius Nedelcu, MD, Letizia Laface, MD, Thierry Perniceni, MD, Brice Gayet, MD, Department of Digestive Surgery, Institut Mutualiste Montsouris, Paris, France; Kathleen Turner, MD, Department of Digestive Surgery, Rennes, France; Alexandre Filipello, MD, Jack Porcheron, MD, Olivier Tiffet, MD, PhD, Department of Digestive Surgery, Saint-Etienne, France; Noémie Kamlet, MD, Rodrigue Chemaly, MD, Amandine Klipfel, MD, Patrick Pessaux, MD, PhD, Cecile Brigand, MD, PhD, Serge Rohr MD, Department of Digestive Surgery, Strasbourg, France; Nicolas Carrère, MD, PhD, Department of Digestive Surgery, Toulouse, France; Chiara Da Re, MD, Frédéric Dumont, MD, Diane Goéré, MD, PhD, Dominique Elias, MD, Department of Digestive Surgery Institut Gustave-Roussy, Villejuif, France; Claude Bertrand, MD, Mont-Godinne University Hospital, Yvoir, Belgium.

Author Contribution

Study conception and design: Williams TESSIER and Christophe MARIETTE; Acquisition of data: All authors; Analysis and interpretation of data: Charlotte COHEN, Williams TESSIER, Caroline GRONNIER, Guillaume PIESSEN, and Christophe MARIETTE; Drafting of manuscript: Charlotte COHEN, Williams TESSIER, and Christophe MARIETTE; Critical revision: All authors.

Disclosure

None.

Author information

Authors and Affiliations

Authors

Consortia

Corresponding author

Correspondence to Charlotte Cohen MD.

Additional information

Collaborators of the FREGAT (French Eso-Gastric Tumors working group) – FRENCH (Fédération de Recherche en Chirurgie) – AFC (Association Française de Chirurgie) Working Groups are listed in “Acknowledgment”.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cohen, C., Tessier, W., Gronnier, C. et al. Salvage Surgery for Esophageal Cancer: How to Improve Outcomes?. Ann Surg Oncol 25, 1277–1286 (2018). https://doi.org/10.1245/s10434-018-6365-1

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-018-6365-1

Keywords

Navigation