Surgical Endoscopy

, Volume 30, Issue 9, pp 3816–3822 | Cite as

Preserving the pulmonary vagus nerve branches during thoracoscopic esophagectomy

  • Teus J. Weijs
  • Jelle P. Ruurda
  • Misha D. P. Luyer
  • Grard A. P. Nieuwenhuijzen
  • Sylvia van der Horst
  • Ronald L. A. W. Bleys
  • Richard van HillegersbergEmail author



Pulmonary vagus branches are transected as part of a transthoracic esophagectomy and lymphadenectomy for cancer. This may contribute to the development of postoperative pulmonary complications. Studies in which sparing of the pulmonary vagus nerve branches during thoracoscopic esophagectomy is investigated are lacking. Therefore, this study aimed to determine the feasibility and pitfalls of sparing pulmonary vagus nerve branches during thoracoscopic esophagectomy.


In 10 human cadavers, a thoracoscopic esophagectomy was performed while sparing the pulmonary vagus nerve branches. The number of intact nerve branches, their distribution over the lung lobes and the number and location of the remaining lymph nodes in the relevant esophageal lymph node stations (7, 10R and 10L) were recorded during microscopic dissection.


A median of 9 (range 5–16) right pulmonary vagus nerve branches were spared, of which 4 (0–12) coursed to the right middle/inferior lung lobe. On the left side, 10 (3–12) vagus nerve branches were spared, of which 4 (2–10) coursed to the inferior lobe. In 8 cases, lymph nodes were left behind, at stations 10R and 10L while sparing the vagus nerve branches. Lymph nodes at station 7 were always removed.


Sparing of pulmonary vagus nerve branches during thoracoscopic esophagectomy is feasible. Extra care should be given to the dissection of peribronchial lymph nodes, station 10R and 10L.


Thoracoscopic esophagectomy Pulmonary nerves Mediastinal lymphadenectomy Pulmonary complications 



We thank Miangela Lacle, pathologist at the University Medical Center Utrecht, for her advice regarding which tissue microsections contained lymphoid tissue and which did not. We thank Simon Plomp and Fiona van Zoomeren of the Department of Anatomy of the University Medical Center Utrecht for their assistance with all the logistics regarding the cadavers. Suzanne Verlinde-Schellekens and Jan-Willem de Groot are acknowledged for performing the histology.

Compliance with ethical standards


Teus J Weijs, MD; Jelle P Ruurda, MD, PhD; Misha DP Luyer, MD, PhD; Grard AP Nieuwenhuijzen, MD, PhD; Sylvia van der Horst, Ronald LAW Bleys, MD, PhD; and Richard van Hillegersberg, MD, PhD have no conflicts of interest to declare.


  1. 1.
    Weijs TJ, Ruurda JP, Nieuwenhuijzen GA, van Hillegersberg R, Luyer MD (2013) Strategies to reduce pulmonary complications after esophagectomy. World J Gastroenterol 19:6509–6514CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Biere SS, van Berge Henegouwen MI, Maas KW, Bonavina L, Rosman C, Garcia JR, Gisbertz SS, Klinkenbijl JH, Hollmann MW, de Lange ES, Bonjer HJ, van der Peet DL, Cuesta MA (2012) Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet 379:1887–1892CrossRefPubMedGoogle Scholar
  3. 3.
    Butler N, Collins S, Memon B, Memon MA (2011) Minimally invasive oesophagectomy: current status and future direction. Surg Endosc 25:2071–2083CrossRefPubMedGoogle Scholar
  4. 4.
    Blencowe NS, Strong S, McNair AG, Brookes ST, Crosby T, Griffin SM, Blazeby JM (2012) Reporting of short-term clinical outcomes after esophagectomy: a systematic review. Ann Surg 255:658–666CrossRefPubMedGoogle Scholar
  5. 5.
    Matsuda S, Takeuchi H, Kawakubo H, Fukuda K, Nakamura R, Takahashi T, Wada N, Saikawa Y, Kitagawa Y (2015) Correlation between intense postoperative inflammatory response and survival of esophageal cancer patients who underwent transthoracic esophagectomy. Ann Surg Oncol. doi: 10.1245/s10434-015-4557-5 Google Scholar
  6. 6.
    van der Sluis PC, Verhage RJ, van der Horst S, van der Wal WM, Ruurda JP, van Hillegersberg R (2014) A new clinical scoring system to define pneumonia following esophagectomy for cancer. Dig Surg 31:108–116CrossRefPubMedGoogle Scholar
  7. 7.
    Tracey KJ (2009) Reflex control of immunity. Nat Rev Immunol 9:418–428CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Belvisi MG (2002) Overview of the innervation of the lung. Curr Opin Pharmacol 2:211–215CrossRefPubMedGoogle Scholar
  9. 9.
    Mazzone SB, Canning BJ (2013) Autonomic neural control of the airways. Handb Clin Neurol. 117:215–228CrossRefPubMedGoogle Scholar
  10. 10.
    Weijs T, Ruurda J, Luyer M, Nieuwenhuijzen G, Van Hillegersberg R, Bleys R (2015) Topography and extent of pulmonary vagus nerve supply with respect to transthoracic oesophagectomy. J Anat 227:431–439CrossRefPubMedGoogle Scholar
  11. 11.
    Fujita H, Hawahara H, Yamana H, Shirohazu G, Yoshimura Y, Minami T, Negoto Y, Irie H, Shima I, Machi J, Kakegawa T (1988) Mediastinal lymphnode dissection procedure during esophageal cancer operation–carefully considered for preserving respiratory function. Jpn J Surg 18:31–34CrossRefPubMedGoogle Scholar
  12. 12.
    Kutup A, Nentwich MF, Bollschweiler E, Bogoevski D, Izbicki JR, Holscher AH (2014) What should be the gold standard for the surgical component in the treatment of locally advanced esophageal cancer: transthoracic versus transhiatal esophagectomy. Ann Surg 260:1016–1022CrossRefPubMedGoogle Scholar
  13. 13.
    Hulscher JB, van Sandick JW, de Boer AG, Wijnhoven BP, Tijssen JG, Fockens P, Stalmeier PF, ten Kate FJ, van Dekken H, Obertop H, Tilanus HW, van Lanschot JJ (2002) Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the esophagus. N Engl J Med 347:1662–1669CrossRefPubMedGoogle Scholar
  14. 14.
    Omloo JM, Lagarde SM, Hulscher JB, Reitsma JB, Fockens P, van Dekken H, Ten Kate FJ, Obertop H, Tilanus HW, van Lanschot JJ (2007) Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the mid/distal esophagus: five-year survival of a randomized clinical trial. Ann Surg 246:992–1000CrossRefPubMedGoogle Scholar
  15. 15.
    Boone J, Schipper ME, Moojen WA, Borel Rinkes IH, Cromheecke GJ, van Hillegersberg R (2009) Robot-assisted thoracoscopic oesophagectomy for cancer. Br J Surg 96:878–886CrossRefPubMedGoogle Scholar
  16. 16.
    van der Sluis PC, Ruurda JP, Verhage RJ, van der Horst S, Haverkamp L, Siersema PD, Borel Rinkes IH, Ten Kate FJ, van Hillegersberg R (2015) Oncologic long-term results of robot-assisted minimally invasive thoraco-laparoscopic esophagectomy with two-field lymphadenectomy for esophageal cancer. Ann Surg Oncol. doi: 10.1245/s10434-015-4544-x PubMedCentralGoogle Scholar
  17. 17.
    Rusch VW, Asamura H, Watanabe H, Giroux DJ, Rami-Porta R, Goldstraw P, Members of IASLC Staging Committee (2009) The IASLC lung cancer staging project: a proposal for a new international lymph node map in the forthcoming seventh edition of the TNM classification for lung cancer. J Thorac Oncol 4:568–577CrossRefPubMedGoogle Scholar
  18. 18.
    Compton CC, Byrd DR, Garcia-Aguilar J, Kurtzman SH, Olawaiye A, Washington MK (2013) AJCC cancer staging atlas, 2nd edn. Springer, New YorkGoogle Scholar
  19. 19.
    Markar S, Gronnier C, Duhamel A, Bigourdan JM, Badic B, du Rieu MC, Lefevre JH, Turner K, Luc G, Mariette C (2015) Pattern of postoperative mortality after esophageal cancer resection according to center volume: results from a large european multicenter study. Ann Surg Oncol. doi: 10.1245/s10434-014-4310-5 PubMedGoogle Scholar
  20. 20.
    Peyre CG, DeMeester SR, Rizzetto C, Bansal N, Tang AL, Ayazi S, Leers JM, Lipham JC, Hagen JA, DeMeester TR (2007) Vagal-sparing esophagectomy: the ideal operation for intramucosal adenocarcinoma and Barrett with high-grade dysplasia. Ann Surg 246:665–671CrossRefPubMedGoogle Scholar
  21. 21.
    DeMeester SR (2010) Vagal-sparing esophagectomy: is it a useful addition? Ann Thorac Surg 89:2156–2158CrossRefGoogle Scholar
  22. 22.
    Schroder W, Vallbohmer D, Bludau M, Banczyk A, Gutschow C, Holscher AH (2008) The resection of the azygos vein-necessary or redundant extension of transthoracic esophagectomy? J Gastrointest Surg 12:1163–1167CrossRefPubMedGoogle Scholar
  23. 23.
    Boone J, Schipper ME, Bleys RL, Borel Rinkes IH, van Hillegersberg R (2008) The effect of azygos vein preservation on mediastinal lymph node harvesting in thoracic esophagolymphadenectomy. Dis Esophagus 21:226–229CrossRefPubMedGoogle Scholar
  24. 24.
    Hou X, Fu JH, Wang X, Zhang LJ, Liu QW, Luo KJ, Lin P, Yang HX (2014) Prophylactic thoracic duct ligation has unfavorable impact on overall survival in patients with resectable oesophageal cancer. Eur J Surg Oncol 40:1756–1762CrossRefPubMedGoogle Scholar
  25. 25.
    Ding X, Zhang J, Li B, Wang Z, Huang W, Zhou T, Wei Y, Li H (2012) A meta-analysis of lymph node metastasis rate for patients with thoracic oesophageal cancer and its implication in delineation of clinical target volume for radiation therapy. Br J Radiol 85:e1110–e1119CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Dresner SM, Lamb PJ, Bennett MK, Hayes N, Griffin SM (2001) The pattern of metastatic lymph node dissemination from adenocarcinoma of the esophagogastric junction. Surgery 129:103–109CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Teus J. Weijs
    • 1
  • Jelle P. Ruurda
    • 1
  • Misha D. P. Luyer
    • 2
  • Grard A. P. Nieuwenhuijzen
    • 2
  • Sylvia van der Horst
    • 1
  • Ronald L. A. W. Bleys
    • 3
  • Richard van Hillegersberg
    • 1
    Email author
  1. 1.Department of Surgery OncologyUniversity Medical Center UtrechtUtrechtThe Netherlands
  2. 2.Department of SurgeryCatharina Hospital EindhovenEindhovenThe Netherlands
  3. 3.Department of AnatomyUniversity Medical Center UtrechtUtrechtThe Netherlands

Personalised recommendations