Clin Endosc.  2014 Nov;47(6):523-529. 10.5946/ce.2014.47.6.523.

Lymph Node Metastases in Esophageal Carcinoma: An Endoscopist's View

• Cho JW
• Choi SC
• Jang JY
• Shin SK
• Choi KD
• Lee JH
• Kim SG
• Sung JK
• Jeon SW
• Choi IJ
• Kim GH
• Jee SR
• Lee WS
• Jung HY
• Korean ESD Study Group

• KMID: 2134490
• DOI: http://doi.org/10.5946/ce.2014.47.6.523

Abstract

One of the most important prognostic factors in esophageal carcinoma is lymph node metastasis, and in particular, the number of affected lymph nodes, which influences long-term outcomes. The esophageal lymphatic system is connected longitudinally and transversally; thus, the pattern of lymph node metastases is very complex. Early esophageal cancer frequently exhibits skipped metastasis, and minimal surgery using sentinel node navigation cannot be performed. In Korea, most esophageal cancer cases are squamous cell carcinoma (SCC), although the incidence of adenocarcinoma has started to increase recently. Most previous reports have failed to differentiate between SCC and adenocarcinoma, despite the fact that the Union for International Cancer Control (7th edition) and American Joint Committee on Cancer staging systems both consider these separately because they differ in cause, biology, lymph node metastasis, and outcome. Endoscopic tumor resection is an effective and safe treatment for lesions with no associated lymph node metastasis. Esophageal mucosal cancer confined to the lamina propria is an absolute indication for endoscopic resection, and a lesion that has invaded the muscularis mucosae can be cured by local resection if invasion to the lymphatic system has not occurred.

Keyword

Esophageal neoplasms; Lymph node metastasis; Endoscopic resection

MeSH Terms

Adenocarcinoma
Biology
Carcinoma, Squamous Cell
Esophageal Neoplasms
Incidence
Joints
Korea
Lymph Nodes*
Lymphatic System
Mucous Membrane
Neoplasm Metastasis*
Neoplasm Staging

Reference

1. Yang JI. A study of esophageal cancer detected by screening upper endoscopy for a routine health check-up. Korean J Helicobacter Up Gastrointest Res. 2013; 13:99–103.

2. Isono K, Sato H, Nakayama K. Results of a nationwide study on the three-field lymph node dissection of esophageal cancer. Oncology. 1991; 48:411–420. PMID: 1745490.

3. Cense HA, van Eijck CH, Tilanus HW. New insights in the lymphatic spread of oesophageal cancer and its implications for the extent of surgical resection. Best Pract Res Clin Gastroenterol. 2006; 20:893–906. PMID: 16997168.

4. Sgourakis G, Gockel I, Lyros O, Hansen T, Mildenberger P, Lang H. Detection of lymph node metastases in esophageal cancer. Expert Rev Anticancer Ther. 2011; 11:601–612. PMID: 21504265.

5. Xu QR, Zhuge XP, Zhang HL, Ping YM, Chen LQ. The N-classification for esophageal cancer staging: should it be based on number, distance, or extent of the lymph node metastasis? World J Surg. 2011; 35:1303–1310. PMID: 21452071.

6. Hosch SB, Stoecklein NH, Pichlmeier U, et al. Esophageal cancer: the mode of lymphatic tumor cell spread and its prognostic significance. J Clin Oncol. 2001; 19:1970–1975. PMID: 11283129.

7. 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. PMID: 14601903.

8. Tachibana M, Kinugasa S, Yoshimura H, et al. Clinical outcomes of extended esophagectomy with three-field lymph node dissection for esophageal squamous cell carcinoma. Am J Surg. 2005; 189:98–109. PMID: 15701501.

9. Rice TW, Rusch VW, Ishwaran H, Blackstone EH. Worldwide Esophageal Cancer Collaboration. Cancer of the esophagus and esophagogastric junction: data-driven staging for the seventh edition of the American Joint Committee on Cancer/International Union Against Cancer Cancer Staging Manuals. Cancer. 2010; 116:3763–3773. PMID: 20564099.

10. Greene FL. American Joint Committee on Cancer. American Cancer Society. AJCC Cancer Staging Manual. 6th ed. New York: Springer-Verlag;2002.

11. Edge SB. American Joint Committee on Cancer. AJCC Cancer Staging Manual. 7th ed. New York: Springer;2010. p. 103.

12. Lieberman MD, Shriver CD, Bleckner S, Burt M. Carcinoma of the esophagus. Prognostic significance of histologic type. J Thorac Cardiovasc Surg. 1995; 109:130–138. PMID: 7815789.

13. Akutsu Y, Matsubara H. The significance of lymph node status as a prognostic factor for esophageal cancer. Surg Today. 2011; 41:1190–1195. PMID: 21874413.

14. O'Riordan JM, Rowley S, Murphy JO, Ravi N, Byrne PJ, Reynolds JV. Impact of solitary involved lymph node on outcome in localized cancer of the esophagus and esophagogastric junction. J Gastrointest Surg. 2007; 11:493–499. PMID: 17436135.

15. Zhang HL, Chen LQ, Liu RL, et al. The number of lymph node metastases influences survival and International Union Against Cancer tumor-node-metastasis classification for esophageal squamous cell carcinoma. Dis Esophagus. 2010; 23:53–58. PMID: 19392846.

16. Kayani B, Zacharakis E, Ahmed K, Hanna GB. Lymph node metastases and prognosis in oesophageal carcinoma: a systematic review. Eur J Surg Oncol. 2011; 37:747–753. PMID: 21839394.

17. 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; 247:365–371. PMID: 18216546.

18. 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; 253:271–278. PMID: 21119508.

19. Hu Y, Hu C, Zhang H, Ping Y, Chen LQ. How does the number of resected lymph nodes influence TNM staging and prognosis for esophageal carcinoma? Ann Surg Oncol. 2010; 17:784–790. PMID: 19953333.

20. Yang HX, Xu Y, Fu JH, Wang JY, Lin P, Rong TH. An evaluation of the number of lymph nodes examined and survival for node-negative esophageal carcinoma: data from China. Ann Surg Oncol. 2010; 17:1901–1911. PMID: 20146101.

21. Greenstein AJ, Litle VR, Swanson SJ, Divino CM, Packer S, Wisnivesky JP. Effect of the number of lymph nodes sampled on postoperative survival of lymph node-negative esophageal cancer. Cancer. 2008; 112:1239–1246. PMID: 18224663.

22. Bollschweiler E, Baldus SE, Schr.der W, et al. High rate of lymph-node metastasis in submucosal esophageal squamous-cell carcinomas and adenocarcinomas. Endoscopy. 2006; 38:149–156. PMID: 16479422.

23. Buskens CJ, Ten Kate FJ, Obertop H, Izbicki JR, van Lanschot JJ. Analysis of micrometastatic disease in histologically negative lymph nodes of patients with adenocarcinoma of the distal esophagus or gastric cardia. Dis Esophagus. 2008; 21:488–495. PMID: 18840133.

24. Sun ZG, Wang Z. Clinical study on lymph node metastatic recurrence in patients with N0 esophageal squamous cell cancer. Dis Esophagus. 2011; 24:182–188. PMID: 21073618.

25. McGuill MJ, Byrne P, Ravi N, Reynolds J. The prognostic impact of occult lymph node metastasis in cancer of the esophagus or esophago-gastric junction: systematic review and meta-analysis. Dis Esophagus. 2008; 21:236–240. PMID: 18430105.

26. Tachibana M, Kinugasa S, Hirahara N, Yoshimura H. Lymph node classification of esophageal squamous cell carcinoma and adenocarcinoma. Eur J Cardiothorac Surg. 2008; 34:427–431. PMID: 18502142.

27. Siewert JR, Stein HJ, Feith M, Bruecher BL, Bartels H, Fink U. 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. 2001; 234:360–367. PMID: 11524589.

28. 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; 242:566–573. PMID: 16192817.

29. Siewert JR, Ott K. Are squamous and adenocarcinomas of the esophagus the same disease? Semin Radiat Oncol. 2007; 17:38–44. PMID: 17185196.

30. Shimada H, Nabeya Y, Matsubara H, et al. Prediction of lymph node status in patients with superficial esophageal carcinoma: analysis of 160 surgically resected cancers. Am J Surg. 2006; 191:250–254. PMID: 16442955.

31. Stiles BM, Mirza F, Coppolino A, et al. Clinical T2-T3N0M0 esophageal cancer: the risk of node positive disease. Ann Thorac Surg. 2011; 92:491–496. PMID: 21704291.

32. 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. PMID: 9527214.

33. Araki K, Ohno S, Egashira A, Saeki H, Kawaguchi H, Sugimachi K. Pathologic features of superficial esophageal squamous cell carcinoma with lymph node and distal metastasis. Cancer. 2002; 94:570–575. PMID: 11900242.

34. 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; 446:497–504. PMID: 15838647.

35. Moriya H, Ohbu M, Kobayashi N, et al. Lymphatic tumor emboli detected by D2-40 immunostaining can more accurately predict lymph-node metastasis. World J Surg. 2011; 35:2031–2037. PMID: 21667194.

36. Sgourakis G, Gockel I, Lyros O, et al. The use of neural networks in identifying risk factors for lymph node metastasis and recommending management of t1b esophageal cancer. Am Surg. 2012; 78:195–206. PMID: 22369829.

37. Tanaka T, Ishiguro H, Kuwabara Y, et al. Vascular endothelial growth factor C (VEGF-C) in esophageal cancer correlates with lymph node metastasis and poor patient prognosis. J Exp Clin Cancer Res. 2010; 29:83. PMID: 20584281.

38. Ono S, Fujishiro M, Koike K. Endoscopic submucosal dissection for superficial esophageal neoplasms. World J Gastrointest Endosc. 2012; 4:162–166. PMID: 22624067.

39. Sgourakis G, Gockel I, Lang H. Endoscopic and surgical resection of T1a/T1b esophageal neoplasms: a systematic review. World J Gastroenterol. 2013; 19:1424–1437. PMID: 23539431.