Discrepancy Between the Clinical and Final Pathological Findings of Lymph Node Metastasis in Superficial Esophageal Cancer



Recent advances in endoscopic examinations have resulted in the detection of a larger number of early esophageal cancers; however, there have been many cases with clinically negative but pathologically positive lymph node metastasis (LNM). In this study, we aimed to evaluate the discrepancy between the clinical and pathological diagnoses of LNM in patients with cT1a-MM/cT1b N0M0 esophageal cancer, and assess LNM size in these patients to clarify the presence of LNM that cannot be detected with current modalities.


This study included 50 patients who underwent surgery for cT1a-MM/cT1b N0M0 thoracic esophageal squamous cell carcinoma between January 2012 and November 2016 at our institution. The maximum size of involved LNs and metastatic nests were measured, and the distribution of LNM was investigated.


Of the 50 patients, 13 (26%) had LNM on pathological examination. Lymphatic invasion was significantly more frequent in the LNM-positive group than in the LNM-negative group (p = 0.005). The median sizes of 28 involved LNs and metastatic nests were 3 and 1.6 mm, respectively. Of these LNs, 20 (71%) were classified as micrometastases (≤ 2 mm). The involved nodes were distributed across three fields.


There was a discrepancy between the clinical and final pathological findings of LNM in patients with cT1a-MM/cT1b N0M0 esophageal cancer. The detection of involved nodes with current modalities in these patients was difficult because of the small size of LNM. Therefore, continued strong consideration for extended LN dissection is necessary in these patients to ensure appropriate diagnosis and treatment.

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  1. 1.

    Abnet CC, Arnold M, Wei WQ. Epidemiology of esophageal squamous cell carcinoma. Gastroenterology. 2018;154(2):360–73.

    Article  Google Scholar 

  2. 2.

    Minami H, Isomoto H, Inoue H, et al. Significance of background coloration in endoscopic detection of early esophageal squamous cell carcinoma. Digestion. 2014;89(1):6–11.

    CAS  Article  Google Scholar 

  3. 3.

    Ono S, Fujishiro M, Koike K. Endoscopic submucosal dissection for superficial esophageal neoplasms. World J Gastrointest Endosc. 2012;4(5):162–6.

    Article  Google Scholar 

  4. 4.

    Kuwano H, Nishimura Y, Oyama T, et al. Guidelines for diagnosis and treatment of carcinoma of the esophagus April 2012 edited by the Japan Esophageal Society. Esophagus. 2015;12:1–30.

    Article  Google Scholar 

  5. 5.

    Tanaka T, Matono S, Mori N, Shirouzu K, Fujita H. T1 Squamous cell carcinoma of the esophagus: long-term outcomes and prognostic factors after esophagectomy. Ann Surg Oncol. 2014;21(3):932–8.

    Article  Google Scholar 

  6. 6.

    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(2):365–71.

    Article  Google Scholar 

  7. 7.

    Wilson M, Rosato EL, Chojnacki KA, et al. Prognostic significance of lymph node metastases and ratio in esophageal cancer. J Surg Res. 2008;146(1):11–5.

    Article  Google Scholar 

  8. 8.

    Kunisaki C, Makino H, Kimura J, et al. Impact of lymph-node metastasis site in patients with thoracic esophageal cancer. J Surg Oncol. 2010;101(1):36–42.

    Article  Google Scholar 

  9. 9.

    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(9):747–53.

    CAS  Article  Google Scholar 

  10. 10.

    van Hagen P, Hulshof MC, van Lanschot JJ, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med. 2012;366:2074–84.

    Article  Google Scholar 

  11. 11.

    Ando N, Kato H, Igaki H, et al. A randomized trial comparing postoperative adjuvant chemotherapy with cisplatin and 5-fluorouracil versus preoperative chemotherapy for localized advanced squamous cell carcinoma of the thoracic esophagus (JCOG9907). Ann Surg Oncol. 2011;19(1):68–74.

    Article  Google Scholar 

  12. 12.

    van Vliet EP, Heijenbrok-Kal MH, Hunink MG, Kuipers EJ, Siersema PD. Staging investigations for oesophageal cancer: a meta-analysis. Br J Cancer. 2008;98(3):547–57.

    Article  Google Scholar 

  13. 13.

    Okada M, Murakami T, Kumano S, et al. Integrated FDG-PET/CT compared with intravenous contrast-enhanced CT for evaluation of metastatic regional lymph nodes in patients with resectable early stage esophageal cancer. Ann Nucl Med. 2009;23(1):73–80.

    Article  Google Scholar 

  14. 14.

    Betancourt Cuellar SL, Sabloff B, Carter BW, et al. Early clinical esophageal adenocarcinoma (cT1): utility of CT in regional nodal metastasis detection and can the clinical accuracy be improved? Eur J Radiol. 2017;88:56–60.

    Article  Google Scholar 

  15. 15.

    Brierley JD, Gospodarowicz MK, Wittekind C (eds). Classification of malignant tumours. 8th ed. Weinheim: Wiley; 2017.

    Google Scholar 

  16. 16.

    Weaver DL. Pathology evaluation of sentinel lymph nodes in breast cancer: protocol recommendations and rationale. Mod Pathol. 2010;23(Suppl 2):S26–32.

    Article  Google Scholar 

  17. 17.

    Foley KG, Christian A, Fielding P, Lewis WG, Roberts SA. Accuracy of contemporary oesophageal cancer lymph node staging with radiological-pathological correlation. Clin Radiol. 2017;72(8):693.e691–7.

    Article  Google Scholar 

  18. 18.

    Kato H, Kuwano H, Nakajima M, et al. Comparison between positron emission tomography and computed tomography in the use of the assessment of esophageal carcinoma. Cancer. 2002;94(4):921–8.

    Article  Google Scholar 

  19. 19.

    Higuchi I, Yasuda T, Yano M, et al. Lack of fludeoxyglucose F 18 uptake in posttreatment positron emission tomography as a significant predictor of survival after subsequent surgery in multimodality treatment for patients with locally advanced esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg. 2008;136(1):205–12, e201–3.

  20. 20.

    Yamada H, Hosokawa M, Itoh K, et al. Diagnostic value of 18F-FDG PET/CT for lymph node metastasis of esophageal squamous cell carcinoma. Surg Today. 2013;44(7):1258–65.

    Article  Google Scholar 

  21. 21.

    Eguchi T, Nakanishi Y, Shimoda T, et al. Histopathological criteria for additional treatment after endoscopic mucosal resection for esophageal cancer: analysis of 464 surgically resected cases. Mod Pathol. 2006;19(3):475–80.

    Article  Google Scholar 

  22. 22.

    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(2):250–4.

    Article  Google Scholar 

  23. 23.

    Akutsu Y, Uesato M, Shuto K, et al. The overall prevalence of metastasis in T1 esophageal squamous cell carcinoma. Ann Surg. 2013;257(6):1032–8.

    Article  Google Scholar 

  24. 24.

    Miyata H, Doki Y, Yasuda T, et al. Evaluation of clinical significance of 18f-fluorodeoxyglucose positron emission tomography in superficial squamous cell carcinomas of the thoracic esophagus. Dis Esophagus. 2008;21(2):144–50.

    CAS  Article  Google Scholar 

  25. 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(3):236–40.

    CAS  Article  Google Scholar 

  26. 26.

    Izbicki JR, Hosch SB, Pichlmeier U, et al. Prognostic value of immunohistochemically identifiable tumor cells in lymph nodes of patients with completely resected esophageal cancer. N Engl J Med. 1997;337(17):1188–94.

    CAS  Article  Google Scholar 

  27. 27.

    Glickman JN, Torres C, Wang HH, et al. The prognostic significance of lymph node micrometastasis in patients with esophageal carcinoma. Cancer. 1999;85(4):769–78.

    CAS  Article  Google Scholar 

  28. 28.

    Matsuda S, Takeuchi H, Kawakubo H, et al. Clinical outcome of transthoracic esophagectomy with thoracic duct resection: number of dissected lymph node and distribution of lymph node metastasis around the thoracic duct. Medicine (Baltimore). 2016;95(24):e3839.

    CAS  Article  Google Scholar 

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Correspondence to Hirofumi Kawakubo MD, PhD.

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Junya Aoyama, Hirofumi Kawakubo, Shuhei Mayanagi, Kazumasa Fukuda, Tomoyuki Irino, Rieko Nakamura, Norihito Wada, Tatsuya Suzuki, Kaori Kameyama, and Yuko Kitagawa report no conflict of interest in this work.

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Aoyama, J., Kawakubo, H., Mayanagi, S. et al. Discrepancy Between the Clinical and Final Pathological Findings of Lymph Node Metastasis in Superficial Esophageal Cancer. Ann Surg Oncol 26, 2874–2881 (2019). https://doi.org/10.1245/s10434-019-07498-2

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