Langenbeck's Archives of Surgery

, Volume 403, Issue 8, pp 977–984 | Cite as

Supraclavicular and celiac metastases in squamous cell carcinoma of the middle thoracic esophagus

  • Akihiko Okamura
  • Masayuki WatanabeEmail author
  • Ryotaro Kozuki
  • Tasuku Toihata
  • Masami Yuda
  • Yu Imamura
  • Shinji Mine



Squamous cell carcinoma of the middle thoracic esophagus (SCC-ME) often metastasizes to the neck, mediastinum, and abdomen. This study aims to assess the prognostic impact of supraclavicular (SC) and celiac (CE) lymph node (LN) metastases in patients with SCC-ME.


We examined 210 patients who underwent curative esophagectomy with three-field LN dissection for SCC-ME. The clinicopathological features and survival outcomes of patients with and without SC and/or CE metastases were compared to assess the prognostic significance of SC and/or CE metastases.


We observed metastases to SC and CE in 25 (11.9%) and 20 (9.5%) patients, respectively. Seven patients (3.3%) had both SC and CE metastases. Although the survival of patients with SC and/or CE metastases was worse compared with those without, that of patients with SC metastases but without CE metastases was comparable with that of patients with CE metastases but without SC metastases; the 5 year overall survival rates were 35.6% and 46.2%, respectively. However, survival of patients with both SC and CE metastases was the worst among all groups, and all patients with both SC and CE metastases experienced disease recurrence.


The prognosis of patients with both SC and CE metastases was extremely poor. In contrast, patients with metastasis to either one of these sites could be candidates for surgery as the main modality in a multidisciplinary strategy.


Esophageal squamous cell carcinoma Lymph node metastasis Supraclavicular metastasis Celiac metastasis Prognosis 


Authors’ contributions

Study conception and design: all authors. Acquisition of data: all authors. Analysis and interpretation of data: Okamura, Watanabe, and Mine. Drafting of manuscript: Okamura, Watanabe, and Mine. Critical revision of manuscript: all authors.

Compliance with ethical standards

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study. This article does not contain any studies with animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

423_2018_1722_Fig3_ESM.png (196 kb)
Supplementary Figure 1

(PNG 196 kb)

423_2018_1722_MOESM1_ESM.tif (2.8 mb)
High Resolution Image (TIF 2829 kb)
423_2018_1722_Fig4_ESM.png (205 kb)
Supplementary Figure 2

(PNG 205 kb)

423_2018_1722_MOESM2_ESM.tif (2.8 mb)
High Resolution Image (TIF 2911 kb)
423_2018_1722_Fig5_ESM.png (207 kb)
Supplementary Figure 3

(PNG 207 kb)

423_2018_1722_MOESM3_ESM.tif (2.9 mb)
High Resolution Image (TIF 3008 kb)
423_2018_1722_MOESM4_ESM.docx (41 kb)
ESM 1 (DOCX 40 kb)


  1. 1.
    Kuwano H, Nishimura Y, Oyama T, Kato H, Kitagawa Y, Kusano M, Shimada H, Takiuchi H, Toh Y, Doki Y, Naomoto Y, Matsubara H, Miyazaki T, Muto M, Yanagisawa A (2015) Guidelines for diagnosis and treatment of carcinoma of the esophagus april 2012 edited by the Japan esophageal society. Esophagus 12:1–30CrossRefGoogle Scholar
  2. 2.
    Brierley JD, Gospodarowicz MK, Wittekind C (2017) TNM classification of malignant tumors. Wiley, EnglandGoogle Scholar
  3. 3.
    Amin MB, Edge SB, Greene FL (2017) AJCC Cancer staging manual. Springer, New YorkCrossRefGoogle Scholar
  4. 4.
    Frizzell B, Sinha D, Williams T, Reed CE, Sherman CA, Turrisi A (2003) Influence of celiac axis lymph nodes in the definitive treatment of esophageal cancer. Am J Clin Oncol 26:215–220Google Scholar
  5. 5.
    Seto Y, Fukuda T, Yamada K, Matsubara T, Hiki N, Fukunaga T, Oyama S, Yamaguchi T, Nakajima T, Kato Y (2008) Celiac lymph nodes: distant or regional for thoracic esophageal carcinoma? Dis Esophagus 21:704–707CrossRefGoogle Scholar
  6. 6.
    Chen G, Wang Z, Liu XY, Zhang MY, Liu FY (2009) Abdominal lymph node metastasis in patients with mid thoracic esophageal squamous cell carcinoma. World J Surg 33:278–283CrossRefGoogle Scholar
  7. 7.
    Shim YM, Park JS, Lee M, Kim D, Kim K (2013) Can common hepatic artery lymph node dissection be safely omitted in surgery for clinical T1N0 thoracic esophageal squamous cell carcinoma? Dis Esophagus 26:272–275CrossRefGoogle Scholar
  8. 8.
    Ma X, Li B, Yang S et al (2014) Extent of lymph node dissection: common hepatic artery lymph node dissection can be omitted for esophageal squamous cell carcinoma. J Thorac Dis 6:S325–S332Google Scholar
  9. 9.
    Tachimori Y, Ozawa S, Numasaki H, Matsubara H, Shinoda M, Toh Y, Udagawa H, Registration Committee for Esophageal Cancer of the Japan Esophageal Society (2014) Supraclavicular node metastasis from thoracic esophageal carcinoma: a surgical series from a Japanese multi-institutional nationwide registry of esophageal cancer. J Thorac Cardiovasc Surg 148:1224–1229CrossRefGoogle Scholar
  10. 10.
    Yamasaki M, Miyata H, Miyazaki Y, Takahashi T, Kurokawa Y, Nakajima K, Takiguchi S, Mori M, Doki Y (2014) Evaluation of the nodal status in the 7th edition of the UICC-TNM classification for esophageal squamous cell carcinoma: proposed modifications for improved survival stratification: impact of lymph node metastases on overall survival after esophagectomy. Ann Surg Oncol 21:2850–2856CrossRefGoogle Scholar
  11. 11.
    Miyata H, Yamasaki M, Miyazaki Y, Takahashi T, Kurokawa Y, Nakajima K, Takiguchi S, Mori M, Doki Y (2015) Clinical importance of supraclavicular lymph node metastasis after neoadjuvant chemotherapy for esophageal squamous cell carcinoma. Ann Surg 262:280–285CrossRefGoogle Scholar
  12. 12.
    Anderegg MC, Lagarde SM, Jagadesham VP et al (2016) Prognostic significance of the location of lymph node metastases in patients with adenocarcinoma of the distal esophagus or gastroesophageal junction. Ann Surg 264:847–853CrossRefGoogle Scholar
  13. 13.
    Cho WK, Oh D, Ahn YC, Shim YM, Zo JI, Sun JM, Ahn MJ, Park K (2017) Supraclavicular and/or celiac lymph node metastases from thoracic esophageal squamous cell carcinoma did not compromise survival following neoadjuvant chemoradiotherapy and surgery. Oncotarget 8:3542–3552Google Scholar
  14. 14.
    Honma Y, Hokamura N, Nagashima K, Sudo K, Shoji H, Iwasa S, Takashima A, Kato K, Hamaguchi T, Boku N, Umezawa R, Ito Y, Itami J, Koyanagi K, Igaki H, Tachimori Y (2017) Clinical outcomes of resectable esophageal cancer with supraclavicular lymph node metastases treated with curative intent. Anticancer Res 37:3741–3749Google Scholar
  15. 15.
    Rutegard M, Lagergren P, Johar A et al (2017) The prognostic role of coeliac node metastasis after resection for distal oesophageal cancer. Sci Rep 7:43744CrossRefGoogle Scholar
  16. 16.
    Sasako M, McCulloch P, Kinoshita T, Maruyama K (1995) New method to evaluate the therapeutic value of lymph node dissection for gastric cancer. Br J Surg 82:346–351CrossRefGoogle Scholar
  17. 17.
    Udagawa H, Ueno M, Shinohara H, Haruta S, Kaida S, Nakagawa M, Tsurumaru M (2012) The importance of grouping of lymph node stations and rationale of three-field lymphoadenectomy for thoracic esophageal cancer. J Surg Oncol 106:742–747CrossRefGoogle Scholar
  18. 18.
    Tachimori Y, Ozawa S, Numasaki H et al (2016) Efficacy of lymph node dissection for each station based on esophageal tumor location. Esophagus 13:138–145CrossRefGoogle Scholar
  19. 19.
    Peters CJ, Hardwick RH, Vowler SL, Fitzgerald RC, on behalf of the Oesophageal Cancer Clinical and Molecular Stratification Study Group (2009) Generation and validation of a revised classification for oesophageal and junctional adenocarcinoma. Br J Surg 96:724–733CrossRefGoogle Scholar
  20. 20.
    Fujita H (2015) History of lymphadenectomy for esophageal cancer and the future prospects for esophageal cancer surgery. Surg Today 45:140–149CrossRefGoogle Scholar
  21. 21.
    Ando N, Iizuka T, Ide H, Ishida K, Shinoda M, Nishimaki T, Takiyama W, Watanabe H, Isono K, Aoyama N, Makuuchi H, Tanaka O, Yamana H, Ikeuchi S, Kabuto T, Nagai K, Shimada Y, Kinjo Y, Fukuda H, Japan Clinical Oncology Group (2003) Surgery plus chemotherapy compared with surgery alone for localized squamous cell carcinoma of the thoracic esophagus: a Japan clinical oncology group study–JCOG9204. J Clin Oncol 21:4592–4596CrossRefGoogle Scholar
  22. 22.
    Ando N, Kato H, Igaki H, Shinoda M, Ozawa S, Shimizu H, Nakamura T, Yabusaki H, Aoyama N, Kurita A, Ikeda K, Kanda T, Tsujinaka T, Nakamura K, Fukuda H (2012) 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 19:68–74CrossRefGoogle Scholar
  23. 23.
    Foley KG, Christian A, Fielding P, Lewis WG, Roberts SA (2017) Accuracy of contemporary oesophageal cancer lymph node staging with radiological-pathological correlation. Clin Radiol 72:693.e1–693.e7CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Akihiko Okamura
    • 1
  • Masayuki Watanabe
    • 1
    Email author
  • Ryotaro Kozuki
    • 1
  • Tasuku Toihata
    • 1
  • Masami Yuda
    • 1
  • Yu Imamura
    • 1
  • Shinji Mine
    • 1
  1. 1.Department of Gastroenterological Surgery, Gastroenterology CenterThe Cancer Institute Hospital of Japanese Foundation for Cancer ResearchTokyoJapan

Personalised recommendations