Skip to main content

Advertisement

SpringerLink
Log in

Significance of Surgery for Resectable M1 Lymph Node Metastases Without Organ Metastasis in Esophageal Carcinoma in the Era of Neoadjuvant Treatment

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

Abstract

Background

M1 esophageal carcinoma goes beyond localized disease and requires treatment with systemic therapy. M1 status is primarily divided into two categories: M1 lymph node metastasis and distant organ metastasis. Oligometastasis is defined as a state of limited metastatic disease, and surgery for oligometastasis of distant organs is reported to be beneficial in limited conditions. The aim of this study was to investigate resected cases of M1 lymph node metastases as the only metastatic site in stage IVB esophageal carcinoma.

Patients and Methods

This study was a single-center retrospective cohort study. Patients with esophageal carcinoma who underwent esophagectomy with curative intent between April 2017 and December 2021 were examined. Neoadjuvant chemotherapy was our standard therapy and administered in almost all cases. We hypothesized that four sites of metastatic M1LN (supraclavicular (no. 104), pretracheal (no. 106pre), posterior thoracic para-aortic (no. 112aoP), and abdominal para-aortic (no. 16a2lat) LNs) were potentially resectable M1LN (rM1LN) metastases with curative intent and compared the prognosis of patients with and without rM1LN metastasis.

Results

Six hundred eight-two patients were included in the study. Among these patients, 80 had rM1LN metastasis and received surgery for curative intent. Short-term safety outcomes were equivalent between patients with and without rM1LN metastases. After propensity score matching, there were no significant differences in overall survival between patients with and without rM1LN metastasis. Multivariate analyses revealed that the only independent prognostic factor was ypN status.

Conclusion

The present study suggests the feasibility and favorable OS in the patients with resection of rM1LN metastasis.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.

    Article  PubMed  Google Scholar 

  2. Dubecz A, Gall I, Solymosi N, et al. Temporal trends in long-term survival and cure rates in esophageal cancer: a SEER database analysis. J Thorac Oncol. 2012;7(2):443–7.

    Article  PubMed  Google Scholar 

  3. Kitagawa Y, Ishihara R, Ishikawa H, et al. Esophageal cancer practice guidelines 2022 edited by the Japan esophageal society: part 1. Esophagus. 2023;20(3):343–72.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Obermannová R, Alsina M, Cervantes A, et al. Oesophageal cancer: ESMO clinical practice guideline for diagnosis, treatment and follow-up. Ann Oncol. 2022;33(10):992–1004.

    Article  PubMed  Google Scholar 

  5. Weichselbaum RR, Hellman S. Oligometastases revisited. Nat Rev Clin Oncol. 2011;8(6):378–82.

    Article  CAS  PubMed  Google Scholar 

  6. Kroese TE, van Laarhoven HWM, Schoppman SF, et al. Definition, diagnosis and treatment of oligometastatic oesophagogastric cancer: a Delphi consensus study in Europe. Eur J Cancer. 2023;185:28–39.

    Article  PubMed  Google Scholar 

  7. Schizas D, Mylonas KS, Kapsampelis P, et al. Patients undergoing surgery for oligometastatic oesophageal cancer survive for more than 2 years: bootstrapping systematic review data. Interact Cardiovasc Thorac Surg. 2020;31(3):299–304.

    Article  PubMed  Google Scholar 

  8. Kanamori J, Aokage K, Hishida T, et al. The role of pulmonary resection in tumors metastatic from esophageal carcinoma. Jpn J Clinl Oncol. 2017;47(1):25–31.

    Article  Google Scholar 

  9. Igaki H, Tachimori Y, Kato H. Improved survival for patients with upper and/or middle mediastinal lymph node metastasis of squamous cell carcinoma of the lower thoracic esophagus treated with 3-field dissection. Ann Surg. 2004;239(4):483–90.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Zhan PL, Canavan ME, Ermer T, et al. Nonregional lymph nodes as the only metastatic site in stage IV esophageal cancer. JTO Clin Res Rep. 2022;3(12):100426.

    PubMed  PubMed Central  Google Scholar 

  11. Schmidt T, Alldinger I, Blank S, et al. Surgery in oesophago-gastric cancer with metastatic disease: treatment, prognosis and preoperative patient selection. Eur J Surg Oncol. 2015;41(10):1340–7.

    Article  CAS  PubMed  Google Scholar 

  12. Tsuburaya A, Mizusawa J, Tanaka Y, et al. Neoadjuvant chemotherapy with S-1 and cisplatin followed by D2 gastrectomy with para-aortic lymph node dissection for gastric cancer with extensive lymph node metastasis. Br J Surg. 2014;101(6):653–60.

    Article  CAS  PubMed  Google Scholar 

  13. Daiko H, Nishimura M. A pilot study of the technical and oncologic feasibility of thoracoscopic esophagectomy with extended lymph node dissection in the prone position for clinical stage I thoracic esophageal carcinoma. Surg Endosc. 2012;26(3):673–80.

    Article  PubMed  Google Scholar 

  14. Robbins KT, Clayman G, Levine PA, et al. Neck dissection classification update: revisions proposed by the American Head and Neck Society and the American Academy of Otolaryngology-Head and Neck Surgery. Arch Otolaryngol Head Neck Surg. 2002;128(7):751–8.

    Article  PubMed  Google Scholar 

  15. Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: part II and III. Esophagus. 2017;14(1):37–65.

    Article  Google Scholar 

  16. Rice TW, Patil DT, Blackstone EH. 8th edition AJCC/UICC staging of cancers of the esophagus and esophagogastric junction: application to clinical practice. Ann Cardiothorac Surg. 2017;6(2):119–30.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: part I. Esophagus. 2017;14(1):1–36.

    Article  Google Scholar 

  18. Daiko H, Fujita T, Oguma J, et al. Novel minimally invasive approach to lymph node dissection around the left renal vein in patients with esophagogastric junction cancer. Esophagus. 2021;18(2):420–3.

    Article  PubMed  Google Scholar 

  19. Kroese TE, van Laarhoven HWM, Nilsson M, et al. Definition of oligometastatic esophagogastric cancer and impact of local oligometastasis-directed treatment: a systematic review and meta-analysis. Eur J Cancer. 2022;166:254–69.

    Article  CAS  PubMed  Google Scholar 

  20. Wu SG, Zhang WW, He ZY, Sun JY, Chen YX, Guo L. Sites of metastasis and overall survival in esophageal cancer: a population-based study. Cancer Manage Res. 2017;9:781–8.

    Article  Google Scholar 

  21. Matsuda S, Tsushima T, Kato K, et al. Defining conversion therapy for esophageal squamous cell carcinoma. Ann Gastroenterol Surg. 2023;7(1):7–9.

    Article  PubMed  Google Scholar 

  22. Kato K, Ito Y, Daiko H, et al. A randomized controlled phase III trial comparing two chemotherapy regimen and chemoradiotherapy regimen as neoadjuvant treatment for locally advanced esophageal cancer, JCOG1109 NExT study. J Clin Oncol. 2022;40:238–238.

    Article  Google Scholar 

  23. van Hagen P, Hulshof MCCM, van Lanschot JJB, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med. 2012;366(22):2074–84.

    Article  PubMed  Google Scholar 

  24. Hoeppner J, Lordick F, Brunner T, et al. ESOPEC: prospective randomized controlled multicenter phase III trial comparing perioperative chemotherapy (FLOT protocol) to neoadjuvant chemoradiation (CROSS protocol) in patients with adenocarcinoma of the esophagus (NCT02509286). BMC Cancer. 2016;16:503.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Reynolds JV, Preston SR, O’Neill B, et al. Trimodality therapy versus perioperative chemotherapy in the management of locally advanced adenocarcinoma of the oesophagus and oesophagogastric junction (Neo-AEGIS): an open-label, randomised, phase 3 trial. Lancet Gastroenterol Hepatol. 2023;8(11):1015–27.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Yokota T, Kato K, Hamamoto Y, et al. Phase II study of chemoselection with docetaxel plus cisplatin and 5-fluorouracil induction chemotherapy and subsequent conversion surgery for locally advanced unresectable oesophageal cancer. Br J Cancer. 2016;115(11):1328–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Terada M, Hara H, Daiko H, et al. Phase III study of tri-modality combination therapy with induction docetaxel plus cisplatin and 5-fluorouracil versus definitive chemoradiotherapy for locally advanced unresectable squamous-cell carcinoma of the thoracic esophagus (JCOG1510: TRIANgLE). Jpn J Clin Oncol. 2019;49(11):1055–60.

    Article  PubMed  Google Scholar 

  28. Hagens ERC, van Berge Henegouwen MI, van Sandick JW, et al. Distribution of lymph node metastases in esophageal carcinoma [TIGER study]: study protocol of a multinational observational study. BMC Cancer. 2019;19(1):662.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Ozawa H, Kawakubo H, Takeuchi M, et al. Prognostic significance of the number and extent of metastatic lymph nodes in patients with esophageal. Ann Surg Oncol. 2021;28(11):6355–63.

    Article  PubMed  Google Scholar 

  30. Kanemura T, Miyata H, Takeoka T, et al. Significance of dissection in each regional lymph-node station of esophageal cancer based on efficacy index and recurrence patterns after curative esophagectomy. Esophagus. 2023;20(3):402–9.

    Article  PubMed  Google Scholar 

  31. Honma Y, Hokamura N, Nagashima K, et al. Clinical outcomes of resectable esophageal cancer with supraclavicular lymph node metastases treated with curative intent. Anticancer Res. 2017;37(7):3741–9.

    PubMed  Google Scholar 

  32. Hsu CP, Hsu NY, Shai SE, Hsia JY, Chen CY. Pre-tracheal lymph node metastasis in squamous cell carcinoma of the thoracic esophagus. Eur J Surg Oncol. 2005;31(7):749–54.

    Article  CAS  PubMed  Google Scholar 

  33. Shishido Y, Miyata H, Sugimura K, et al. Successful resection after neoadjuvant chemotherapy for esophageal cancer with posterior thoracic paraaortic lymph node metastasis: a case report and literature review. Gen Thorac Cardiovasc Surg. 2017;65(9):542–8.

    Article  PubMed  Google Scholar 

  34. Itazaki Y, Tsujimoto H, Sugasawa H, et al. Bilateral approach for thoracoscopic esophagectomy in a patient with esophageal cancer and solitary posterior thoracic para-aortic lymph node metastasis. Acta Medica Okayama. 2020;74(6):521–4.

    PubMed  Google Scholar 

  35. Sano T, Sasako M, Yamamoto S, et al. Gastric cancer surgery: morbidity and mortality results from a prospective randomized controlled trial comparing D2 and extended para-aortic lymphadenectomy–Japan Clinical Oncology Group study 9501. J Clinical Oncol. 2004;22(14):2767–73.

    Article  Google Scholar 

  36. Al-Batran SE, Homann N, Pauligk C, et al. Effect of neoadjuvant chemotherapy followed by surgical resection on survival in patients with limited metastatic gastric or gastroesophageal junction cancer: the AIO-FLOT3 trial. JAMA Oncol. 2017;3(9):1237–44.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Lavacchi D, Giommoni E, Cianchi F, Antonuzzo L. Treatment strategy for oligometastatic gastric cancer: brief considerations. J Gastrointest Cancer. 2023;54(1):6–8.

    Article  PubMed  Google Scholar 

  38. Shimada H, Okazumi S-i, Matsubara H, et al. Surgical outcome after the clearance of abdominal metastatic lymph nodes in 138 patients with thoracic esophageal carcinoma. Am J Surg. 2007;193(4):448–52.

    Article  PubMed  Google Scholar 

  39. Mine S, Sano T, Hiki N, Yamada K, Nunobe S, Yamaguchi T. Lymphadenectomy around the left renal vein in Siewert type II adenocarcinoma of the oesophagogastric junction. Br J Surg. 2012;100(2):261–6.

    Article  PubMed  Google Scholar 

Download references

Funding

This study has no funding.

Author information

Authors and Affiliations

  1. Department of Esophageal Surgery, National Cancer Center Hospital, Tokyo, Japan

    Shota Igaue MD, Ryoko Nozaki MD, Daichi Utsunomiya MD, Yuto Kubo MD, Kentaro Kubo MD, Daisuke Kurita MD, Koshiro Ishiyama MD, PhD, Junya Oguma MD, PhD & Hiroyuki Daiko MD, PhD, FACS

  2. Department Head and Neck, Esophageal Medical Oncology, National Cancer Center Hospital, Tokyo, Japan

    Shun Yamamoto MD & Ken Kato MD, PhD

  3. Course of Advanced Clinical Research of Cancer, Juntendo University Graduate School of Medicine, Tokyo, Japan

    Shota Igaue MD & Hiroyuki Daiko MD, PhD, FACS

Authors
  1. Shota Igaue MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ryoko Nozaki MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daichi Utsunomiya MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuto Kubo MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kentaro Kubo MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Daisuke Kurita MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shun Yamamoto MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Koshiro Ishiyama MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Junya Oguma MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ken Kato MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hiroyuki Daiko MD, PhD, FACS
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroyuki Daiko MD, PhD, FACS.

Ethics declarations

Disclosure

Ken Kato reports consulting fees from Bristol Myers Squibb and Merck Sharp & Dohme, BeiGene, Roche, AstraZeneca, and Bayer; honoraria from Ono Pharmaceuticals, Bristol Myers Squibb, and Taiho; research funding from Ono Pharmaceuticals, Bristol Myers Squibb, Merck Sharp & Dohme, BeiGene, Chugai, Shionogi, AstraZeneca, and Bayer for research subjects outside the submitted work.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 16 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Igaue, S., Nozaki, R., Utsunomiya, D. et al. Significance of Surgery for Resectable M1 Lymph Node Metastases Without Organ Metastasis in Esophageal Carcinoma in the Era of Neoadjuvant Treatment. Ann Surg Oncol 31, 1525–1535 (2024). https://doi.org/10.1245/s10434-023-14562-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-023-14562-5

Keywords

Search

Navigation