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Surgery Today

, Volume 49, Issue 5, pp 378–386 | Cite as

Preoperative lymph node status on computed tomography influences the survival of pT1b, T2 and T3 esophageal squamous cell carcinoma

  • Kotaro SugawaraEmail author
  • Hiroharu Yamashita
  • Yukari Uemura
  • Koichi Yagi
  • Masato Nishida
  • Susumu Aikou
  • Sachiyo Nomura
  • Yasuyuki Seto
Original Article
  • 170 Downloads

Abstract

Purpose

The preoperative lymph node status is critical for tailoring optimal treatments for esophageal squamous cell carcinoma (ESCC). This study aimed to evaluate the prognostic impact of a diagnostic criterion based solely on the short-axis diameters of lymph nodes depicted on computed tomography (CT) in ESCC patients undergoing upfront esophagectomy.

Methods

We retrospectively reviewed 246 pT1b–T3 ESCC patients undergoing upfront esophagectomy. Clinically positive lymph node metastasis (cN+) was defined as nodes with a short-axis diameter of at least 8 mm on CT.

Results

Ninety-three patients had a cN+ status according to this criterion. The overall and recurrence-free survival rates were significantly lower in the cN+ group than in the cN− group (P < 0.001). The overall survival rate was markedly lower in the “pN2/3 and cN+” group than in the other groups (vs. pN0: P < 0.001, vs. pN1: P = 0.002, vs. “pN2/3 and cN−”: P < 0.001). However, the overall survival rate of the “pN2/3 and cN−” group was similar to that of the pN0–1 groups. A multivariate analysis showed that cN+ (P = 0.002), major complications (P = 0.001), and pT3 (P = 0.021) were independently associated with a poor prognosis.

Conclusion

A diagnostic criterion based solely on the short-axis diameters of lymph nodes depicted on CT was useful for stratifying the survival in ESCC patients.

Keywords

Esophageal squamous cell carcinoma Preoperative lymph node status Computed tomography 

Abbreviations

ESCC

Esophageal squamous cell carcinoma

CT

Computed tomography

NACRT

Neoadjuvant chemoradiotherapy

LN

Lymph node

VATS

Video-assisted thoracoscopic surgery

EGD

Esophagogastroduodenoscopy

NAC

Neoadjuvant chemotherapy

FDG-PET

18F-fluorodeoxyglucose positron tomography

EUS

Endoscopic ultrasonography

HR

Hazard ratios

CI

Confidence interval

Notes

Funding

None.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

References

  1. 1.
    Rustgi AK, El-Serag HB. Esophageal carcinoma. N Engl J Med. 2014;371(26):2499–509.CrossRefPubMedGoogle Scholar
  2. 2.
    Sugawara K, Yamashita H, Uemura Y, Mitsui T, Yagi K, Nishida M, et al. Numeric pathologic lymph node classification shows prognostic superiority to topographic pN classification in esophageal squamous cell carcinoma. Surgery. 2017;162;846–56.CrossRefPubMedGoogle Scholar
  3. 3.
    Ando N, Kato H, Igaki H, Shinoda M, Ozawa S, Shimizu 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. 2012;19(1):68–74.CrossRefPubMedGoogle Scholar
  4. 4.
    Sjoquist KM, Burmeister BH, Smithers BM, Zalcberg JR, Simes RJ, Barbour A, et al. Survival after neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal carcinoma: an updated meta-analysis. Lancet Oncol. 2011;12(7):681–92.CrossRefGoogle Scholar
  5. 5.
    Natsugoe S, Yoshinaka H, Shimada M, Sakamoto F, Morinaga T, Nakano S, et al. Number of lymph node metastases determined by presurgical ultrasound and endoscopic ultrasound is related to prognosis in patients with esophageal carcinoma. Ann Surg. 2001;234(5):613–8.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Peyre CG, Hagen JA, DeMeester SR, Van Lanschot JJ, Holscher A, Law S, et al. Predicting systemic disease in patients with esophageal cancer after esophagectomy: a multinational study on the significance of the number of involved lymph nodes. Ann Surg. 2008;248(6):979–85.CrossRefPubMedGoogle Scholar
  7. 7.
    Mariette C, Triboulet JP. Should resectable esophageal cancer be resected? Ann Surg Oncol. 2006;13(4):447–9.CrossRefPubMedGoogle Scholar
  8. 8.
    Kaklamanos IG, Walker GR, Ferry K, Franceschi D, Livingstone AS. Neoadjuvant treatment for resectable cancer of the esophagus and the gastroesophageal junction: a meta-analysis of randomized clinical trials. Ann Surg Oncol. 2003;10(7):754–61.CrossRefPubMedGoogle Scholar
  9. 9.
    Tepper J, Krasna MJ, Niedzwiecki D, Hollis D, Reed CE, Goldberg R, et al. Phase III trial of trimodality therapy with cisplatin, fluorouracil, radiotherapy, and surgery compared with surgery alone for esophageal cancer: CALGB 9781. J Clin Oncol. 2008;26(7):1086–92.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    van Hagen P, Hulshof MC, van Lanschot JJ, Steyerberg EW, van Berge Henegouwen MI, Wijnhoven BP, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med. 2012;366(22):2074–84.CrossRefGoogle Scholar
  11. 11.
    Mariette C, Dahan L, Mornex F, Maillard E, Thomas PA, Meunier B, et al. Surgery alone versus chemoradiotherapy followed by surgery for stage I and II esophageal cancer: final analysis of randomized controlled phase III trial FFCD 9901. J Clin Oncol. 2014;32(23):2416–22.CrossRefPubMedGoogle Scholar
  12. 12.
    Yokota T, Igaki H, Kato K, Tsubosa Y, Mizusawa J, Katayama H, et al. Accuracy of preoperative diagnosis of lymph node metastasis for thoracic esophageal cancer patients from JCOG9907 trial. Int J Clin Oncol. 2016;21(2):283–8.CrossRefPubMedGoogle Scholar
  13. 13.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    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;72:693-e1.CrossRefGoogle Scholar
  15. 15.
    Rice TW, Ishwaran H, Hofstetter WL, Kelsen DP, Apperson-Hansen C, Blackstone EH. Recommendations for pathologic staging (pTNM) of cancer of the esophagus and esophagogastric junction for the 8th edition AJCC/UICC staging manuals. Dis Esophagus. 2016;29(8):897–905.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240(2):205–13.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Pencina MJ, D’Agostino RB. Overall C as a measure of discrimination in survival analysis: model specific population value and confidence interval estimation. Stat Med. 2004;23(13):2109–23.CrossRefGoogle Scholar
  18. 18.
    Harrell FE Jr, Lee KL, Mark DB. Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996;15(4):361–87.CrossRefPubMedGoogle Scholar
  19. 19.
    Kajiyama Y, Iwanuma Y, Tomita N, Amano T, Isayama F, Matsumoto T, et al. Size analysis of lymph node metastasis in esophageal cancer: diameter distribution and assessment of accuracy of preoperative diagnosis. Esophagus. 2006;3(4):189–95.CrossRefGoogle Scholar
  20. 20.
    Park SY, Kim DJ, Jung HS, Yun MJ, Lee JW, Park CK. Relationship between the size of metastatic lymph nodes and positron emission tomographic/computer tomographic findings in patients with esophageal squamous cell carcinoma. World J Surg. 2015;39(12):2948–54.CrossRefPubMedGoogle Scholar
  21. 21.
    Lerut T, Flamen P, Ectors N, Van Cutsem E, Peeters M, Hiele M, et al. Histopathologic validation of lymph node staging with FDG-PET scan in cancer of the esophagus and gastroesophageal junction: a prospective study based on primary surgery with extensive lymphadenectomy. Ann Surg. 2000;232(6):743–52.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Grotenhuis BA, Wijnhoven BP, Poley JW, Hermans JJ, Biermann K, Spaander MC, et al. Preoperative assessment of tumor location and station-specific lymph node status in patients with adenocarcinoma of the gastroesophageal junction. World J Surg. 2013;37(1):147–55.CrossRefPubMedGoogle Scholar
  23. 23.
    Holscher AH, Dittler HJ, Siewert JR. Staging of squamous esophageal cancer: accuracy and value. World J Surg. 1994;18(3):312–20.CrossRefPubMedGoogle Scholar
  24. 24.
    Nishimaki T, Tanaka O, Ando N, Ide H, Watanabe H, Shinoda M, et al. Evaluation of the accuracy of preoperative staging in thoracic esophageal cancer. Ann Thorac Surg. 1999;68(6):2059–64.CrossRefPubMedGoogle Scholar
  25. 25.
    Kato H, Kuwano H, Nakajima M, Miyazaki T, Yoshikawa M, Ojima H, 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.CrossRefPubMedGoogle Scholar
  26. 26.
    Tio TL, Cohen P, Coene PP, Udding J, den Hartog Jager FC, Tytgat GN. Endosonography and computed tomography of esophageal carcinoma. Preoperative classification compared to the new (1987) TNM system. Gastroenterology. 1989;96(6):1478–86.CrossRefPubMedGoogle Scholar
  27. 27.
    O’Farrell NJ, Malik V, Donohoe CL, Johnston C, Muldoon C, Reynolds JV, et al. Appraisal of staging endoscopic ultrasonography in a modern high-volume esophageal program. World J Surg. 2013;37(7):1666–72.CrossRefPubMedGoogle Scholar
  28. 28.
    Stahl M, Budach W, Meyer HJ, Cervantes A. Esophageal cancer: clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2010;21(Suppl 5):v46–9.CrossRefPubMedGoogle Scholar
  29. 29.
    Ajani JA, D'Amico TA, Almhanna K, Bentrem DJ, Besh S, Chao J, et al. Esophageal and esophagogastric junction cancers, version 1.2015. J Natl Compr Canc Netw. 2015;13(2):194–227.CrossRefGoogle Scholar
  30. 30.
    Findlay JM, Bradley KM, Maile EJ, Braden B, Maw J, Phillips-Hughes J, et al. Pragmatic staging of oesophageal cancer using decision theory involving selective endoscopic ultrasonography, PET and laparoscopy. Br J Surg. 2015;102(12):1488–99.CrossRefPubMedGoogle Scholar
  31. 31.
    Yuan S, Yu Y, Chao KS, Fu Z, Yin Y, Liu T, et al. Additional value of PET/CT over PET in assessment of locoregional lymph nodes in thoracic esophageal squamous cell cancer. J Nucl Med. 2006;47(8):1255–9.PubMedGoogle Scholar
  32. 32.
    Yoon YC, Lee KS, Shim YM, Kim BT, Kim K, Kim TS. Metastasis to regional lymph nodes in patients with esophageal squamous cell carcinoma: CT versus FDG PET for presurgical detection prospective study. Radiology. 2003;227(3):764–70.CrossRefPubMedGoogle Scholar
  33. 33.
    Funai T, Osugi H, Higashino M, Kinoshita H. Estimation of lymph node metastasis by size in patients with intrathoracic oesophageal cancer. Br J Surg. 2000;87(9):1234–9.CrossRefPubMedGoogle Scholar
  34. 34.
    Dhar DK, Yoshimura H, Kinukawa N, Maruyama R, Tachibana M, Kohno H, et al. Metastatic lymph node size and colorectal cancer prognosis. J Am Coll Surg. 2005;200(1):20–8.CrossRefPubMedGoogle Scholar
  35. 35.
    Dhar DK, Tachibana M, Kinukawa N, Riruke M, Kohno H, Little AG, et al. The prognostic significance of lymph node size in patients with squamous esophageal cancer. Ann Surg Oncol. 2002;9(10):1010–6.CrossRefPubMedGoogle Scholar
  36. 36.
    Chi YK, Chen Y, Li XT, Sun YS. Prognostic significance of the size and number of lymph nodes on pre and post neoadjuvant chemotherapy CT in patients with pN0 esophageal squamous cell carcinoma: a 5-year follow-up study. Oncotarget. 2017;8(37):61662–73.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Tokunaga M, Sugisawa N, Tanizawa Y, Bando E, Kawamura T, Terashima M. The impact of preoperative lymph node size on long-term outcome following curative gastrectomy for gastric cancer. Ann Surg Oncol. 2013;20(5):1598–603.CrossRefPubMedGoogle Scholar
  38. 38.
    Chi YK, Zhang XP, Li J, Sun YS. To be or not to be: significance of lymph nodes on pretreatment CT in predicting survival of rectal cancer patients. Eur J Radiol. 2011;77(3):473–7.CrossRefPubMedGoogle Scholar
  39. 39.
    Gabriel E, Attwood K, Du W, Tuttle R, Alnaji RM, Nurkin S, et al. Association between clinically staged node-negative esophageal adenocarcinoma and overall survival benefit from neoadjuvant chemoradiation. JAMA Surg. 2016;151(3):234–45.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Speicher PJ, Ganapathi AM, Englum BR, Hartwig MG, Onaitis MW, D’Amico TA, et al. Induction therapy does not improve survival for clinical stage T2N0 esophageal cancer. J Thorac Oncol. 2014;9(8):1195–201.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Mine S, Watanabe M, Imamura Y, Okamura A, Kurogochi T, Sano T. Clinical significance of the pre-therapeutic nodal size in patients undergoing neo-adjuvant treatment followed by esophagectomy for esophageal squamous cell carcinoma. World J Surg. 2017;41(1):184–90.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Department of Gastrointestinal Surgery, Graduate School of MedicineThe University of TokyoTokyoJapan
  2. 2.Department of Bariatric and Metabolic Care, Graduate School of MedicineThe University of TokyoTokyoJapan
  3. 3.Biostatistics Division, Clinical Research Support Center, Graduate School of MedicineThe University of TokyoTokyoJapan

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