Abstract
Background
The American Joint Committee on Cancer (AJCC) nodal staging for esophageal squamous cell carcinoma (ESCC) has been defined by the number of metastatic lymph nodes (N system). However, the precise counting of individual positive lymph nodes is difficult and unreliable in some clinical settings, which calls for a more available and reliable system. This study examined the performance of a newly proposed nodal staging category, termed the S system, based on the number of metastatic lymph node stations.
Methods
Using the Kaplan–Meier method and Cox-regression analysis, this study retrospectively analyzed the overall survival (OS) of 2285 ESCC patients who underwent esophagectomy in three major China hospitals. Predictive models were constructed, and C-indices were computed to evaluate the discriminatory power of the S system, and to compare it with the N system.
Results
The categories defined by the S system were more homogeneous in terms of OS than those defined by the N system. Overall, the S system had a slightly better C-index (p = 0.659) than the N system ((p = 0.658). Subgroup analyses also showed that the C-index of the S system was slightly better than that of the N system for each subgroup of sex and age, but the two were comparable for each subgroup defined by the tumor location.
Conclusion
The S system demonstrated a competing prognostic performance compared with the current AJCC N system. Due to the relatively easy accessibility of the number of metastatic lymph node stations, the S system may offer an easier option for cancer staging without a loss of discriminative power.
Similar content being viewed by others
References
Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108.
Enzinger P, Mayer R. Esophageal cancer. N Engl J Med. 2003;349:2241–52.
Rice TW, Ishwaran H, Hofstetter WL, et al. Esophageal cancer: associations with (pN+) lymph node metastases. Ann Surg. 2017;265:122–9.
Gertler R, Stein HJ, Schuster T, Rondak IC, Höfler H, Feith M. Prevalence and topography of lymph node metastases in early esophageal and gastric cancer. Ann Surg. 2014;259:96–101.
Hsu PK, Wu YC, Chou TY, Huang CS, Hsu WH. Comparison of the 6th and 7th editions of the American Joint Committee on Cancer tumor-node-metastasis staging system in patients with resected esophageal carcinoma. Ann Thorac Surg. 2010;89:1024–31.
Talsma K, van Hagen P, Grotenhuis BA, et al. Comparison of the 6th and 7th editions of the UICC–AJCC TNM classification for esophageal cancer. Ann Surg Oncol. 2012;19:2142–8.
Wang J, Dang P, Weng HR, et al. Comparison of a lymph node ratio based staging system with the 7th AJCC system for gastric cancer: analysis of 18,043 patients from the SEER database. Ann Surg. 2012;255:478–85.
Amin MB, Edge S, Greene F, et al. AJCC cancer staging manual. Chicago, IL: Springer; 2017. p. 185–202.
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;35:1303–10.
Wang L, Zhang H, Ruan Y, et al. Tuberculosis prevalence in China, 1990–2010: a longitudinal analysis of national survey data. Lancet. 2014;383:2057–64.
Peng J, Wang WP, Dong T, Cai J, Ni PZ, Chen LQ. Refining the nodal staging for esophageal squamous cell carcinoma based on lymph node stations. Ann Thorac Surg. 2016;101:280–6.
Chen SB, Weng HR, Wang G, et al. Prognostic factors and outcome for patients with esophageal squamous cell carcinoma underwent surgical resection alone: evaluation of the seventh edition of the American Joint Committee on Cancer staging system for esophageal squamous cell carcinoma. J Thorac Oncol. 2013;8:495–501.
Ning ZH, Wang ZG, Chen J, et al. Proposed modification of nodal staging as an alternative to the seventh edition of the American Joint Committee on cancer tumor-node-metastasis staging system improves the prognostic prediction in the resected esophageal squamous cell carcinoma. J Thorac Oncol. 2015;10:1091–8.
Yamasaki M, Miyata H, Miyazaki Y, et al. 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. 2014;21:2850–6.
Peng J, Wang WP, Yuan Y, Wang ZQ, Wang Y, Chen LQ. Adequate lymphadenectomy in patients with oesophageal squamous cell carcinoma: resecting the minimal number of lymph node stations. Eur J Cardiothorac Surg. 2016;49:e141–6.
Edge S, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A. AJCC cancer staging manual. New York, NY: Springer; 2010.
Udagawa H, Ueno M. Comparison of two major staging systems of esophageal cancer-toward more practical common scale for tumor staging. Ann Transl Med. 2018;6:76.
Zhang D, Zheng Y, Wang Z, et al. Comparison of the 7th and proposed 8th editions of the AJCC/UICC TNM staging system for esophageal squamous cell carcinoma underwent radical surgery. Eur J Surg Oncol. 2017;43:1949–55.
Rice TW, Apperson-Hansen C, DiPaola LM, et al. Worldwide esophageal cancer collaboration: clinical staging data. Dis Esophagus. 2016;29:707–14.
Rice TW, Lerut TE, Orringer MB, et al. Worldwide esophageal cancer collaboration: neoadjuvant pathologic staging data. Dis Esophagus. 2016;29:715–23.
Rice TW, Chen LQ, Hofstetter WL, et al. Worldwide esophageal cancer collaboration: pathologic staging data. Dis Esophagus. 2016;29:724–33.
Fu X, Liu Q, Luo K, et al. Lymph node station ratio: revised nodal category for resected esophageal squamous cell carcinoma patients. J Surg Oncol. 2017;116:939–46.
Hsu PK, Huang CS, Wang BY, Wu YC, Chou TY, Hsu WH. The prognostic value of the number of negative lymph nodes in esophageal cancer patients after transthoracic resection. Ann Thorac Surg. 2013;96:995–1001.
Chen SB, Weng HR, Wang G, et al. Lymph node ratio-based staging system for esophageal squamous cell carcinoma. World J Gastroenterol. 2015;21:7514–21.
Tan Z, Ma G, Yang H, Zhang L, Rong T, Lin P. Can lymph node ratio replace pn categories in the tumor-node-metastasis classification system for esophageal cancer? J Thorac Oncol. 2014;9:1214–21.
Tong LL, Gao P, Wang ZN, et al. Can lymph node ratio take the place of pN categories in the UICC/AJCC TNM classification system for colorectal cancer? Ann Surg Oncol. 2011;18:2453–60.
Yokota T, Igaki H, Kato K, et al. Accuracy of preoperative diagnosis of lymph node metastasis for thoracic esophageal cancer patients from JCOG9907 trial. Int J Clin Oncol. 2016;21:283–8.
Choi J, Kim SG, Kim JS, Jung HC, Song IS. Comparison of endoscopic ultrasonography (EUS), positron emission tomography (PET), and computed tomography (CT) in the preoperative locoregional staging of resectable esophageal cancer. Surg Endosc. 2010;24:1380–6.
Acknowledgment
The authors are grateful for Martina Fu, the editorial assistant from Yi Li’s lab at the University of Michigan, for proofreading the manuscript and for many helpful suggestions that improved the presentation of the article. This study was supported by a Sichuan Science and Technology Program (2018HH0150).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Disclosure
There are no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yuan, Y., Hong, H.G., Zeng, X. et al. Lymph Node Station-Based Nodal Staging System for Esophageal Squamous Cell Carcinoma: A Large-Scale Multicenter Study. Ann Surg Oncol 26, 4045–4052 (2019). https://doi.org/10.1245/s10434-019-07601-7
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1245/s10434-019-07601-7