Abstract
Although increasing evidence indicates that cancers are associated with inflammation, the prognostic role of the neutrophil-to-lymphocyte ratio (NLR) and the platelet-to-lymphocyte ratio (PLR) in patients with esophageal squamous cell carcinoma remains controversial. We determined the prognostic roles of NLR and PLR in patients with esophageal squamous cell carcinoma who underwent surgical treatment. We retrospectively reviewed 119 patients with esophageal squamous cell carcinoma who underwent surgical resection and complete lymph node dissection from 2004 to 2012. The preoperative NLR and PLR were measured. The patients included 112 (94.1 %) males (mean age, 63.64 ± 8.42 years) of whom 37 (31.1 %) were pathological stage I, 33 (27.7 %) were stage II, and 49 (41.2 %) were stage III. The median follow-up period was 28.68 months. Recurrence was reported in 48 (40.3 %) patients. Mean NLR and PLR were 2.35 ± 1.39 and 140.77 ± 70.47, respectively. A multivariate analysis revealed that NLR was a risk factor for disease-free survival (DFS) (hazard ratio [HR], 1.194; p = 0.031) and overall survival (OS) (HR, 1.230; p = 0.011), whereas PLR was not a risk factor for DFS or OS. The 3-year OS rates were 51.0 % in low-NLR (<2.97) patients and 17.4 % in high-NLR (≥2.97) patients (p = 0.007). Akaike’s information criterion decreased when the NLR was included in the multivariate model compared to the multivariate model without NLR. A high NLR was a significant prognostic factor for OS and DFS in patients with surgically treated esophageal squamous cell carcinoma, whereas PLR showed no prognostic significance.
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Garcia M, Jemal A, Ward E, Center M, Hao Y, Siegel R, et al. Global cancer facts and figures 2007. Atlanta, GA: American Cancer Society. 2007;1(3):52.
Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63(1):11–30.
Yuequan J, Shifeng C, Bing Z. Prognostic factors and family history for survival of esophageal squamous cell carcinoma patients after surgery. Ann Thorac Surg. 2010;90(3):908–13.
Guo H, Zhu H, Xi Y, Zhang B, Li L, Huang Y, et al. Diagnostic and prognostic value of 18F-FDG PET/CT for patients with suspected recurrence from squamous cell carcinoma of the esophagus. J Nucl Med. 2007;48(8):1251–8.
Tachibana M, Hirahara N, Kinugasa S, Yoshimura H. Clinicopathologic features of superficial esophageal cancer: results of consecutive 100 patients. Ann Surg Oncol. 2008;15(1):104–16.
Ancona E, Rampado S, Cassaro M, Battaglia G, Ruol A, Castoro C, et al. Prediction of lymph node status in superficial esophageal carcinoma. Ann Surg Oncol. 2008;15(11):3278–88.
Lee PC, Port JL, Paul S, Stiles BM, Altorki NK. Predictors of long-term survival after resection of esophageal carcinoma with nonregional nodal metastases. Ann Thorac Surg. 2009;88(1):186–93.
DeNardo DG, Johansson M, Coussens LM. Immune cells as mediators of solid tumor metastasis. Cancer Metastasis Rev. 2008;27(1):11–8.
Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet. 2001;357(9255):539–45.
Cho H, Hur HW, Kim SW, Kim SH, Kim JH, Kim YT, et al. Pre-treatment neutrophil to lymphocyte ratio is elevated in epithelial ovarian cancer and predicts survival after treatment. Cancer Immunol Immunother. 2009;58(1):15–23.
Ueno H, Hawrylowicz CM, Banchereau J. Immunological intervention in human diseases. J Transl Med. 2007;5(1):59.
Paramanathan A, Saxena A, Morris DL. A systematic review and meta-analysis on the impact of pre-operative neutrophil lymphocyte ratio on long term outcomes after curative intent resection of solid tumours. Surg Oncol. 2014;23(1):31–9.
Cedres S, Torrejon D, Martinez A, Martinez P, Navarro A, Zamora E, et al. Neutrophil to lymphocyte ratio (NLR) as an indicator of poor prognosis in stage IV non-small cell lung cancer. Clin Transl Oncol. 2012;14(11):864–9.
Proctor M, McMillan D, Morrison D, Fletcher C, Horgan P, Clarke S. A derived neutrophil to lymphocyte ratio predicts survival in patients with cancer. Br J Cancer. 2012;107(4):695–9.
Rice TW, Blackstone EH, Rusch VW. of the AJCC Cancer Staging Manual: esophagus and esophagogastric junction. Ann Surg Oncol. 2010;17(7):1721–4.
Stylianou C, Pickles A, Roberts SA. Using Bonferroni, BIC and AIC to assess evidence for alternative biological pathways: covariate selection for the multilevel embryo-uterus model. BMC Med Res Methodol. 2013;13(1):73.
Hothorn T, Lausen B. On the exact distribution of maximally selected rank statistics. Comput Stat Data Anal. 2003;43(2):121–37.
Sharaiha RZ, Halazun KJ, Mirza F, Port JL, Lee PC, Neugut AI, et al. Elevated preoperative neutrophil: lymphocyte ratio as a predictor of postoperative disease recurrence in esophageal cancer. Ann Surg Oncol. 2011;18(12):3362–9.
Sato H, Tsubosa Y, Kawano T. Correlation between the pretherapeutic neutrophil to lymphocyte ratio and the pathologic response to neoadjuvant chemotherapy in patients with advanced esophageal cancer. World J Surg. 2012;36(3):617–22.
Rashid F, Waraich N, Bhatti I, Saha S, Khan RN, Ahmed J, et al. A pre-operative elevated neutrophil: lymphocyte ratio does not predict survival from oesophageal cancer resection. World J Surg Oncol. 2010;8(1):1–10.
Dutta S, Crumley AB, Fullarton GM, Horgan PG, McMillan DC. Comparison of the prognostic value of tumour-and patient-related factors in patients undergoing potentially curative resection of oesophageal cancer. World J Surg. 2011;35(8):1861–6.
Feng J-F, Huang Y, Liu J-S. Combination of neutrophil lymphocyte ratio and platelet lymphocyte ratio is a useful predictor of postoperative survival in patients with esophageal squamous cell carcinoma. OncoTargets Ther. 2013;6:1605.
Feng J-F, Huang Y, Chen QX. A new inflammation index is useful for patients with esophageal squamous cell carcinoma. OncoTargets Ther. 2014;7:1811.
Kishi Y, Kopetz S, Chun YS, Palavecino M, Abdalla EK, Vauthey J-N. Blood neutrophil-to-lymphocyte ratio predicts survival in patients with colorectal liver metastases treated with systemic chemotherapy. Ann Surg Oncol. 2009;16(3):614–22.
Aliustaoglu M, Bilici A, Ustaalioglu BBO, Konya V, Gucun M, Seker M, et al. The effect of peripheral blood values on prognosis of patients with locally advanced gastric cancer before treatment. Med Oncol. 2010;27(4):1060–5.
Liao Q, Zhao Y-P, Yang Y-C, Li L-J, Long X, Han S-M. Combined detection of serum tumor markers for differential diagnosis of solid lesions located at the pancreatic head. Hepatobiliary Pancreat Dis Int. 2007;6(6):641–5.
Bhatti I, Peacock O, Lloyd G, Larvin M, Hall RI. Preoperative hematologic markers as independent predictors of prognosis in resected pancreatic ductal adenocarcinoma: neutrophil-lymphocyte versus platelet-lymphocyte ratio. Am J Surg. 2010;200(2):197–203.
Klinger MH, Jelkmann W. Review: role of blood platelets in infection and inflammation. J Interf Cytokine Res. 2002;22(9):913–22.
Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860–7.
Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, et al. Polarization of tumor-associated neutrophil phenotype by TGF-β: “N1” versus “N2” TAN. Cancer Cell. 2009;16(3):183–94.
Michiels S, Koscielny S, Hill C. Prediction of cancer outcome with microarrays: a multiple random validation strategy. Lancet. 2005;365(9458):488–92.
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The institutional review board of our institution approved this retrospective study (AJIRB-MED-MDB-15-400), and the requirement to obtain informed consent was waived.
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This study was supported by the new faculty research fund of Ajou University School of Medicine.
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Jung, J., Park, S.Y., Park, Sj. et al. Prognostic value of the neutrophil-to-lymphocyte ratio for overall and disease-free survival in patients with surgically treated esophageal squamous cell carcinoma. Tumor Biol. 37, 7149–7154 (2016). https://doi.org/10.1007/s13277-015-4596-3
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DOI: https://doi.org/10.1007/s13277-015-4596-3