Abstract
Background
It is reported that several systemic immunoinflammatory measures, including systemic immune-inflammatory index (SII), neutrophil-to-lymphocyte ratio (NLR), platelet-to-lymphocyte ratio, and C-reactive protein (CRP)-to-albumin ratio (CAR), are associated with survival in patients with various types of cancer.
Objective
The aim of the present study was to clear which systemic immunoinflammatory measures had the greatest prognostic values. In addition, we examined which component had the greatest prognostic power in patients with esophageal cancer.
Methods
Preoperative systemic immunoinflammatory measures were evaluated in 143 patients undergoing esophageal resection for esophageal cancer from 2009 to 2014. Univariate and multivariate analyses were performed to determine the prognostic significance of these markers. Receiver operating characteristic (ROC) curves were plotted, and the area under the ROC curves (AUROCs) were compared to verify the accuracy of each measure in predicting overall survival (OS).
Results
In univariate analysis, preoperative SII, NLR, and CAR were the predictors of OS in patients who underwent esophagectomy for esophageal cancer (p < 0.05, respectively), whereas in multivariate analysis, CAR and pathological tumor depth were the significant predictors of OS (hazard ratio [HR] 1.994, p = 0.03 vs. HR 1.967, p = 0.02, respectively). According to AUROC, the CRP (0.66) and albumin levels (0.66) were more important systemic immunoinflammatory measures than neutrophil (0.58), lymphocyte (0.63), and platelet (0.56) levels.
Conclusion
Among systemic immunoinflammatory measures, CAR was the most significant predictor of OS in patients with esophageal cancer. CRP and albumin levels were more important components of systemic immunoinflammatory measures.
Similar content being viewed by others
References
Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med. 2003; 349: 2241–52.
Ferlay J, Soerjomataram I, Dikshit R et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015; 136: E359–86.
Kinoshita A, Onoda H, Imai N et al. Comparison of the prognostic value of inflammation-based prognostic scores in patients with hepatocellular carcinoma. Br J Cancer. 2012; 107: 988–93.
Kubo T, Ono S, Ueno H et al. Impact of the perioperative neutrophil-to-lymphocyte ratio on the long-term survival following an elective resection of colorectal carcinoma. Int J Colorectal Dis. 2014; 29: 1091–99.
Kishi Y, Kopetz S, Chun YS et al. Blood neutrophil-to-lymphocyte ratio predicts survival in patients with colorectal liver metastases treated with systemic chemotherapy. Ann Surg Oncol. 2009; 16: 614–22.
Yang C, Sun W, Cui W et al. Procoagulant role of neutrophil extracellular traps in patients with gastric cancer. Int J Clin Exp Pathol. 2015; 8: 14075–86.
Duan H, Zhang X, Wang F-X et al. Prognostic role of neutrophil-lymphocyte ratio in operable esophageal squamous cell carcinoma. World J Gastroenterol. 2015; 21: 5591.
Feng JF, Huang Y, Chen QX. Preoperative platelet lymphocyte ratio (PLR) is superior to neutrophil lymphocyte ratio (NLR) as a predictive factor in patients with esophageal squamous cell carcinoma. World J Surg Oncol. 2014; 12: 58.
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: 617–22.
Sharaiha RZ, Halazun KJ, Mirza F et al. Elevated preoperative neutrophil: lymphocyte ratio as a predictor of postoperative disease recurrence in esophageal cancer. Ann Surg Oncol. 2011; 18: 3362–69.
Wei X-L, Wang F-H, Zhang D-S et al. A novel inflammation-based prognostic score in esophageal squamous cell carcinoma: the C-reactive protein/albumin ratio. BMC Cancer. 2015; 15: 350.
Xu X-L, Yu H-Q, Hu W et al. A novel inflammation-based prognostic score, the C-reactive protein/albumin ratio predicts the prognosis of patients with operable esophageal squamous cell carcinoma. PloS One. 2015; 10: e0138657.
Wang K, Diao F, Ye Z et al. Prognostic value of systemic immune-inflammation index in patients with gastric cancer. Chin J Cancer. 2017; 36: 75.
Sobin LH, Gospodarowicz MK, Wittekind C. TNM classification of malignant tumours. Wiley, New York; 2011.
Tsujimoto H, Takahata R, Nomura S et al. Video-assisted thoracoscopic surgery for esophageal cancer attenuates postoperative systemic responses and pulmonary complications. Surgery. 2012; 151: 667–73.
Tsujimoto H, Ono S, Sugasawa H et al. Gastric tube reconstruction by laparoscopy-assisted surgery attenuates postoperative systemic inflammatory response after esophagectomy for esophageal cancer. World J Surg. 2010; 34: 2830–36.
Aiko S, Yoshizumi Y, Ishizuka T et al. Enteral immuno-enhanced diets with arginine are safe and beneficial for patients early after esophageal cancer surgery. Dis Esophagus. 2008; 21: 619–27.
Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008; 454: 436.
Ying H-Q, Deng Q-W, He B-S et al. The prognostic value of preoperative NLR, d-NLR, PLR and LMR for predicting clinical outcome in surgical colorectal cancer patients. Med Oncol. 2014; 31: 305.
Sarraf KM, Belcher E, Raevsky E et al. Neutrophil/lymphocyte ratio and its association with survival after complete resection in non–small cell lung cancer. J Thorac Cardiovasc Surg. 2009; 137: 425–28.
Liu X, Sun X, Liu J et al. Preoperative C-reactive protein/albumin ratio predicts prognosis of patients after curative resection for gastric cancer. Transl Oncol. 2015; 8: 339–45.
Wang J, Jia Y, Wang N et al. The clinical significance of tumor-infiltrating neutrophils and neutrophil-to-CD8+ lymphocyte ratio in patients with resectable esophageal squamous cell carcinoma. J Transl Med. 2014; 12: 7.
Tsujimoto H, Ono S, Ichikura T et al. Roles of inflammatory cytokines in the progression of gastric cancer: friends or foes? Gastric Cancer. 2010; 13: 212–21.
Shimada H, Takiguchi N, Kainuma O et al. High preoperative neutrophil-lymphocyte ratio predicts poor survival in patients with gastric cancer. Gastric Cancer 2010; 13: 170–76.
Hirahara N, Tajima Y, Fujii Y et al. A novel prognostic scoring system using inflammatory response biomarkers for esophageal squamous cell carcinoma. World J Surg. 2018; 42: 172–84.
Ando N, Kato H, Igaki 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: 68–74.
Dutta S, Crumley AB, Fullarton GM et al. Comparison of the prognostic value of tumour and patient related factors in patients undergoing potentially curative resection of gastric cancer. Am J Surg. 2012; 204: 294–99.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Disclosures
Yusuke Ishibashi, Hironori Tsujimoto, Shuichi Hiraki, Isao Kumano, Yoshihisa Yaguchi, Hiroyuki Horiguchi, Shinsuke Nomura, Nozomi Ito, Eiji Shinto, Suefumi Aosasa, Junji Yamamoto, and Hideki Ueno declare no conflicts of interest directly relevant to the content of this article.
Ethical Statements
Written informed consent was obtained from all patients who participated in this study.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Fig.
1 Overall survival after esophagectomy for esophageal cancer according to the PLR. PLR platelet-to-lymphocyte ratio (TIFF 835 kb)
Table
1 Univariate and multivariate analyses that may affect overall survival of esophageal cancer patients. HR hazard ratio, CI confidence interval, SII systemic immune-inflammatory index, NLR neutrophil-to-lymphocyte ratio, PLR platelet-to-lymphocyte ratio, CAR C-reactive protein-to-albumin ratio (DOCX 14 kb)
Table
2 Platelet counts and AUROCs used to predict 5-year survival in patients who did or did not receive antiplatelet and/or anticoagulant therapies. Platelet counts are expressed as mean ± standard deviation. AUROC area under receiver operating characteristic curve (DOCX 11 kb)
Rights and permissions
About this article
Cite this article
Ishibashi, Y., Tsujimoto, H., Hiraki, S. et al. Prognostic Value of Preoperative Systemic Immunoinflammatory Measures in Patients with Esophageal Cancer. Ann Surg Oncol 25, 3288–3299 (2018). https://doi.org/10.1245/s10434-018-6651-y
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1245/s10434-018-6651-y