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Combined analysis of the pre- and postoperative neutrophil–lymphocyte ratio predicts the outcomes of patients with gastric cancer

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Abstract

Purpose

The neutrophil–lymphocyte ratio (NLR) is a biochemical marker of the systemic inflammatory response and has been associated with prognosis for various types of cancer. This retrospective study investigates the relationship between the pre- and postoperative NLR and the prognosis of gastric cancer patients.

Methods

The subjects were 280 patients who underwent curative surgery for histopathologically diagnosed gastric adenocarcinoma.

Results

The preoperative NLR was significantly correlated with tumor size, tumor depth, lymphatic invasion, venous invasion, and disease stage. In contrast, there was no correlation between the postoperative NLR and the various clinicopathological variables. Prognosis was significantly worse for patients with a high preoperative NLR than for those with a low preoperative NLR. Prognosis was also significantly worse for patients with a high postoperative NLR than for those with a low postoperative NLR. Furthermore, the prognosis was worse for gastric cancer patients whose pre- and postoperative NLRs were both high. Multivariate analysis indicated that a high pre- and postoperative NLR was an independent prognostic indicator.

Conclusions

The combination of pre- and postoperative NLRs appears to be useful for predicting the prognosis of gastric cancer patients.

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References

  1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.

    Article  PubMed  Google Scholar 

  2. Bozzetti F, Bonfanti G, Morabito A, Bufalino R, Menotti V, Andreola S, et al. A multifactorial approach for the prognosis of patients with carcinoma of the stomach after curative resection. Surg Gynecol Obstet. 1986;162:229–34.

    CAS  PubMed  Google Scholar 

  3. Maruyama K. The most important prognostic factors for gastric cancer patients. Scand J Gastroenterol. 1987;22:63–8.

    Article  Google Scholar 

  4. Fuse N, Kuboki Y, Kuwata T, Nishina T, Kadowaki S, Shinozaki E, et al. Prognostic impact of HER2, EGFR, and c-MET status on overall survival of advanced gastric cancer patients. Gastric Cancer. 2016;19:183–91.

    Article  CAS  PubMed  Google Scholar 

  5. Higaki E, Kuwata T, Nagatsuma AK, Nishida Y, Kinoshita T, Aizawa M, et al. Gene copy number gain of EGFR is a poor prognostic biomarker in gastric cancer: evaluation of 855 patients with bright-field dual in situ hybridization (DISH) method. Gastric Cancer. 2016;19:63–73.

    Article  CAS  PubMed  Google Scholar 

  6. Okugawa Y, Toiyama Y, Hur K, Toden S, Saigusa S, Tanaka K, et al. Metastasis-associated long non-coding RNA drives gastric cancer development and promotes peritoneal metastasis. Carcinogenesis. 2014;35:2731–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Wu JG, Wang JJ, Jiang X, Lan JP, He XJ, Wang HJ, et al. MiR-125b promotes cell migration and invasion by targeting PPP1CA-Rb signal pathways in gastric cancer, resulting in a poor prognosis. Gastric Cancer. 2015;18:729–39.

    Article  CAS  PubMed  Google Scholar 

  8. Kurokawa Y, Matsuura N, Kimura Y, Adachi S, Fujita J, Imamura H, et al. Multicenter large-scale study of prognostic impact of HER2 expression in patients with resectable gastric cancer. Gastric Cancer. 2015;18:691–7.

    Article  CAS  PubMed  Google Scholar 

  9. Zhang H, Wang X, Shen Z, Xu J, Qin J, Sun Y. Infiltration of diametrically polarized macrophages predicts overall survival of patients with gastric cancer after surgical resection. Gastric Cancer. 2015;18:740–50.

    Article  CAS  PubMed  Google Scholar 

  10. Park HJ, Ahn JY, Jung HY, Lim H, Lee JH, Choi KS, et al. Clinical characteristics and outcomes for gastric cancer patients aged 18–30 years. Gastric Cancer. 2014;17:649–60.

    Article  PubMed  Google Scholar 

  11. Nam DH, Lee YK, Park JC, Lee H, Shin SK, Lee SK, et al. Prognostic value of early postoperative tumor marker response in gastric cancer. Ann Surg Oncol. 2013;20:3905–11.

    Article  PubMed  Google Scholar 

  12. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.

    Article  CAS  PubMed  Google Scholar 

  13. Lee S, Oh SY, Kim SH, Lee JH, Kim MC, Kim KH, et al. Prognostic significance of neutrophil lymphocyte ratio and platelet lymphocyte ratio in advanced gastric cancer patients treated with FOLFOX chemotherapy. BMC Cancer. 2013;13:350.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Templeton AJ, McNamara MG, Seruga B, Vera-Badillo FE, Aneja P, Ocana A, et al. Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis. J Natl Cancer Inst. 2014;106:dju124.

    Article  PubMed  Google Scholar 

  15. Proctor MJ, Morrison DS, Talwar D, Balmer SM, Fletcher CD, O’Reilly DS, et al. A comparison of inflammation-based prognostic scores in patients with cancer. A Glasgow Inflammation Outcome Study. Eur J Cancer. 2011;47:2633–41.

    Article  PubMed  Google Scholar 

  16. Pinato DJ, North BV, Sharma R. A novel, externally validated inflammation-based prognostic algorithm in hepatocellular carcinoma: the prognostic nutritional index (PNI). Br J Cancer. 2012;106:1439–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Fox P, Hudson M, Brown C, Lord S, Gebski V, De Souza P, et al. Markers of systemic inflammation predict survival in patients with advanced renal cell cancer. Br J Cancer. 2013;109:147–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Stotz M, Gerger A, Eisner F, Szkandera J, Loibner H, Ress AL, et al. Increased neutrophil–lymphocyte ratio is a poor prognostic factor in patients with primary operable and inoperable pancreatic cancer. Br J Cancer. 2013;109:416–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kim JH, Han DS, Bang HY, Kim PS, Lee KY. Preoperative neutrophil-to-lymphocyte ratio is a prognostic factor for overall survival in patients with gastric cancer. Ann Surg Treat Res. 2015;89:81–6.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Kumar R, Geuna E, Michalarea V, Guardascione M, Naumann U, Lorente D, et al. The neutrophil–lymphocyte ratio and its utilisation for the management of cancer patients in early clinical trials. Br J Cancer. 2015;112:1157–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 2011;14:101–12.

    Article  Google Scholar 

  22. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al. The Clavien–Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187–96.

    Article  PubMed  Google Scholar 

  23. Katayama H, Kurokawa Y, Nakamura K, Ito H, Kanemitsu Y, Masuda N, et al. Extended Clavien–Dindo classification of surgical complications: Japan Clinical Oncology Group postoperative complications criteria. Surg Today. 2016;46:668–85.

    Article  PubMed  Google Scholar 

  24. Langsenlehner T, Thurner EM, Krenn-Pilko S, Langsenlehner U, Stojakovic T, Gerger A, et al. Validation of the neutrophil-to-lymphocyte ratio as a prognostic factor in a cohort of European prostate cancer patients. World J Urol. 2015;33:1661–7.

    Article  CAS  PubMed  Google Scholar 

  25. Yamada D, Eguchi H, Asaoka T, Tomihara H, Noda T, Wada H, et al. The basal nutritional state of PDAC patients is the dominant factor for completing adjuvant chemotherapy. Surg Today. 2017;. doi:10.1007/s00595-017-1522-x.

    Google Scholar 

  26. Dan J, Zhang Y, Peng Z, Huang J, Gao H, Xu L, et al. Postoperative neutrophil-to-lymphocyte ratio change predicts survival of patients with small hepatocellular carcinoma undergoing radiofrequency ablation. PLoS One. 2013;8:e58184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Peng W, Li C, Wen TF, Yan LN, Li B, Wang WT, et al. Neutrophil to lymphocyte ratio changes predict small hepatocellular carcinoma survival. J Surg Res. 2014;192:402–8.

    Article  PubMed  Google Scholar 

  28. Tokunaga M, Tanizawa Y, Bando E, Kawamura T, Terashima M. Poor survival rate in patients with postoperative intra-abdominal infectious complications following curative gastrectomy for gastric cancer. Ann Surg Oncol. 2013;20:1575–83.

    Article  PubMed  Google Scholar 

  29. Hayashi T, Yoshikawa T, Aoyama T, Hasegawa S, Yamada T, Tsuchida K, et al. Impact of infectious complications on gastric cancer recurrence. Gastric Cancer. 2015;18:368–74.

    Article  PubMed  Google Scholar 

  30. Takaya S, Saito H, Ikeguchi M. Upregulation of immune checkpoint molecules, PD-1 and LAG-3, on CD4+ and CD8+ T cells after gastric cancer surgery. Yonago Acta Medica. 2015;58:39–44.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Wang KX, Denhardt DT. Osteopontin: role in immune regulation and stress responses. Cytokine Growth Factor Rev. 2008;19:333–45.

    Article  CAS  PubMed  Google Scholar 

  32. Rose-John S, Waetzig GH, Scheller J, Grotzinger J, Seegert D. The IL-6/sIL-6R complex as a novel target for therapeutic approaches. Expert Opin Ther Targets. 2007;11:613–24.

    Article  CAS  PubMed  Google Scholar 

  33. Wu CY, Wu MS, Chiang EP, Wu CC, Chen YJ, Chen CJ, et al. Elevated plasma osteopontin associated with gastric cancer development, invasion and survival. Gut. 2007;56:782–9.

    Article  CAS  PubMed  Google Scholar 

  34. Rittling SR, Chambers AF. Role of osteopontin in tumour progression. Br J Cancer. 2004;90:1877–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Middleton K, Jones J, Lwin Z, Coward JI. Interleukin-6: an angiogenic target in solid tumours. Crit Rev Oncol Hematol. 2014;89:129–39.

    Article  PubMed  Google Scholar 

  36. Rangaswami H, Bulbule A, Kundu GC. Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol. 2006;16:79–87.

    Article  CAS  PubMed  Google Scholar 

  37. Denhardt DT, Noda M, O’Regan AW, Pavlin D, Berman JS. Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J Clin Investig. 2001;107:1055–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Vesely MD, Schreiber RD. Cancer immunoediting: antigens, mechanisms, and implications to cancer immunotherapy. Ann N Y Acad Sci. 2013;1284:1–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Choi Y, Kim JW, Nam KH, Han SH, Kim JW, Ahn SH, et al. Systemic inflammation is associated with the density of immune cells in the tumor microenvironment of gastric cancer. Gastric Cancer. 2017;20:602–11.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Division of Surgical Oncology, Department of Surgery, School of Medicine, Tottori University Faculty of Medicine, 36-1 Nishi-cho, Yonago, 683-8504, Japan

    Kozo Miyatani, Hiroaki Saito, Yusuke Kono, Yuki Murakami, Hirohiko Kuroda, Tomoyuki Matsunaga, Yoji Fukumoto, Tomohiro Osaki, Keigo Ashida & Yoshiyuki Fujiwara

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  1. Kozo Miyatani
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  2. Hiroaki Saito
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  3. Yusuke Kono
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  4. Yuki Murakami
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  5. Hirohiko Kuroda
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  6. Tomoyuki Matsunaga
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  8. Tomohiro Osaki
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  10. Yoshiyuki Fujiwara
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Correspondence to Hiroaki Saito.

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All procedures performed in studies involving human participants were done in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Miyatani, K., Saito, H., Kono, Y. et al. Combined analysis of the pre- and postoperative neutrophil–lymphocyte ratio predicts the outcomes of patients with gastric cancer. Surg Today 48, 300–307 (2018). https://doi.org/10.1007/s00595-017-1587-6

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  • DOI: https://doi.org/10.1007/s00595-017-1587-6

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