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Score of the preoperative absolute number of lymphocytes, monocytes, and neutrophils as a prognostic indicator for patients with gastric cancer

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Abstract

Purpose

The association between the preoperative absolute neutrophil count (NC), lymphocyte count (LC), and monocyte count (MC) in the peripheral blood and the prognosis of gastric cancer (GC) patients has not been investigated widely.

Methods

We enrolled 445 patients who underwent surgery for GC between January, 2005 and April, 2013 to analyze the correlations among NC, LC, and MC and their prognoses.

Results

Based on cut-off values calculated by ROC analysis, patients were sub grouped as having: NC ≥ 4477 (NCHigh), NC < 4477 (NCLow); and as LC ≥ 1447 (LCHigh), LC < 1447 (LCLow); and as MC ≥ 658.5 (MCHigh), MC < 658.5 (MCLow). Each group was assigned as follows; NCHigh group = 1, NCLow group = 0, LCHigh group = 0, LCLow group = 1, MCHigh group = 1, MCLow group = 0, and the sum of each score was defined as the lymphocyte–monocyte–neutrophil score (LMN score). The overall 5-year survival rates were 89%, 74%, 57.8%, and 53.3% for LMN scores of 0, 1, 2, and 3, respectively (P = 0.0004). Multivariate analysis indicated that the LMN score was an independent prognostic indicator.

Conclusions

The combination of preoperative NC, LC, and MC appears to be a useful indicator of GC prognosis.

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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. 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 

  3. 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 

  4. Saito H, Kono Y, Murakami Y, Shishido Y, Kuroda H, Matsunaga T, et al. Postoperative serum albumin is a potential prognostic factor for older patients with gastric cancer. Yonago Acta Med. 2018;61:72–8.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Saito H, Kono Y, Murakami Y, Shishido Y, Kuroda H, Yamamoto M, et al. Prognostic significance of pre- and postoperative lymphocyte counts in patients with gastric cancer. Digestive Surg. 2019;36:137–43.

    Article  Google Scholar 

  6. Saito H, Kono Y, Murakami Y, Shishido Y, Kuroda H, Matsunaga T, et al. Prognostic significance of platelet-based inflammatory indicators in patients with gastric cancer. World J Surg. 2018;42:2542–50.

    Article  PubMed  Google Scholar 

  7. Kono Y, Saito H, Murakami Y, Shishido Y, Kuroda H, Matsunaga T, et al. Postoperative ratio of the maximum C-reactive protein level to the minimum peripheral lymphocyte count as a prognostic indicator for gastric cancer patients. Surg Today 2018.

  8. Miyatani K, Saito H, Kono Y, Murakami Y, Kuroda H, Matsunaga T, et al. Combined analysis of the pre- and postoperative neutrophil–lymphocyte ratio predicts the outcomes of patients with gastric cancer. Surg Today. 2018;48:300–7.

    Article  PubMed  Google Scholar 

  9. Murakami Y, Saito H, Kono Y, Shishido Y, Kuroda H, Matsunaga T, et al. Combined analysis of the preoperative and postoperative prognostic nutritional index offers a precise predictor of the prognosis of patients with gastric cancer. Surg Today. 2018;48:395–403.

    Article  PubMed  Google Scholar 

  10. Saito H, Kono Y, Murakami Y, Shishido Y, Kuroda H, Matsunaga T, et al. Prognostic significance of the preoperative ratio of C-reactive protein to albumin and neutrophil–lymphocyte ratio in gastric cancer patients. World J Surg. 2018;42:1819–25.

    Article  PubMed  Google Scholar 

  11. Clark EJ, Connor S, Taylor MA, Madhavan KK, Garden OJ, Parks RW. Preoperative lymphocyte count as a prognostic factor in resected pancreatic ductal adenocarcinoma. HPB (Oxford). 2007;9:456–60.

    Article  CAS  Google Scholar 

  12. Feng JF, Liu JS, Huang Y. Lymphopenia predicts poor prognosis in patients with esophageal squamous cell carcinoma. Med (Baltimore). 2014;93:e257.

    Article  Google Scholar 

  13. Saroha S, Uzzo RG, Plimack ER, Ruth K, Al-Saleem T. Lymphopenia is an independent predictor of inferior outcome in clear cell renal carcinoma. J Urol. 2013;189:454–61.

    Article  PubMed  Google Scholar 

  14. Borregaard N. Neutrophils, from marrow to microbes. Immunity. 2010;33:657–70.

    Article  CAS  PubMed  Google Scholar 

  15. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303:1532–5.

    Article  CAS  PubMed  Google Scholar 

  16. Teramukai S, Kitano T, Kishida Y, Kawahara M, Kubota K, Komuta K, et al. Pretreatment neutrophil count as an independent prognostic factor in advanced non-small-cell lung cancer: an analysis of Japan Multinational Trial Organisation LC00-03. Eur J Cancer. 2009;45:1950–8.

    Article  PubMed  Google Scholar 

  17. Lee YY, Choi CH, Kim HJ, Kim TJ, Lee JW, Lee JH, et al. Pretreatment neutrophil:lymphocyte ratio as a prognostic factor in cervical carcinoma. Anticancer Res. 2012;32:1555–611.

    PubMed  Google Scholar 

  18. Sadeghi N, Badalato GM, Hruby G, Grann V, McKiernan JM. Does absolute neutrophil count predict high tumor grade in African-American men with prostate cancer? Prostate. 2012;72:386–91.

    Article  PubMed  Google Scholar 

  19. Gondo T, Nakashima J, Ohno Y, Choichiro O, Horiguchi Y, Namiki K, et al. Prognostic value of neutrophil-to-lymphocyte ratio and establishment of novel preoperative risk stratification model in bladder cancer patients treated with radical cystectomy. Urology. 2012;79:1085–91.

    Article  PubMed  Google Scholar 

  20. Jiang Y, Xu H, Jiang H, Ding S, Zheng T. Pretreatment neutrophil–lymphocyte count ratio may associate with gastric cancer presence. Cancer Biomark. 2016;16:523–8.

    Article  CAS  PubMed  Google Scholar 

  21. Chen Z, Chen W, Wang J, Zhu M, Zhuang Z. Pretreated baseline neutrophil count and chemotherapy-induced neutropenia may be conveniently available as prognostic biomarkers in advanced gastric cancer. Intern Med J. 2015;45:854–9.

    Article  CAS  PubMed  Google Scholar 

  22. Kaynar M, Yildirim ME, Badem H, Cavis M, Tekinarslan E, Istanbulluoglu MO, et al. Bladder cancer invasion predictability based on preoperative neutrophil–lymphocyte ratio. Tumour Biol. 2014;35:6601–5.

    Article  PubMed  Google Scholar 

  23. Watt DG, Martin JC, Park JH, Horgan PG, McMillan DC. Neutrophil count is the most important prognostic component of the differential white cell count in patients undergoing elective surgery for colorectal cancer. Am J Surg. 2015;210:24–30.

    Article  PubMed  Google Scholar 

  24. Mantovani A, Schioppa T, Porta C, Allavena P, Sica A. Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev. 2006;25:315–22.

    Article  PubMed  Google Scholar 

  25. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420:860–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Tang X. Tumor-associated macrophages as potential diagnostic and prognostic biomarkers in breast cancer. Cancer Lett. 2013;332:3–10.

    Article  CAS  PubMed  Google Scholar 

  27. Shigeoka M, Urakawa N, Nakamura T, Nishio M, Watajima T, Kuroda D, et al. Tumor associated macrophage expressing CD204 is associated with tumor aggressiveness of esophageal squamous cell carcinoma. Cancer Sci. 2013;104:1112–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zhou K, Yan Y, Zhao S, Li B. Clinical application and prognostic assessment of serum tumor associated material (TAM) from esophageal cancer patients. Eur Rev Med Pharmacol Sci. 2014;18:3870–6.

    CAS  PubMed  Google Scholar 

  29. Japanese classification of gastric carcinoma: 3rd English edition. Gastric cancer : official journal of the International Gastric Cancer Association and the Japanese Gastric Cancer Association 2011;14:101–12.

  30. Ray-Coquard I, Cropet C, Van Glabbeke M, Sebban C, Le Cesne A, Judson I, et al. Lymphopenia as a prognostic factor for overall survival in advanced carcinomas, sarcomas, and lymphomas. Cancer Res. 2009;69:5383–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Gooden MJ, de Bock GH, Leffers N, Daemen T, Nijman HW. The prognostic influence of tumour-infiltrating lymphocytes in cancer: a systematic review with meta-analysis. Br J Cancer. 2011;105:93–103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006;313:1960–4.

    Article  CAS  PubMed  Google Scholar 

  33. Tang Y, Xu X, Guo S, Zhang C, Tang Y, Tian Y, et al. An increased abundance of tumor-infiltrating regulatory T cells is correlated with the progression and prognosis of pancreatic ductal adenocarcinoma. PLoS One. 2014;9:e91551.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Qiu H, Xiao-Jun W, Zhi-Wei Z, Gong C, Guo-Qiang W, Li-Yi Z, et al. The prognostic significance of peripheral T-lymphocyte subsets and natural killer cells in patients with colorectal cancer. Hepatogastroenterology. 2009;56:1310–5.

    PubMed  Google Scholar 

  35. Tachibana T, Onodera H, Tsuruyama T, Mori A, Nagayama S, Hiai H, et al. Increased intratumor Valpha24-positive natural killer T cells: a prognostic factor for primary colorectal carcinomas. Clin Cancer Res. 2005;11:7322–7.

    Article  CAS  PubMed  Google Scholar 

  36. Berntsson J, Nodin B, Eberhard J, Micke P, Jirstrom K. Prognostic impact of tumour-infiltrating B cells and plasma cells in colorectal cancer. Int J Cancer. 2016;139:1129–39.

    Article  CAS  PubMed  Google Scholar 

  37. Yoshikawa T, Saito H, Osaki T, Matsumoto S, Tsujitani S, Ikeguchi M. Elevated Fas expression is related to increased apoptosis of circulating CD8+ T cell in patients with gastric cancer. J Surg Res. 2008;148:143–51.

    Article  CAS  PubMed  Google Scholar 

  38. Sionov RV, Fridlender ZG, Granot Z. The multifaceted roles neutrophils play in the tumor microenvironment. Cancer Microenviron. 2015;8:125–58.

    Article  CAS  PubMed  Google Scholar 

  39. Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: "N1" versus "N2" TAN. Cancer Cell. 2009;16:183–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Sun R, Luo J, Li D, Shu Y, Luo C, Wang SS, et al. Neutrophils with protumor potential could efficiently suppress tumor growth after cytokine priming and in presence of normal NK cells. Oncotarget. 2014;5:12621–344.

    PubMed  PubMed Central  Google Scholar 

  41. Ikeguchi M, Hatada T, Yamamoto M, Miyake T, Matsunaga T, Fukumoto Y, et al. Serum interleukin-6 and -10 levels in patients with gastric cancer. Gastric Cancer. 2009;12:95–100.

    Article  CAS  PubMed  Google Scholar 

  42. Gordon SR, Maute RL, Dulken BW, Hutter G, George BM, McCracken MN, et al. PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature. 2017;545:495–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Matsunaga T, Saito H, Ikeguchi M. Increased B7–H1 and B7–H4 expressions on circulating monocytes and tumor-associated macrophages are involved in immune evasion in patients with gastric cancer. Yonago Acta Med. 2011;54:1–10.

    PubMed  PubMed Central  Google Scholar 

  44. 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 Obst. 1986;162:229–34.

    CAS  Google Scholar 

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

    Article  Google Scholar 

  46. Shimada H, Noie T, Ohashi M, Oba K, Takahashi Y. Clinical significance of serum tumor markers for gastric cancer: a systematic review of literature by the Task Force of the Japanese Gastric Cancer Association. Gastric Cancer. 2014;17:26–33.

    Article  CAS  PubMed  Google Scholar 

  47. Lin JX, Wang W, Lin JP, Xie JW, Wang JB, Lu J, et al. Preoperative tumor markers independently predict survival in stage III gastric cancer patients: should we include tumor markers in AJCC staging? Ann Surg Oncol. 2018;25:2703–12.

    Article  PubMed  Google Scholar 

  48. Uda H, Kanda M, Tanaka C, Kobayashi D, Inaoka K, Tanaka Y, et al. Perioperative serum carcinoembryonic antigen levels predict recurrence and survival of patients with pathological T2–4 gastric cancer treated with curative gastrectomy. Digestive Surg. 2018;35:55–63.

    Article  CAS  Google Scholar 

  49. Fujiya K, Tokunaga M, Makuuchi R, Nishiwaki N, Omori H, Takagi W, et al. Early detection of nonperitoneal recurrence may contribute to survival benefit after curative gastrectomy for gastric cancer. Gastric Cancer. 2017;20:141–9.

    Article  PubMed  Google Scholar 

  50. Park CH, Park JC, Chung H, Shin SK, Lee SK, Cheong JH, et al. Impact of the surveillance interval on the survival of patients who undergo curative surgery for gastric cancer. Ann Surg Oncol. 2016;23:539–45.

    Article  PubMed  Google Scholar 

  51. Saito T, Nishikawa H, Wada H, Nagano Y, Sugiyama D, Atarashi K, et al. Two FOXP3(+)CD4(+) T cell subpopulations distinctly control the prognosis of colorectal cancers. Nat Med. 2016;22:679–84.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

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

    Hiroaki Saito, Shota Shimizu, Yusuke Kono, Yuki Murakami, Yuji Shishido, Kozo Miyatani, Tomoyuki Matsunaga, Yoji Fukumoto, Keigo Ashida & Yoshiyuki Fujiwara

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  1. Hiroaki Saito
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  2. Shota Shimizu
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  3. Yusuke Kono
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Correspondence to Hiroaki Saito.

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Saito, H., Shimizu, S., Kono, Y. et al. Score of the preoperative absolute number of lymphocytes, monocytes, and neutrophils as a prognostic indicator for patients with gastric cancer. Surg Today 49, 850–858 (2019). https://doi.org/10.1007/s00595-019-01817-6

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