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Albumin and Derived Neutrophil-to-Lymphocyte Ratio is a Novel Prognostic Factor for Patients with Esophageal Squamous Cell Carcinoma

  • Thoracic Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Multidisciplinary treatment combining neoadjuvant treatment (NAT) and surgery has slightly improved the prognosis of patients with esophageal squamous cell carcinoma (ESCC). Although various biomarkers targeting nutrition and inflammation are associated with cancer prognosis, most studies have focused on conditions prior to NAT. Developing real-time and sensitive biomarkers that monitor changes in systemic conditions during NAT is important. We established a novel nutritional and inflammatory index, represented as the albumin to derived neutrophil-to-lymphocyte ratio (Alb-dNLR), and calculated the change in Alb-dNLR (ΔAlb-dNLR) during neoadjuvant chemotherapy (nCT). In this study, we aimed to evaluate whether ΔAlb-dNLR is associated with prognosis in patients with ESCC.

Methods

We investigated 172 patients who underwent nCT before esophagectomy between April 2010 and March 2018. The dNLR was calculated as the ratio of neutrophil count to (white blood cell count – neutrophil count), Alb-dNLR was calculated by dividing the serum albumin level by the dNLR, and ΔAlb-dNLR was evaluated by dividing the post-Alb-dNLR by the pre-Alb-dNLR. Patients were divided into ‘high’ and ‘low’ groups according to the ΔAlb-dNLR.

Results

Thirty-nine patients (22.7%) had a low ΔAlb-dNLR (≤ 0.8), and the 5-year overall survival (OS) rates in patients with low and high ΔAlb-dNLR were 38.1% and 53.6%, respectively (p = 0.0072). Multivariate analyses demonstrated that estimated blood loss (p = 0.044), pathological T stage (p = 0.0005), pathological N stage (p = 0.017), and ΔAlb-dNLR (p = 0.005) were independent prognostic factors for OS.

Conclusions

ΔAlb-dNLR is a useful prognostic factor for OS in patients with ESCC receiving nCT.

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References

  1. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–49.

    Article  Google Scholar 

  2. 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.

    Article  Google Scholar 

  3. Jin F, Han A, Shi F, Kong L, Yu J. The postoperative neutrophil-to-lymphocyte ratio and changes in this ratio predict survival after the complete resection of stage I non-small cell lung cancer. Onco Targets Ther. 2016;9:6529–37.

    Article  CAS  Google Scholar 

  4. Peng W, Li C, Zhu WJ, et al. Prognostic value of the platelet to lymphocyte ratio change in liver cancer. J Surg Res. 2015;194:464–70.

    Article  Google Scholar 

  5. Oshima M, Okano K, Suto H, et al. Changes and prognostic impact of inflammatory nutritional factors during neoadjuvant chemoradiotherapy for patients with resectable and borderline resectable pancreatic cancer. BMC Gastroenterol. 2020;20:423.

    Article  CAS  Google Scholar 

  6. Fukuoka T, Maeda K, Nagahara H, et al. Change in PMI during neoadjuvant therapy is a predictive prognostic marker in rectal cancer. Anticancer Res. 2019;39:5157–63.

    Article  CAS  Google Scholar 

  7. Kim KH, Hwang HK, Kang IC, Lee WJ, Kang CM. Oncologic impact of preoperative prognostic nutritional index change in resected pancreatic cancer following neoadjuvant chemotherapy. Pancreatology. 2020;20:247–53.

    Article  Google Scholar 

  8. Otowa Y, Nakamura T, Takiguchi G, et al. Changes in modified Glasgow prognostic score after neoadjuvant chemotherapy is a prognostic factor in clinical stage II/III esophageal cancer. Dis Esophagus. 2016;29:146–51.

    Article  Google Scholar 

  9. Abe T, Oshikiri T, Goto H, et al. Albumin-derived NLR score is a novel prognostic marker for esophageal squamous cell carcinoma. Ann Surg Oncol. 2022;29:2663–71. https://doi.org/10.1245/s10434-021-11012-y.

    Article  PubMed  Google Scholar 

  10. Brierley J, Gospodarowicz MK, Wittekind C, Sauvage M, Union internationale contre le c (UICC). TNM Classification of Malignant Tumours. UICC; 2017.

    Google Scholar 

  11. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.

    Article  Google Scholar 

  12. Proctor MJ, McMillan DC, Morrison DS, Fletcher CD, Horgan PG, Clarke SJ. A derived neutrophil to lymphocyte ratio predicts survival in patients with cancer. Br J Cancer. 2012;107:695–9.

    Article  CAS  Google Scholar 

  13. Hajian-Tilaki K. Receiver operating characteristic (ROC) curve analysis for medical diagnostic test evaluation. Caspian J Intern Med. 2013;4:627–35.

    PubMed  PubMed Central  Google Scholar 

  14. Park SH, Goo JM, Jo CH. Receiver operating characteristic (ROC) curve: practical review for radiologists. Korean J Radiol. 2004;5:11–8.

    Article  Google Scholar 

  15. Kato T, Oshikiri T, Urakawa N, et al. Preoperative neutrophil-to-lymphocyte ratio predicts the prognosis of esophageal squamous cell cancer patients undergoing minimally invasive esophagectomy after neoadjuvant chemotherapy. J Surg Oncol. 2021;124:1022–30.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Chandrasinghe PC, Ediriweera DS, Kumarage SK, Deen KI. Pre-operative hypoalbuminaemia predicts poor overall survival in rectal cancer: a retrospective cohort analysis. BMC Clin Pathol. 2013;13:12–12.

    Article  CAS  Google Scholar 

  18. Crumley ABC, Stuart RC, McKernan M, McMillan DC. Is hypoalbuminemia an independent prognostic factor in patients with gastric cancer? World J Surg. 2010;34:2393–8.

    Article  Google Scholar 

  19. Gupta D, Lis CG. Pretreatment serum albumin as a predictor of cancer survival: a systematic review of the epidemiological literature. Nutr J. 2010;9:69.

    Article  Google Scholar 

  20. Wang Y, Chen L, Wu Y, Li P, Che G. The prognostic value of modified Glasgow prognostic score in patients with esophageal squamous cell cancer: a meta-analysis. Nutr Cancer. 2020;72(7):1146–54.

    Article  CAS  Google Scholar 

  21. Sakai M, Sohda M, Saito H, et al. Comparative analysis of immunoinflammatory and nutritional measures in surgically resected esophageal cancer: a single-center retrospective study. In Vivo. 2020;34(2):881–7.

    Article  CAS  Google Scholar 

  22. Matsuda S, Takeuchi H, Kawakubo H, et al. Validation study of fibrinogen and albumin score in esophageal cancer patients who underwent esophagectomy: multicenter prospective cohort study. Ann Surg Oncol. 2021;28(2):774–84.

    Article  Google Scholar 

  23. Nakamura M, Iwahashi M, Nakamori M, et al. A new prognostic score for the survival of patients with esophageal squamous cell carcinoma. Surg Today. 2014;44(5):875–83.

    Article  CAS  Google Scholar 

  24. Dan J, Tan J, Huang J, et al. The dynamic change of neutrophil to lymphocyte ratio is predictive of pathological complete response after neoadjuvant chemotherapy in breast cancer patients. Breast Cancer. 2020;27(5):982–8.

    Article  Google Scholar 

  25. Matsuda S, Takeuchi H, Kawakubo H, et al. Prognostic impact of change in the fibrinogen and albumin score during preoperative treatment in esophageal cancer patients. World J Surg. 2017;41(11):2788–95.

    Article  Google Scholar 

  26. Kelly RJ, Ajani JA, Kuzdzal J, et al. Adjuvant nivolumab in resected esophageal or gastroesophageal junction cancer. N Engl J Med. 2021;384:1191–203.

    Article  CAS  Google Scholar 

  27. Kassis ES, Kosinski AS, Ross P Jr, Koppes KE, Donahue JM, Daniel VC. Predictors of anastomotic leak after esophagectomy: an analysis of the society of thoracic surgeons general thoracic database. Ann Thorac Surg. 2013;96:1919–26.

    Article  Google Scholar 

  28. Fransen LFC, Berkelmans GHK, Asti E, et al. The effect of postoperative complications after minimally invasive esophagectomy on long-term survival: an international multicenter cohort study. Ann Surg. 2021;274:e1129–37.

    Article  Google Scholar 

  29. Aoyama T, Atsumi Y, Hara K, et al. Risk factors for postoperative anastomosis leak after esophagectomy for esophageal cancer. In Vivo. 2020;34:857–62.

    Article  Google Scholar 

  30. Herzberg J, Strate T, Guraya SY, Honarpisheh H. Risk factors for anastomotic leakage after surgical resections for esophageal cancer. Langenbecks Arch Surg. 2021;406:1859–66.

    Article  Google Scholar 

  31. Sun ZW, Du H, Li JR, Qin HY. Constructing a risk prediction model for anastomotic leakage after esophageal cancer resection. J Int Med Res. 2020;48:300060519896726.

    CAS  PubMed  Google Scholar 

  32. Huang C, Yao H, Huang Q, Lu H, Xu M, Wu J. A novel nomogram to predict the risk of anastomotic leakage in patients after oesophagectomy. BMC Surg. 2020;20:64.

    Article  Google Scholar 

  33. Giger U, Büchler M, Farhadi J, et al. Preoperative immunonutrition suppresses perioperative inflammatory response in patients with major abdominal surgery: a randomized controlled pilot study. Ann Surg Oncol. 2007;14(10):2798–806.

    Article  Google Scholar 

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Authors and Affiliations

  1. Division of Gastrointestinal Surgery, Department of Surgery, Graduate School of Medicine, Kobe University, Kobe, Hyogo, Japan

    Tomoki Abe MD, Taro Oshikiri MD, Hironobu Goto MD, Takashi Kato MD, Manabu Horikawa MD, Ryuichiro Sawada MD, Hitoshi Harada MD, Naoki Urakawa MD, Hiroshi Hasegawa MD, Shingo Kanaji MD, Kimihiro Yamashita MD, Tetsu Nakamura MD & Yoshihiro Kakeji MD

  2. Division of Minimally Invasive Surgery, Department of Surgery, Graduate School of Medicine, Kobe University, Kobe, Hyogo, Japan

    Takeru Matsuda MD

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  1. Tomoki Abe MD
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Correspondence to Taro Oshikiri MD.

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Tomoki Abe, Taro Oshikiri, Hironobu Goto, Takashi Kato, Manabu Horikawa, Ryuichiro Sawada, Hitoshi Harada, Naoki Urakawa, Hiroshi Hasegawa, Shingo Kanaji, Kimihiro Yamashita, Takeru Matsuda, and Yoshihiro Kakeji have no conflicts of interest or financial ties to disclose.

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Abe, T., Oshikiri, T., Goto, H. et al. Albumin and Derived Neutrophil-to-Lymphocyte Ratio is a Novel Prognostic Factor for Patients with Esophageal Squamous Cell Carcinoma. Ann Surg Oncol 29, 6860–6866 (2022). https://doi.org/10.1245/s10434-022-11868-8

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