Construction and verification of nomogram prediction model for survival prognosis of patients with esophageal squamous cell carcinoma_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

GUO Jiayi ^1,2 , SONG Zhengyu ^1,2 , ZHANG Haiping ^1,2 , ZHANG Liwei ^1,2 ,  EDRIS·Awut ^1,2

1. Department of Thoracic Surgery, The First Affiliated Hospital of Xinjiang Medical University, Urumqi, 830054, P. R. China;
2. State Key Laboratory of Xinjiang Medical University, Urumqi, 830054, P. R. China;

Corresponding author：

EDRIS·Awut, Email: 15999180777@qq.com

Keywords：

Esophageal squamous cell carcinoma; nomogram model; serum albumin-to-globulin ratio; neutrophil-lymphocyte ratio; survival analysis

DOI：

10.7507/1007-4848.202304024

Video：

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Objective To investigate the prognostic value of preoperative serum albumin-to-globulin ratio (AGR) and neutrophil-lymphocyte ratio (NLR) in the overall survival (OS) of patients with esophageal squamous cell carcinoma (ESCC), and to establish an individualized nomogram model and evaluate its efficacy, in order to provide a possible evaluation basis for the clinical treatment and postoperative follow-up of ESCC patients. Methods AGR, NLR, clinicopathological and follow-up data of ESCC patients diagnosed via pathology in the Department of Thoracic Surgery, The First Affiliated Hospital of Xinjiang Medical University from 2010 to 2017 were collected. The correlation between NLR/AGR and clinicopathological data were analyzed. Kaplan-Meier analysis and log-rank test were used for survival analysis. The optimal cut-off values of AGR and NLR were determined by X-tile software, and the patients were accordingly divided into a high-level group and a low-level group. At the same time, univariate and multivariate Cox regression analyses were used to identify independent risk factors affecting OS in the ESCC patients, and a nomogram prediction model was constructed and internally verified. The diagnostic efficacy of the model was evaluated by receiver operating characteristic (ROC) curve and calibration curve, and the clinical application value was evaluated by decision curve analysis. Results A total of 150 patients were included in this study, including 105 males and 45 females with a mean age of 62.3±9.3 years, and the follow-up time was 1-5 years. The 5-year OS rate of patients in the high-level AGR group was significantly higher than that in the low-level group (χ²=6.339, P=0.012), and the median OS of the two groups was 25 months and 12.5 months, respectively. The 5-year OS rate of patients in the high-level NLR group was significantly lower than that in the low-level NLR group (χ²=5.603, P=0.018), and the median OS of the two groups was 18 months and 39 months, respectively. Multivariate Cox analysis showed that AGR, NLR, T stage, lymph node metastasis, N stage, and differentiation were independent risk factors for the OS of ESCC patients. The C-index of the nomogram model was 0.689 [95%CI (0.640, 0.740)] after internal validation. The area under the ROC curve of predicting 1-, 3-, and 5-year OS rate was 0.773, 0.724 and 0.725, respectively. At the same time, the calibration curve and the decision curve suggest that the model had certain efficacy in predicting survival and prognosis. Conclusion Preoperative AGR and NLR are independent risk factors for ESCC patients. High level of AGR and low level of NLR may be associated with longer OS in the patients; the nomogram model based on AGR, NLR and clinicopathological features may be used as a method to predict the survival and prognosis of ESCC patients, which is expected to provide a reference for the development of personalized treatment for patients.

Citation： GUO Jiayi, SONG Zhengyu, ZHANG Haiping, ZHANG Liwei, EDRIS·Awut. Construction and verification of nomogram prediction model for survival prognosis of patients with esophageal squamous cell carcinoma. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2024, 31(5): 718-727. doi: 10.7507/1007-4848.202304024 Copy

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2.	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(3): 209-249.
3.	Jiang H, Teng H, Sun Y, et al. Near-infrared fluorescent image-guided lymphatic mapping in esophageal squamous cell carcinoma. Ann Surg Oncol, 2020, 27(10): 3799-3807.
4.	Tachimori Y. Pattern of lymph node metastases of squamous cell esophageal cancer based on the anatomical lymphatic drainage system: Efficacy of lymph node dissection according to tumor location. J Thorac Dis, 2017, 9(Suppl 8): S724-S730.
5.	Semenkovich TR, Yan Y, Subramanian M, et al. A clinical nomogram for predicting node-positive disease in esophageal cancer. Ann Surg, 2021, 273(6): e214-e221.
6.	Zhang Y, Cao Y, Zhang J, et al. Lymph node ratio improves prediction of overall survival in esophageal cancer patients receiving neoadjuvant chemoradiotherapy: A national cancer database analysis. Ann Surg, 2023, 277(6): e1239-e1246.
7.	Raman V, Jawitz OK, Farrow NE, et al. The relationship between lymph node ratio and survival benefit with adjuvant chemotherapy in node-positive esophageal adenocarcinoma. Ann Surg, 2022, 275(3): e562-e567.
8.	Cruz-Reyes N, Radisky DC. Inflammation, infiltration, and evasion-tumor promotion in the aging breast. Cancers (Basel), 2023, 15(6): 1836.
9.	Jaillon S, Galdiero MR, Del Prete D, et al. Neutrophils in innate and adaptive immunity. Semin Immunopathol, 2013, 35(4): 377-394.
10.	Masucci MT, Minopoli M, Carriero MV. Tumor associated neutrophils. Their role in tumorigenesis, metastasis, prognosis and therapy. Front Oncol, 2019, 9: 1146.
11.	Shen M, Hu P, Donskov F, et al. Tumor-associated neutrophils as a new prognostic factor in cancer: A systematic review and meta-analysis. PLoS One, 2014, 9(6): e98259.
12.	Quigley DA, Kristensen V. Predicting prognosis and therapeutic response from interactions between lymphocytes and tumor cells. Mol Oncol, 2015, 9(10): 2054-2062.
13.	Arango-Prado MDC, Villegas-Valverde CA, Torres-López G, et al. Lymphocyte subsets in defense against new pathogens in patients with cancer. MEDICC Rev, 2022, 24(2): 26-34.
14.	Yang Z, Zheng Y, Wu Z, et al. Association between pre-diagnostic serum albumin and cancer risk: Results from a prospective population-based study. Cancer Med, 2021, 10(12): 4054-4065.
15.	Vavricka SR, Burri E, Beglinger C, et al. Serum protein electrophoresis: An underused but very useful test. Digestion, 2009, 79(4): 203-210.
16.	Han X, Liu S, Yang G, et al. Prognostic value of systemic hemato-immunological indices in uterine cervical cancer: A systemic review, meta-analysis, and meta-regression of observational studies. Gynecol Oncol, 2021, 160(1): 351-360.
17.	Wang Y, Chen L, Zhang B, et al. Pretreatment inflammatory-nutritional biomarkers predict responses to neoadjuvant chemoradiotherapy and survival in locally advanced rectal cancer. Front Oncol, 2021, 11: 639909.
18.	Simonaggio A, Elaidi R, Fournier L, et al. Variation in neutrophil to lymphocyte ratio (NLR) as predictor of outcomes in metastatic renal cell carcinoma (mRCC) and non-small cell lung cancer (mNSCLC) patients treated with nivolumab. Cancer Immunol Immunother, 2020, 69(12): 2513-2522.
19.	Xie HL, Zhang Q, Ruan GT, et al. Evaluation and validation of the prognostic value of serum albumin to globulin ratio in patients with cancer cachexia: Results from a large multicenter collaboration. Front Oncol, 2021, 11: 707705.
20.	Zhang F, Sun P, Wang ZQ, et al. Low preoperative albumin-globulin score predicts favorable survival in esophageal squamous cell carcinoma. Oncotarget, 2016, 7(21): 30550-30560.
21.	Xuan Q, Yang Y, Ji H, et al. Combination of the preoperative albumin to globulin ratio and neutrophil to lymphocyte ratio as a novel prognostic factor in patients with triple negative breast cancer. Cancer Manag Res, 2019, 11: 5125-5131.
22.	Rice TW, Gress DM, Patil DT, et al. Cancer of the esophagus and esophagogastric junction: Major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin, 2017, 67(4): 304-317.
23.	Kelly RJ. Emerging multimodality approaches to treat localized esophageal cancer. J Natl Compr Canc Netw, 2019, 17(8): 1009-1014.
24.	Hayama T, Ozawa T, Tsukamoto M, et al. Predicting overall survival using preoperative nutritional and inflammation status for colorectal cancer. In Vivo, 2022, 36(1): 450-457.
25.	Meyer EJ, Nenke MA, Rankin W, et al. Corticosteroid-binding globulin: A review of basic and clinical advances. Horm Metab Res, 2016, 48(6): 359-371.
26.	Vasson MP, Talvas J, Perche O, et al. Immunonutrition improves functional capacities in head and neck and esophageal cancer patients undergoing radiochemotherapy: A randomized clinical trial. Clin Nutr, 2014, 33(2): 204-210.
27.	Oki S, Toiyama Y, Okugawa Y, et al. Clinical burden of preoperative albumin-globulin ratio in esophageal cancer patients. Am J Surg, 2017, 214(5): 891-898.
28.	Xu K, Yan Y, Cheng C, et al. The relationship between serum albumin and prostate-specific antigen: A analysis of the National Health and Nutrition Examination Survey, 2003-2010. Front Public Health, 2023, 11: 1078280.
29.	Xu SS, Li S, Xu HX, et al. Haemoglobin, albumin, lymphocyte and platelet predicts postoperative survival in pancreatic cancer. World J Gastroenterol, 2020, 26(8): 828-838.
30.	Kim J, Bae JS. Tumor-associated macrophages and neutrophils in tumor microenvironment. Mediators Inflamm, 2016, 2016: 6058147.
31.	Mohme M, Riethdorf S, Pantel K. Circulating and disseminated tumour cells: Mechanisms of immune surveillance and escape. Nat Rev Clin Oncol, 2017, 14(3): 155-167.
32.	Galon J, Costes A, Sanchez-Cabo F, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science, 2006, 313(5795): 1960-1964.
33.	Stenström J, Hedenfalk I, Hagerling C. Regulatory T lymphocyte infiltration in metastatic breast cancer: An independent prognostic factor that changes with tumor progression. Breast Cancer Res, 2021, 23(1): 27.
34.	Atsumi Y, Kawahara S, Kakuta S, et al. Low preoperative albumin-to-globulin ratio is a marker of poor prognosis in patients with esophageal cancer. In Vivo, 2021, 35(6): 3555-3561.
35.	Zhang J, Lin Z, Zhou J, et al. Effects of preoperative albumin-to-globulin ratio on overall survival and quality of life in esophageal cell squamous carcinoma patients: A prospective cohort study. BMC Cancer, 2023, 23(1): 342.
36.	Wang N, Li X, Luo H, et al. Prognostic value of pretreatment inflammatory biomarkers in primary small cell carcinoma of the esophagus. Thorac Cancer, 2019, 10(10): 1913-1918.
37.	Wang C, Tong J, Tang M, et al. Pretreatment neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as prognostic factors and reference markers of treatment options for locally advanced squamous cell carcinoma located in the middle and upper esophagus. Cancer Manag Res, 2021, 13: 1075-1085.

1. Arnold M, Soerjomataram I, Ferlay J, et al. Global incidence of oesophageal cancer by histological subtype in 2012. Gut, 2015, 64(3): 381-387.
2. 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(3): 209-249.
3. Jiang H, Teng H, Sun Y, et al. Near-infrared fluorescent image-guided lymphatic mapping in esophageal squamous cell carcinoma. Ann Surg Oncol, 2020, 27(10): 3799-3807.
4. Tachimori Y. Pattern of lymph node metastases of squamous cell esophageal cancer based on the anatomical lymphatic drainage system: Efficacy of lymph node dissection according to tumor location. J Thorac Dis, 2017, 9(Suppl 8): S724-S730.
5. Semenkovich TR, Yan Y, Subramanian M, et al. A clinical nomogram for predicting node-positive disease in esophageal cancer. Ann Surg, 2021, 273(6): e214-e221.
6. Zhang Y, Cao Y, Zhang J, et al. Lymph node ratio improves prediction of overall survival in esophageal cancer patients receiving neoadjuvant chemoradiotherapy: A national cancer database analysis. Ann Surg, 2023, 277(6): e1239-e1246.
7. Raman V, Jawitz OK, Farrow NE, et al. The relationship between lymph node ratio and survival benefit with adjuvant chemotherapy in node-positive esophageal adenocarcinoma. Ann Surg, 2022, 275(3): e562-e567.
8. Cruz-Reyes N, Radisky DC. Inflammation, infiltration, and evasion-tumor promotion in the aging breast. Cancers (Basel), 2023, 15(6): 1836.
9. Jaillon S, Galdiero MR, Del Prete D, et al. Neutrophils in innate and adaptive immunity. Semin Immunopathol, 2013, 35(4): 377-394.
10. Masucci MT, Minopoli M, Carriero MV. Tumor associated neutrophils. Their role in tumorigenesis, metastasis, prognosis and therapy. Front Oncol, 2019, 9: 1146.
11. Shen M, Hu P, Donskov F, et al. Tumor-associated neutrophils as a new prognostic factor in cancer: A systematic review and meta-analysis. PLoS One, 2014, 9(6): e98259.
12. Quigley DA, Kristensen V. Predicting prognosis and therapeutic response from interactions between lymphocytes and tumor cells. Mol Oncol, 2015, 9(10): 2054-2062.
13. Arango-Prado MDC, Villegas-Valverde CA, Torres-López G, et al. Lymphocyte subsets in defense against new pathogens in patients with cancer. MEDICC Rev, 2022, 24(2): 26-34.
14. Yang Z, Zheng Y, Wu Z, et al. Association between pre-diagnostic serum albumin and cancer risk: Results from a prospective population-based study. Cancer Med, 2021, 10(12): 4054-4065.
15. Vavricka SR, Burri E, Beglinger C, et al. Serum protein electrophoresis: An underused but very useful test. Digestion, 2009, 79(4): 203-210.
16. Han X, Liu S, Yang G, et al. Prognostic value of systemic hemato-immunological indices in uterine cervical cancer: A systemic review, meta-analysis, and meta-regression of observational studies. Gynecol Oncol, 2021, 160(1): 351-360.
17. Wang Y, Chen L, Zhang B, et al. Pretreatment inflammatory-nutritional biomarkers predict responses to neoadjuvant chemoradiotherapy and survival in locally advanced rectal cancer. Front Oncol, 2021, 11: 639909.
18. Simonaggio A, Elaidi R, Fournier L, et al. Variation in neutrophil to lymphocyte ratio (NLR) as predictor of outcomes in metastatic renal cell carcinoma (mRCC) and non-small cell lung cancer (mNSCLC) patients treated with nivolumab. Cancer Immunol Immunother, 2020, 69(12): 2513-2522.
19. Xie HL, Zhang Q, Ruan GT, et al. Evaluation and validation of the prognostic value of serum albumin to globulin ratio in patients with cancer cachexia: Results from a large multicenter collaboration. Front Oncol, 2021, 11: 707705.
20. Zhang F, Sun P, Wang ZQ, et al. Low preoperative albumin-globulin score predicts favorable survival in esophageal squamous cell carcinoma. Oncotarget, 2016, 7(21): 30550-30560.
21. Xuan Q, Yang Y, Ji H, et al. Combination of the preoperative albumin to globulin ratio and neutrophil to lymphocyte ratio as a novel prognostic factor in patients with triple negative breast cancer. Cancer Manag Res, 2019, 11: 5125-5131.
22. Rice TW, Gress DM, Patil DT, et al. Cancer of the esophagus and esophagogastric junction: Major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin, 2017, 67(4): 304-317.
23. Kelly RJ. Emerging multimodality approaches to treat localized esophageal cancer. J Natl Compr Canc Netw, 2019, 17(8): 1009-1014.
24. Hayama T, Ozawa T, Tsukamoto M, et al. Predicting overall survival using preoperative nutritional and inflammation status for colorectal cancer. In Vivo, 2022, 36(1): 450-457.
25. Meyer EJ, Nenke MA, Rankin W, et al. Corticosteroid-binding globulin: A review of basic and clinical advances. Horm Metab Res, 2016, 48(6): 359-371.
26. Vasson MP, Talvas J, Perche O, et al. Immunonutrition improves functional capacities in head and neck and esophageal cancer patients undergoing radiochemotherapy: A randomized clinical trial. Clin Nutr, 2014, 33(2): 204-210.
27. Oki S, Toiyama Y, Okugawa Y, et al. Clinical burden of preoperative albumin-globulin ratio in esophageal cancer patients. Am J Surg, 2017, 214(5): 891-898.
28. Xu K, Yan Y, Cheng C, et al. The relationship between serum albumin and prostate-specific antigen: A analysis of the National Health and Nutrition Examination Survey, 2003-2010. Front Public Health, 2023, 11: 1078280.
29. Xu SS, Li S, Xu HX, et al. Haemoglobin, albumin, lymphocyte and platelet predicts postoperative survival in pancreatic cancer. World J Gastroenterol, 2020, 26(8): 828-838.
30. Kim J, Bae JS. Tumor-associated macrophages and neutrophils in tumor microenvironment. Mediators Inflamm, 2016, 2016: 6058147.
31. Mohme M, Riethdorf S, Pantel K. Circulating and disseminated tumour cells: Mechanisms of immune surveillance and escape. Nat Rev Clin Oncol, 2017, 14(3): 155-167.
32. Galon J, Costes A, Sanchez-Cabo F, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science, 2006, 313(5795): 1960-1964.
33. Stenström J, Hedenfalk I, Hagerling C. Regulatory T lymphocyte infiltration in metastatic breast cancer: An independent prognostic factor that changes with tumor progression. Breast Cancer Res, 2021, 23(1): 27.
34. Atsumi Y, Kawahara S, Kakuta S, et al. Low preoperative albumin-to-globulin ratio is a marker of poor prognosis in patients with esophageal cancer. In Vivo, 2021, 35(6): 3555-3561.
35. Zhang J, Lin Z, Zhou J, et al. Effects of preoperative albumin-to-globulin ratio on overall survival and quality of life in esophageal cell squamous carcinoma patients: A prospective cohort study. BMC Cancer, 2023, 23(1): 342.
36. Wang N, Li X, Luo H, et al. Prognostic value of pretreatment inflammatory biomarkers in primary small cell carcinoma of the esophagus. Thorac Cancer, 2019, 10(10): 1913-1918.
37. Wang C, Tong J, Tang M, et al. Pretreatment neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as prognostic factors and reference markers of treatment options for locally advanced squamous cell carcinoma located in the middle and upper esophagus. Cancer Manag Res, 2021, 13: 1075-1085.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Construction and verification of nomogram prediction model for survival prognosis of patients with esophageal squamous cell carcinoma

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