Association between albumin to fibrinogen ratio or prognostic nutrition index and recurrence of venous thromboembolism_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LI Ling ^1,2 , HUANG Jing ^1,2 , XU Jing ^1,2 , MA Yukui ¹ ,  WU Zhoupeng ¹

1. Division of Vascular Surgery, Department of General Surgery, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;
2. West China School of Nursing, Sichuan University, Chengdu 610041, P. R. China;

Corresponding?author：

WU Zhoupeng, Email: lzwzp19@163.com

Keywords：

venous thromboembolism; anticoagulation therapy; prognostic nutritional index; albumin-to-fibrinogen ratio; recurrence

DOI：

10.7507/1007-9424.202412031

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Objective To investigate association between the nutrition-related indicators and the recurrence of venous thromboembolism (VTE). Methods The clinical data from the patients with VTE receiving 3 or 6 months of anticoagulation therapy at the West China Hospital of Sichuan University, from January 2020 to October 2022, were retrospective analyzed. The multivariate logistic regression analysis was used to assess the association between the nutrition-related indicators such as albumin to fibrinogen ratio (AFR) and prognostic nutrition index (PNI) and VTE recurrence. The test level was set as α=0.05. Results A total of 141 patients with VTE were enrolled, of whom 12 (8.5%) experienced recurrence within 2 years. The multivariate logistic regression analysis identified several risk factors for recurrence, including diabetes [β=–3.368, OR (95%CI)=0.034 (0.001, 0.920), P=0.044], pulmonary embolism [β=–0.454, OR (95%CI)=0.635 (0.423, 0.954), P=0.029], and decreased AFR [β=–0.454, OR (95%CI)=0.635 (0.423, 0.954), P=0.029], but it was not found that the PNI was associated with VTE recurrence [β=–0.153, OR (95%CI)=0.858 (0.722, 1.020), P=0.083]. Conclusion The findings of this study indicate that close monitoring for recurrent VTE is warranted in patients with diabetes mellitus, pulmonary embolism, and decreased AFR receiving anticoagulation therapy.

Citation： LI Ling, HUANG Jing, XU Jing, MA Yukui, WU Zhoupeng. Association between albumin to fibrinogen ratio or prognostic nutrition index and recurrence of venous thromboembolism. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2025, 32(6): 775-778. doi: 10.7507/1007-9424.202412031 Copy

1.	Naess IA, Christiansen SC, Romundstad P, et al. Incidence and mortality of venous thrombosis: a population-based study. J Thromb Haemost, 2007, 5(4): 692-699.
2.	孫曉萱. 老年靜脈血栓栓塞患者復發風險預測及動態列線圖. 南昌: 南昌大學醫學部, 2024.
3.	Guan X, Gong M, Wang X, et al. Low preoperative fibrinogen level is risk factor for neurological complications in acute aortic dissection. Medicine (Baltimore), 2018, 97(21): e10830. doi: 10.1097/MD.0000000000010830.
4.	Ying J, Zhou D, Gu T, et al. Pretreatment albumin/fibrinogen ratio as a promising predictor for the survival of advanced non small-cell lung cancer patients undergoing first-line platinum-based chemotherapy. BMC Cancer, 2019, 19(1): 288. doi: 10.1186/s12885-019-5490-y.
5.	吳靜, 楊紅梅, 劉旭輝. 預后營養指數對急性心肌梗死患者介入術后發生急性損傷的預測價值分析. 心肺血管病雜志, 2024, 43(8): 812-817.
6.	王蔚文. 臨床疾病診斷與療效判定標準. 北京: 科學技術文獻出版社, 2010.
7.	Onodera T, Goseki N, Kosaki G. Prognostic nutritional index in gastrointestinal surgery of malnourished cancer patients. Nihon Geka Gakkai Zasshi, 1984, 85(9): 1001-1005.
8.	Eichinger S, Minar E, Bialonczyk C, et al. D-dimer levels and risk of recurrent venous thromboembolism. JAMA, 2003, 290(8): 1071-1074.
9.	Spencer FA, Gurwitz JH, Schulman S, et al. Venous thromboembolism in older adults: A community-based study. Am J Med, 2014, 127(6): 530-537.
10.	de Moreuil C, Le Mao R, Le Moigne E, et al. Long-term recurrence risk after a first venous thromboembolism in men and women under 50 years old: A French prospective cohort. Eur J Intern Med, 2021, 84: 24-31.
11.	Roach RE, Lijfering WM, Tait RC, et al. Sex difference in the risk of recurrent venous thrombosis: A detailed analysis in four European cohorts. J Thromb Haemost, 2015, 13(10): 1815-1822.
12.	Kyrle PA, Kammer M, Eischer L, et al. The long-term recurrence risk of patients with unprovoked venous thromboembolism: an observational cohort study. J Thromb Haemost, 2016, 14(12): 2402-2409.
13.	Burns KEA, Heels-Ansdell D, Thabane L, et al. Sex differences in thromboprophylaxis of the critically ill: A secondary analysis of a randomized trial. Can J Anaesth, 2023, 70(6): 1008-1018.
14.	Karahan O, Acet H, Erta? F, et al. The relationship between fibrinogen to albumin ratio and severity of coronary artery disease in patients with STEMI. Am J Emerg Med, 2016, 34(6): 1037-1042.
15.	Karahan O, Yavuz C, Kankilic N, et al. Simple blood tests as predictive markers of disease severity and clinical condition in patients with venous insufficiency. Blood Coagul Fibrinolysis, 2016, 27(6): 684-690.
16.	Guclu H, Ozal SA, Pelitli Gurlu V, et al. Increased fibrinogen to albumin ratio in ischemic retinal vein occlusions. Eur J Ophthalmol, 2017, 27(6): 735-739.
17.	Zhao Y, Yang J, Ji Y, et al. Usefulness of fibrinogen-to-albumin ratio to predict no-reflow and short-term prognosis in patients with ST-segment elevation myocardial infarction undergoing primary percutaneous coronary intervention. Heart Vessels, 2019, 34(10): 1600-1607.
18.	Kassab RB, Elhenawy AA, AbdulrahmanTheyab, et al. Modulation of inflammatory, oxidative, and apoptotic stresses mediates the renoprotective effect of daidzein against glycerol-induced acute kidney injury in rats. Environ Sci Pollut Res Int, 2023, 30(56): 119016-119033.
19.	Gassa A, Borghardt JH, Maier J, et al. Effect of preoperative low serum albumin on postoperative complications and early mortality in patients undergoing transcatheter aortic valve replacement. J Thorac Dis, 2018, 10(12): 6763-6770.
20.	Jensen T, Kierulf P, Sandset PM, et al. Fibrinogen and fibrin induce synthesis of proinflammatory cytokines from isolated peripheral blood mononuclear cells. Thromb Haemost, 2007, 97(5): 822-829.
21.	Machlus KR, Cardenas JC, Church FC, et al. Causal relationship between hyperfibrinogenemia, thrombosis, and resistance to thrombolysis in mice. Blood, 2011, 117(18): 4953-4963.
22.	Induruwa I, Moroi M, Bonna A, et al. Platelet collagen receptor glycoprotein Ⅵ-dimer recognizes fibrinogen and fibrin through their D-domains, contributing to platelet adhesion and activation during thrombus formation. J Thromb Haemost, 2018, 16(2): 389-404.
23.	Yhim HY, Jang MJ, Kwak JY, et al. The incidence, risk factors, and prognosis of recurrent venous thromboembolism (VTE) in patients with advanced solid cancers receiving anticoagulation therapy after the diagnosis of index VTE. Thromb Res, 2013, 131(4): e133-e140. doi: 10.1016/j.thromres.2013.01.025.
24.	Baglin T, Douketis J, Tosetto A, et al. Does the clinical presentation and extent of venous thrombosis predict likelihood and type of recurrence? A patient-level meta-analysis. J Thromb Haemost, 2010, 8(11): 2436-2442.
25.	Kruyt ND, Biessels GJ, Devries JH, et al. Hyperglycemia in acute ischemic stroke: pathophysiology and clinical management. Nat Rev Neurol, 2010, 6(3): 145-155.
26.	Vazzana N, Ranalli P, Cuccurullo C, et al. Diabetes mellitus and thrombosis. Thromb Res, 2012, 129(3): 371-377.
27.	von Haehling S, Doehner W, Anker SD. Nutrition, metabolism, and the complex pathophysiology of cachexia in chronic heart failure. Cardiovasc Res, 2007, 73(2): 298-309.
28.	章黎, 王新穎. 《中國成人患者腸外腸內營養臨床應用指南(2023版)》解讀. 腫瘤代謝與營養電子雜志, 2023, 10(6): 718-723.

1. Naess IA, Christiansen SC, Romundstad P, et al. Incidence and mortality of venous thrombosis: a population-based study. J Thromb Haemost, 2007, 5(4): 692-699.
2. 孫曉萱. 老年靜脈血栓栓塞患者復發風險預測及動態列線圖. 南昌: 南昌大學醫學部, 2024.
3. Guan X, Gong M, Wang X, et al. Low preoperative fibrinogen level is risk factor for neurological complications in acute aortic dissection. Medicine (Baltimore), 2018, 97(21): e10830. doi: 10.1097/MD.0000000000010830.
4. Ying J, Zhou D, Gu T, et al. Pretreatment albumin/fibrinogen ratio as a promising predictor for the survival of advanced non small-cell lung cancer patients undergoing first-line platinum-based chemotherapy. BMC Cancer, 2019, 19(1): 288. doi: 10.1186/s12885-019-5490-y.
5. 吳靜, 楊紅梅, 劉旭輝. 預后營養指數對急性心肌梗死患者介入術后發生急性損傷的預測價值分析. 心肺血管病雜志, 2024, 43(8): 812-817.
6. 王蔚文. 臨床疾病診斷與療效判定標準. 北京: 科學技術文獻出版社, 2010.
7. Onodera T, Goseki N, Kosaki G. Prognostic nutritional index in gastrointestinal surgery of malnourished cancer patients. Nihon Geka Gakkai Zasshi, 1984, 85(9): 1001-1005.
8. Eichinger S, Minar E, Bialonczyk C, et al. D-dimer levels and risk of recurrent venous thromboembolism. JAMA, 2003, 290(8): 1071-1074.
9. Spencer FA, Gurwitz JH, Schulman S, et al. Venous thromboembolism in older adults: A community-based study. Am J Med, 2014, 127(6): 530-537.
10. de Moreuil C, Le Mao R, Le Moigne E, et al. Long-term recurrence risk after a first venous thromboembolism in men and women under 50 years old: A French prospective cohort. Eur J Intern Med, 2021, 84: 24-31.
11. Roach RE, Lijfering WM, Tait RC, et al. Sex difference in the risk of recurrent venous thrombosis: A detailed analysis in four European cohorts. J Thromb Haemost, 2015, 13(10): 1815-1822.
12. Kyrle PA, Kammer M, Eischer L, et al. The long-term recurrence risk of patients with unprovoked venous thromboembolism: an observational cohort study. J Thromb Haemost, 2016, 14(12): 2402-2409.
13. Burns KEA, Heels-Ansdell D, Thabane L, et al. Sex differences in thromboprophylaxis of the critically ill: A secondary analysis of a randomized trial. Can J Anaesth, 2023, 70(6): 1008-1018.
14. Karahan O, Acet H, Erta? F, et al. The relationship between fibrinogen to albumin ratio and severity of coronary artery disease in patients with STEMI. Am J Emerg Med, 2016, 34(6): 1037-1042.
15. Karahan O, Yavuz C, Kankilic N, et al. Simple blood tests as predictive markers of disease severity and clinical condition in patients with venous insufficiency. Blood Coagul Fibrinolysis, 2016, 27(6): 684-690.
16. Guclu H, Ozal SA, Pelitli Gurlu V, et al. Increased fibrinogen to albumin ratio in ischemic retinal vein occlusions. Eur J Ophthalmol, 2017, 27(6): 735-739.
17. Zhao Y, Yang J, Ji Y, et al. Usefulness of fibrinogen-to-albumin ratio to predict no-reflow and short-term prognosis in patients with ST-segment elevation myocardial infarction undergoing primary percutaneous coronary intervention. Heart Vessels, 2019, 34(10): 1600-1607.
18. Kassab RB, Elhenawy AA, AbdulrahmanTheyab, et al. Modulation of inflammatory, oxidative, and apoptotic stresses mediates the renoprotective effect of daidzein against glycerol-induced acute kidney injury in rats. Environ Sci Pollut Res Int, 2023, 30(56): 119016-119033.
19. Gassa A, Borghardt JH, Maier J, et al. Effect of preoperative low serum albumin on postoperative complications and early mortality in patients undergoing transcatheter aortic valve replacement. J Thorac Dis, 2018, 10(12): 6763-6770.
20. Jensen T, Kierulf P, Sandset PM, et al. Fibrinogen and fibrin induce synthesis of proinflammatory cytokines from isolated peripheral blood mononuclear cells. Thromb Haemost, 2007, 97(5): 822-829.
21. Machlus KR, Cardenas JC, Church FC, et al. Causal relationship between hyperfibrinogenemia, thrombosis, and resistance to thrombolysis in mice. Blood, 2011, 117(18): 4953-4963.
22. Induruwa I, Moroi M, Bonna A, et al. Platelet collagen receptor glycoprotein Ⅵ-dimer recognizes fibrinogen and fibrin through their D-domains, contributing to platelet adhesion and activation during thrombus formation. J Thromb Haemost, 2018, 16(2): 389-404.
23. Yhim HY, Jang MJ, Kwak JY, et al. The incidence, risk factors, and prognosis of recurrent venous thromboembolism (VTE) in patients with advanced solid cancers receiving anticoagulation therapy after the diagnosis of index VTE. Thromb Res, 2013, 131(4): e133-e140. doi: 10.1016/j.thromres.2013.01.025.
24. Baglin T, Douketis J, Tosetto A, et al. Does the clinical presentation and extent of venous thrombosis predict likelihood and type of recurrence? A patient-level meta-analysis. J Thromb Haemost, 2010, 8(11): 2436-2442.
25. Kruyt ND, Biessels GJ, Devries JH, et al. Hyperglycemia in acute ischemic stroke: pathophysiology and clinical management. Nat Rev Neurol, 2010, 6(3): 145-155.
26. Vazzana N, Ranalli P, Cuccurullo C, et al. Diabetes mellitus and thrombosis. Thromb Res, 2012, 129(3): 371-377.
27. von Haehling S, Doehner W, Anker SD. Nutrition, metabolism, and the complex pathophysiology of cachexia in chronic heart failure. Cardiovasc Res, 2007, 73(2): 298-309.
28. 章黎, 王新穎. 《中國成人患者腸外腸內營養臨床應用指南(2023版)》解讀. 腫瘤代謝與營養電子雜志, 2023, 10(6): 718-723.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Association between albumin to fibrinogen ratio or prognostic nutrition index and recurrence of venous thromboembolism

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