Systemic Immune-Inflammation Index as a Predictor of Left Atrial Thrombosis in Nonvalvular Atrial Fibrillation
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Abstract
Background: The systemic immune-inflammation index (SII) has recently been investigated for cardiovascular diseases. We aimed to evaluate the relationship between SII and left atrial thrombosis (LAT).
Methods: This retrospective, case-control study recruited patients with nonvalvular atrial fibrillation (NVAF) who underwent transesophageal echocardiography (TEE) for LAT detection before cardioversion or catheter ablation at a tertiary hospital between 2012 and 2021. Demographic characteristics were obtained from the hospital data system. According to TEE findings, the patients were categorized into LAT (+) and (-) groups. Age, gender, history of chronic diseases, urea, creatinine, albumin, hemogram parameters, the neutrophil-lymphocyte ratio (NLR), the platelet-lymphocyte ratio (PLR), SII, the CHADS₂ score, the CHA₂DS₂-VASc score, echocardiographic parameters, antiaggregant-anticoagulant use, and non-paroxysmal atrial fibrillation were included and analyzed.
Results: The study population consisted of 403 patients, including 228 men (56.6%), at a mean age of 60.84±12.26 years. A high white blood cell count (WBC) (OR, 1.26; 95% CI, 1.05 to 1.51; P=0.013), a high SII (OR, 1.00, 95% CI, 1.00 to 1.00; P=0.003), and a low ejection fraction (OR, 0.95; 95% CI, 0.90 to 0.99; P=0.018) were independent predictors of LAT (+). A spontaneous echo contrast (OR, 2.43; 95% CI, 1.35 to 4.39; P=0.003) was associated with LAT (+). SII values above 693.6 predicted LAT (+) with 71.6% sensitivity and 71.7% specificity (AUC, 0.77; P<0.001). The predictiveness of SII was similar to that of NLR (0.77 vs 0.74, P=0.093) but higher than PLR (0.77 vs 0.67; P<0.001) and WBC (0.77 vs 0.69; P=0.031).
Conclusion: SII is an independent predictor of LAT in patients with NVAF.
1. Kannel WB, Wolf PA, Benjamin EJ, Levy D. Prevalence, incidence, prognosis, and predisposing conditions for atrial fibrillation: population-based estimates. Am J Cardiol 1998;82:2-9.
2. Wolf PA, Abbott RD, Kannel WB. Atrial fibrillation as an independent risk factor for stroke: the Framingham Study. Stroke 1991;22:983-988.
3. Jaber WA, Prior DL, Thamilarasan M, Grimm RA, Thomas JD, Klein AL, Asher CR. Efficacy of anticoagulation in resolving left atrial and left atrial appendage thrombi: A transesophageal echocardiographic study. Am Heart J 2000;140:150-156.
4. McCready JW, Nunn L, Lambiase PD, Ahsan SY, Segal OR, Rowland E, Lowe MD, Chow AW. Incidence of left atrial thrombus prior to atrial fibrillation ablation: is pre-procedural transoesophageal echocardiography mandatory? Europace 2010;12:927-932.
5. Koca V, Bozat T, Akkaya V, Sarikamis C, Turk T, Vural H, Ozdemir A. Left atrial thrombus detection with multiplane transesophageal echocardiography: an echocardiographic study with surgical verification. J Heart Valve Dis 1999;8:63-66.
6. Hindricks G, Potpara T, Dagres N, Arbelo E, Bax JJ, Blomström-Lundqvist C, et al; ESC Scientific Document Group. 2020 ESC Guidelines for the diagnosis and management of atrial fibrillation developed in collaboration with the European Association for Cardio-Thoracic Surgery (EACTS): The Task Force for the diagnosis and management of atrial fibrillation of the European Society of Cardiology (ESC) Developed with the special contribution of the European Heart Rhythm Association (EHRA) of the ESC. Eur Heart J 2021;42:373-498.
7. Guo Y, Lip GY, Apostolakis S. Inflammation in atrial fibrillation. J Am Coll Cardiol 2012;60:2263-2270.
8. Watson T, Shantsila E, Lip GY. Mechanisms of thrombogenesis in atrial fibrillation: Virchow's triad revisited. Lancet 2009;373:155-166.
9. Boos CJ, Anderson RA, Lip GY. Is atrial fibrillation an inflammatory disorder? Eur Heart J 2006;27:136-149.
10. Shen LF, Wang QY, Yu Q. The Systemic Immune-Inflammation Index and Albumin as Prognostic Predictors in Laryngeal Carcinoma. Nutr Cancer 2021;73:1916-1923.
11. Huang H, Liu Q, Zhu L, Zhang Y, Lu X, Wu Y, Liu L. Prognostic Value of Preoperative Systemic Immune-Inflammation Index in Patients with Cervical Cancer. Sci Rep 2019;9:3284.
12. Liu Y, Ye T, Chen L, Jin T, Sheng Y, Wu G, Zong G. Systemic immune-inflammation index predicts the severity of coronary stenosis in patients with coronary heart disease. Coron Artery Dis 2021;32:715-720.
13. Tosu AR, Kalyoncuoglu M, Biter Hİ, Cakal S, Selcuk M, Çinar T, Belen E, Can MM. Prognostic Value of Systemic Immune-Inflammation Index for Major Adverse Cardiac Events and Mortality in Severe Aortic Stenosis Patients after TAVI. Medicina (Kaunas) 2021;57:588.
14. Hu B, Yang XR, Xu Y, Sun YF, Sun C, Guo W, Zhang X, Wang WM, Qiu SJ, Zhou J, Fan J. Systemic immune-inflammation index predicts prognosis of patients after curative resection for hepatocellular carcinoma. Clin Cancer Res 2014;20:6212-6222.
15. Gage BF, Waterman AD, Shannon W, Boechler M, Rich MW, Radford MJ. Validation of clinical classification schemes for predicting stroke: results from the National Registry of Atrial Fibrillation. JAMA 2001;285:2864-2870.
16. Lip GY, Nieuwlaat R, Pisters R, Lane DA, Crijns HJ. Refining clinical risk stratification for predicting stroke and thromboembolism in atrial fibrillation using a novel risk factor-based approach: the euro heart survey on atrial fibrillation. Chest 2010;137:263-272.
17. McDonagh TA, Metra M, Adamo M, Gardner RS, Baumbach A, Böhm M, Burri H, Butler J, Čelutkienė J, Chioncel O, Cleland JGF, Coats AJS, Crespo-Leiro MG, Farmakis D, Gilard M, Heymans S, Hoes AW, Jaarsma T, Jankowska EA, Lainscak M, Lam CSP, Lyon AR, McMurray JJV, Mebazaa A, Mindham R, Muneretto C, Francesco Piepoli M, Price S, Rosano GMC, Ruschitzka F, Kathrine Skibelund A; ESC Scientific Document Group. 2021 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure. Eur Heart J 2021;42:3599-3726.
18. Williams B, Mancia G, Spiering W, Agabiti Rosei E, Azizi M, Burnier M, et al. 2018 ESC/ESH Guidelines for the management of arterial hypertension: The Task Force for the management of arterial hypertension of the European Society of Cardiology and the European Society of Hypertension: The Task Force for the management of arterial hypertension of the European Society of Cardiology and the European Society of Hypertension. J Hypertens 2018;36:1953-2041.
19. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2013;36:67-74.
20. Gramiak R, Shah PM. Detection of intracardiac blood flow by pulsed echo-ranging ultrasound. Radiology 1971;100:415-418.
21. Beppu S, Nimura Y, Sakakibara H, Nagata S, Park YD, Izumi S. Smoke-like echo in the left atrial cavity in mitral valve disease: its features and significance. J Am Coll Cardiol 1985;6:744-749.
22. Uziębło-Życzkowska B, Krzesiński P, Jurek A, Kapłon-Cieślicka A, Gorczyca I, Budnik M, Gielerak G, Kiliszek M, Gawałko M, Scisło P, Kochanowski J, Jelonek O, Michalska A, Starzyk K, Filipiak KJ, Wożakowska-Kapłon B, Opolski G. Left Ventricular Ejection Fraction Is Associated with the Risk of Thrombus in the Left Atrial Appendage in Patients with Atrial Fibrillation. Cardiovasc Ther 2020;2020:3501749.
23. Almorad A, Ohanyan A, Pintea Bentea G, Wielandts JY, El Haddad M, Lycke M, O'Neill L, Morissens M, De Keyzer E, Nguyen T, Anghel L, Samyn S, Berdaoui B, Tavernier R, Vandekerckhove Y, Duytschaever M, Verbeet T, Knecht S, Castro Rodriguez J. D-dimer blood concentrations to exclude left atrial thrombus in patients with atrial fibrillation. Heart 2021;107:195-200.
24. Zhang X, Hu M, Wang X, Zhang C, Chen W, Chen S, Zhou J, Chen Y, Lou L, Chen G, Dong F, Hu S, Zheng L, Yang J. New perspective on the risk markers for left atrial thrombosis in patients with atrial fibrillation. Eur J Prev Cardiol 2021;28:641-647.
25. Zhou X, Wang Z, Dou S, Chen K, Liu E, Liu T, Li G, Che J. Biomarkers for Predicting Left Atrial or Left Atrial Appendage Thrombus in Anticoagulated Patients with Nonvalvular Atrial Fibrillation. Cardiol Res Pract 2020;2020:1683142.
26. Jia F, Tian Y, Lei S, Yang Y, Luo S, He Q. Incidence and predictors of left atrial thrombus in patients with atrial fibrillation prior to ablation in the real world of China. Indian Pacing Electrophysiol J 2019;19:134-139.
27. Watson T, Shantsila E, Lip GY. Mechanisms of thrombogenesis in atrial fibrillation: Virchow's triad revisited. Lancet 2009;373:155-166.
28. Yalcin M, Aparci M, Uz O, Isilak Z, Balta S, Dogan M, Kardesoglu E, Uzun M. Neutrophil-lymphocyte ratio may predict left atrial thrombus in patients with nonvalvular atrial fibrillation. Clin Appl Thromb Hemost 2015;21:166-171.
29. Maehama T, Okura H, Imai K, Saito K, Yamada R, Koyama T, Hayashida A, Neishi Y, Kawamoto T, Yoshida K. Systemic inflammation and left atrial thrombus in patients with non-rheumatic atrial fibrillation. J Cardiol 2010;56:118-124.
30. Laridan E, Martinod K, De Meyer SF. Neutrophil Extracellular Traps in Arterial and Venous Thrombosis. Semin Thromb Hemost 2019;45:86-93.
31. Laridan E, Denorme F, Desender L, François O, Andersson T, Deckmyn H, Vanhoorelbeke K, De Meyer SF. Neutrophil extracellular traps in ischemic stroke thrombi. Ann Neurol 2017;82:223-232.
32. Tarnowski D, Poitz DM, Plichta L, Heidrich FM, Wiedemann S, Ruf T, Mierke J, Löhn T, Jellinghaus S, Strasser RH, Ibrahim K, Pfluecke C. Comparison of diverse platelet activation markers as indicators for left atrial thrombus in atrial fibrillation. Platelets 2018;29:41-47.
33. Hotchkiss RS, Karl IE. The pathophysiology and treatment of sepsis. N Engl J Med 2003;348:138-150.
34. Li S, Liu K, Gao Y, Zhao L, Zhang R, Fang H, Tao Y, Liu H, Zhao J, Xia Z, Xu Y, Song B. Prognostic value of systemic immune-inflammation index in acute/subacute patients with cerebral venous sinus thrombosis. Stroke Vasc Neurol 2020;5:368-373.
35. Gok M, Kurtul A. A novel marker for predicting severity of acute pulmonary embolism: systemic immune-inflammation index. Scand Cardiovasc J 2021;55:91-96.
36. Peng J, Wang H, Zhang L, Lin Z. Construction and efficiency analysis of prediction model for venous thromboembolism risk in the elderly after hip fracture. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2021;46:142-148.
37. Huang J, Zhang Q, Wang R, Ji H, Chen Y, Quan X, Zhang C. Systemic Immune-Inflammatory Index Predicts Clinical Outcomes for Elderly Patients with Acute Myocardial Infarction Receiving Percutaneous Coronary Intervention. Med Sci Monit 2019;25:9690-9701.
38. Erdoğan M, Erdöl MA, Öztürk S, Durmaz T. Systemic immune-inflammation index is a novel marker to predict functionally significant coronary artery stenosis. Biomark Med 2020;14:1553-1561.
39. Geng Y, Shao Y, Zhu D, Zheng X, Zhou Q, Zhou W, Ni X, Wu C, Jiang J. Systemic Immune-Inflammation Index Predicts Prognosis of Patients with Esophageal Squamous Cell Carcinoma: A Propensity Score-matched Analysis. Sci Rep 2016;6:39482.
2. Wolf PA, Abbott RD, Kannel WB. Atrial fibrillation as an independent risk factor for stroke: the Framingham Study. Stroke 1991;22:983-988.
3. Jaber WA, Prior DL, Thamilarasan M, Grimm RA, Thomas JD, Klein AL, Asher CR. Efficacy of anticoagulation in resolving left atrial and left atrial appendage thrombi: A transesophageal echocardiographic study. Am Heart J 2000;140:150-156.
4. McCready JW, Nunn L, Lambiase PD, Ahsan SY, Segal OR, Rowland E, Lowe MD, Chow AW. Incidence of left atrial thrombus prior to atrial fibrillation ablation: is pre-procedural transoesophageal echocardiography mandatory? Europace 2010;12:927-932.
5. Koca V, Bozat T, Akkaya V, Sarikamis C, Turk T, Vural H, Ozdemir A. Left atrial thrombus detection with multiplane transesophageal echocardiography: an echocardiographic study with surgical verification. J Heart Valve Dis 1999;8:63-66.
6. Hindricks G, Potpara T, Dagres N, Arbelo E, Bax JJ, Blomström-Lundqvist C, et al; ESC Scientific Document Group. 2020 ESC Guidelines for the diagnosis and management of atrial fibrillation developed in collaboration with the European Association for Cardio-Thoracic Surgery (EACTS): The Task Force for the diagnosis and management of atrial fibrillation of the European Society of Cardiology (ESC) Developed with the special contribution of the European Heart Rhythm Association (EHRA) of the ESC. Eur Heart J 2021;42:373-498.
7. Guo Y, Lip GY, Apostolakis S. Inflammation in atrial fibrillation. J Am Coll Cardiol 2012;60:2263-2270.
8. Watson T, Shantsila E, Lip GY. Mechanisms of thrombogenesis in atrial fibrillation: Virchow's triad revisited. Lancet 2009;373:155-166.
9. Boos CJ, Anderson RA, Lip GY. Is atrial fibrillation an inflammatory disorder? Eur Heart J 2006;27:136-149.
10. Shen LF, Wang QY, Yu Q. The Systemic Immune-Inflammation Index and Albumin as Prognostic Predictors in Laryngeal Carcinoma. Nutr Cancer 2021;73:1916-1923.
11. Huang H, Liu Q, Zhu L, Zhang Y, Lu X, Wu Y, Liu L. Prognostic Value of Preoperative Systemic Immune-Inflammation Index in Patients with Cervical Cancer. Sci Rep 2019;9:3284.
12. Liu Y, Ye T, Chen L, Jin T, Sheng Y, Wu G, Zong G. Systemic immune-inflammation index predicts the severity of coronary stenosis in patients with coronary heart disease. Coron Artery Dis 2021;32:715-720.
13. Tosu AR, Kalyoncuoglu M, Biter Hİ, Cakal S, Selcuk M, Çinar T, Belen E, Can MM. Prognostic Value of Systemic Immune-Inflammation Index for Major Adverse Cardiac Events and Mortality in Severe Aortic Stenosis Patients after TAVI. Medicina (Kaunas) 2021;57:588.
14. Hu B, Yang XR, Xu Y, Sun YF, Sun C, Guo W, Zhang X, Wang WM, Qiu SJ, Zhou J, Fan J. Systemic immune-inflammation index predicts prognosis of patients after curative resection for hepatocellular carcinoma. Clin Cancer Res 2014;20:6212-6222.
15. Gage BF, Waterman AD, Shannon W, Boechler M, Rich MW, Radford MJ. Validation of clinical classification schemes for predicting stroke: results from the National Registry of Atrial Fibrillation. JAMA 2001;285:2864-2870.
16. Lip GY, Nieuwlaat R, Pisters R, Lane DA, Crijns HJ. Refining clinical risk stratification for predicting stroke and thromboembolism in atrial fibrillation using a novel risk factor-based approach: the euro heart survey on atrial fibrillation. Chest 2010;137:263-272.
17. McDonagh TA, Metra M, Adamo M, Gardner RS, Baumbach A, Böhm M, Burri H, Butler J, Čelutkienė J, Chioncel O, Cleland JGF, Coats AJS, Crespo-Leiro MG, Farmakis D, Gilard M, Heymans S, Hoes AW, Jaarsma T, Jankowska EA, Lainscak M, Lam CSP, Lyon AR, McMurray JJV, Mebazaa A, Mindham R, Muneretto C, Francesco Piepoli M, Price S, Rosano GMC, Ruschitzka F, Kathrine Skibelund A; ESC Scientific Document Group. 2021 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure. Eur Heart J 2021;42:3599-3726.
18. Williams B, Mancia G, Spiering W, Agabiti Rosei E, Azizi M, Burnier M, et al. 2018 ESC/ESH Guidelines for the management of arterial hypertension: The Task Force for the management of arterial hypertension of the European Society of Cardiology and the European Society of Hypertension: The Task Force for the management of arterial hypertension of the European Society of Cardiology and the European Society of Hypertension. J Hypertens 2018;36:1953-2041.
19. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2013;36:67-74.
20. Gramiak R, Shah PM. Detection of intracardiac blood flow by pulsed echo-ranging ultrasound. Radiology 1971;100:415-418.
21. Beppu S, Nimura Y, Sakakibara H, Nagata S, Park YD, Izumi S. Smoke-like echo in the left atrial cavity in mitral valve disease: its features and significance. J Am Coll Cardiol 1985;6:744-749.
22. Uziębło-Życzkowska B, Krzesiński P, Jurek A, Kapłon-Cieślicka A, Gorczyca I, Budnik M, Gielerak G, Kiliszek M, Gawałko M, Scisło P, Kochanowski J, Jelonek O, Michalska A, Starzyk K, Filipiak KJ, Wożakowska-Kapłon B, Opolski G. Left Ventricular Ejection Fraction Is Associated with the Risk of Thrombus in the Left Atrial Appendage in Patients with Atrial Fibrillation. Cardiovasc Ther 2020;2020:3501749.
23. Almorad A, Ohanyan A, Pintea Bentea G, Wielandts JY, El Haddad M, Lycke M, O'Neill L, Morissens M, De Keyzer E, Nguyen T, Anghel L, Samyn S, Berdaoui B, Tavernier R, Vandekerckhove Y, Duytschaever M, Verbeet T, Knecht S, Castro Rodriguez J. D-dimer blood concentrations to exclude left atrial thrombus in patients with atrial fibrillation. Heart 2021;107:195-200.
24. Zhang X, Hu M, Wang X, Zhang C, Chen W, Chen S, Zhou J, Chen Y, Lou L, Chen G, Dong F, Hu S, Zheng L, Yang J. New perspective on the risk markers for left atrial thrombosis in patients with atrial fibrillation. Eur J Prev Cardiol 2021;28:641-647.
25. Zhou X, Wang Z, Dou S, Chen K, Liu E, Liu T, Li G, Che J. Biomarkers for Predicting Left Atrial or Left Atrial Appendage Thrombus in Anticoagulated Patients with Nonvalvular Atrial Fibrillation. Cardiol Res Pract 2020;2020:1683142.
26. Jia F, Tian Y, Lei S, Yang Y, Luo S, He Q. Incidence and predictors of left atrial thrombus in patients with atrial fibrillation prior to ablation in the real world of China. Indian Pacing Electrophysiol J 2019;19:134-139.
27. Watson T, Shantsila E, Lip GY. Mechanisms of thrombogenesis in atrial fibrillation: Virchow's triad revisited. Lancet 2009;373:155-166.
28. Yalcin M, Aparci M, Uz O, Isilak Z, Balta S, Dogan M, Kardesoglu E, Uzun M. Neutrophil-lymphocyte ratio may predict left atrial thrombus in patients with nonvalvular atrial fibrillation. Clin Appl Thromb Hemost 2015;21:166-171.
29. Maehama T, Okura H, Imai K, Saito K, Yamada R, Koyama T, Hayashida A, Neishi Y, Kawamoto T, Yoshida K. Systemic inflammation and left atrial thrombus in patients with non-rheumatic atrial fibrillation. J Cardiol 2010;56:118-124.
30. Laridan E, Martinod K, De Meyer SF. Neutrophil Extracellular Traps in Arterial and Venous Thrombosis. Semin Thromb Hemost 2019;45:86-93.
31. Laridan E, Denorme F, Desender L, François O, Andersson T, Deckmyn H, Vanhoorelbeke K, De Meyer SF. Neutrophil extracellular traps in ischemic stroke thrombi. Ann Neurol 2017;82:223-232.
32. Tarnowski D, Poitz DM, Plichta L, Heidrich FM, Wiedemann S, Ruf T, Mierke J, Löhn T, Jellinghaus S, Strasser RH, Ibrahim K, Pfluecke C. Comparison of diverse platelet activation markers as indicators for left atrial thrombus in atrial fibrillation. Platelets 2018;29:41-47.
33. Hotchkiss RS, Karl IE. The pathophysiology and treatment of sepsis. N Engl J Med 2003;348:138-150.
34. Li S, Liu K, Gao Y, Zhao L, Zhang R, Fang H, Tao Y, Liu H, Zhao J, Xia Z, Xu Y, Song B. Prognostic value of systemic immune-inflammation index in acute/subacute patients with cerebral venous sinus thrombosis. Stroke Vasc Neurol 2020;5:368-373.
35. Gok M, Kurtul A. A novel marker for predicting severity of acute pulmonary embolism: systemic immune-inflammation index. Scand Cardiovasc J 2021;55:91-96.
36. Peng J, Wang H, Zhang L, Lin Z. Construction and efficiency analysis of prediction model for venous thromboembolism risk in the elderly after hip fracture. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2021;46:142-148.
37. Huang J, Zhang Q, Wang R, Ji H, Chen Y, Quan X, Zhang C. Systemic Immune-Inflammatory Index Predicts Clinical Outcomes for Elderly Patients with Acute Myocardial Infarction Receiving Percutaneous Coronary Intervention. Med Sci Monit 2019;25:9690-9701.
38. Erdoğan M, Erdöl MA, Öztürk S, Durmaz T. Systemic immune-inflammation index is a novel marker to predict functionally significant coronary artery stenosis. Biomark Med 2020;14:1553-1561.
39. Geng Y, Shao Y, Zhu D, Zheng X, Zhou Q, Zhou W, Ni X, Wu C, Jiang J. Systemic Immune-Inflammation Index Predicts Prognosis of Patients with Esophageal Squamous Cell Carcinoma: A Propensity Score-matched Analysis. Sci Rep 2016;6:39482.
| Files | ||
| Issue | Vol 18 No 2 (2023): J Teh Univ Heart Ctr | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/jthc.v18i2.13317 | |
| Keywords | ||
| Thrombus Atrial fibrillation Inflammation Biomarkers Echocardiography | ||
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How to Cite
1.
Dolu AK, Akyıldız Akçay F, Atalay M, Karaca M. Systemic Immune-Inflammation Index as a Predictor of Left Atrial Thrombosis in Nonvalvular Atrial Fibrillation. J Tehran Heart Cent. 2023;18(2):87-93.
