Changes in hematological inflammatory markers in patients with unstable angina and post-COVID-19 syndrome: impact of smoking
DOI:
https://doi.org/10.14739/2310-1210.2025.6.331606Keywords:
unstable angina, post-COVID syndrome, smoking, leukocytes, inflammatory markersAbstract
To evaluate changes in key hematological parameters and levels of leukocyte inflammatory markers in patients with unstable angina (UA), stratified by post-COVID-19 syndrome status and smoking history.
Materials and methods. A total of 147 patients with UA were included in the study. Group I included 87 patients with post-COVID-19 syndrome, and Group II consisted of 60 patients without post-COVID-19 syndrome. Each group was subdivided by smoking status: IA and IIA (smokers), IB and IIB (non-smokers). The following parameters were assessed in all subgroups: main hematological indicators and leukocyte inflammatory markers: neutrophil/lymphocyte ratio (NLR), monocyte/lymphocyte ratio (MLR), platelet/lymphocyte ratio (PLR), systemic immune inflammation index (SII), systemic inflammation response index (SIRI), and aggregate index of systemic inflammation (AISI).
Results. Mean levels of MLR (37.93 %), SIRI (55.90 %), and AISI (53.99 %) were significantly higher in subgroup IA (smokers with post-COVID-19 syndrome) compared to subgroup IIA (smokers without post-COVID-19 syndrome). In subgroup IA, the proportion of patients exceeding optimal threshold values for MLR, SII, SIRI, and AISI was also 20–35 % significantly higher than in subgroup IIA. Among non-smokers with post-COVID-19 syndrome (subgroup IB), mean levels of NLR, SII, SIRI, and AISI were 33–40 % significantly higher than in subgroup of non-smokers without post-COVID-19 syndrome (subgroup IIB). Additionally, the percentage of individuals exceeding optimal thresholds for NLR, MLR, PLR, SII, and AISI was 20–30 % higher in subgroup IB than in subgroup IIB. The highest mean levels of NLR (50.0 %), MLR (37.9 %), as well as SII, SIRI, and AISI (52–62 %) were observed in subgroup IA compared to subgroup IIB.
Conclusions. Patients with post-COVID-19 syndrome demonstrated significantly higher levels of leukocyte inflammatory markers. In both smoker subgroups (IA and IIA) compared to non-smoker subgroups (IB and IIB), NLR, MLR, SII, SIRI, and AISI levels were significantly elevated by 33–55 %. The most pronounced changes in blood inflammatory markers and the highest proportions of patients exceeding optimal thresholds (NLR, MLR, PLR, SII, SIRI) were recorded in subgroup IA (smokers with post-COVID-19 syndrome).
References
Ballering AV, van Zon SK, Olde Hartman TC, Rosmalen JG; Lifelines Corona Research Initiative. Persistence of somatic symptoms after COVID-19 in the Netherlands: an observational cohort study. Lancet. 2022;400(10350):452-61. doi: https://doi.org/10.1016/S0140-6736(22)01214-4
Scholkmann F, May CA. COVID-19, post-acute COVID-19 syndrome (PACS, "long COVID") and post-COVID-19 vaccination syndrome (PCVS, "post-COVIDvac-syndrome"): Similarities and differences. Pathol Res Pract. 2023;246:154497. doi: https://doi.org/10.1016/j.prp.2023.154497
Fernández-de-Las-Peñas C, Florencio LL, Gómez-Mayordomo V, Cuadrado ML, Palacios-Ceña D, Raveendran AV. Proposed integrative model for post-COVID symptoms. Diabetes Metab Syndr. 2021;15(4):102159. doi: https://doi.org/10.1016/j.dsx.2021.05.032
Yong SJ, Liu S. Proposed subtypes of post-COVID-19 syndrome (or long-COVID) and their respective potential therapies. Rev Med Virol. 2022;32(4):e2315. doi: https://doi.org/10.1002/rmv.2315
Reese JT, Blau H, Casiraghi E, Bergquist T, Loomba JJ, Callahan TJ, et al. Generalisable long COVID subtypes: findings from the NIH N3C and RECOVER programmes. EBioMedicine. 2023;87:104413. doi: https://doi.org/10.1016/j.ebiom.2022.104413
Raveendran AV, Jayadevan R, Sashidharan S. Long COVID: An overview. Diabetes Metab Syndr. 2021;15(3):869-75. doi: https://doi.org/10.1016/j.dsx.2021.04.007. Erratum in: Diabetes Metab Syndr. 2022;16(5):102504. doi: https://doi.org/10.1016/j.dsx.2022.102504. Erratum in: Diabetes Metab Syndr. 2022;16(12):102660. doi: https://doi.org/10.1016/j.dsx.2022.102660
Fischer A, Badier N, Zhang L, Elbéji A, Wilmes P, Oustric P, et al. Long COVID Classification: Findings from a Clustering Analysis in the Predi-COVID Cohort Study. Int J Environ Res Public Health. 2022;19(23):16018. doi: https://doi.org/10.3390/ijerph192316018
Task Force for the management of COVID-19 of the European Society of Cardiology. European Society of Cardiology guidance for the diagnosis and management of cardiovascular disease during the COVID-19 pandemic: part 1-epidemiology, pathophysiology, and diagnosis. Eur Heart J. 2022;43(11):1033-58. doi: https://doi.org/10.1093/eurheartj/ehab696. Erratum in: Eur Heart J. 2022;43(18):1776. doi: https://doi.org/10.1093/eurheartj/ehab866
Lechuga GC, Morel CM, De-Simone SG. Hematological alterations associated with long COVID-19. Front Physiol. 2023;14:1203472. doi: https://doi.org/10.3389/fphys.2023.1203472
Galúcio VCA, Menezes DC, Lima PD, Palácios VR, Vasconcelos PF, Quaresma JA, Falcão LF. Evaluation of the Hematological Patterns from Up to 985 Days of Long COVID: A Cross-Sectional Study. Viruses. 2023;15(4):879. doi: https://doi.org/10.3390/v15040879
Al-Aly Z, Bowe B, Xie Y. Long COVID after breakthrough SARS-CoV-2 infection. Nat Med. 2022;28(7):1461-7. doi: https://doi.org/10.1038/s41591-022-01840-0
Łuczyk RJ, Ślifirczyk A, Sieńska W, Łuczyk M, Baryła-Matejczuk M, Sikora K, et al. What Increases Smokers' Stress? Degree of Nicotine Dependence and Motivation to Quit Smoking in People After Myocardial Infarction. J Clin Med. 2025;14(5):1545. doi: https://doi.org/10.3390/jcm14051545
Pedersen KM, Çolak Y, Ellervik C, Hasselbalch HC, Bojesen SE, Nordestgaard BG. Smoking and Increased White and Red Blood Cells. Arterioscler Thromb Vasc Biol. 2019;39(5):965-77. doi: https://doi.org/10.1161/ATVBAHA.118.312338
Han K, Shi D, Yang L, Wang Z, Li Y, Gao F, et al. Prognostic value of systemic inflammatory response index in patients with acute coronary syndrome undergoing percutaneous coronary intervention. Ann Med. 2022;54(1):1667-77. doi: https://doi.org/10.1080/07853890.2022.2083671
Li Q, Ma X, Shao Q, Yang Z, Wang Y, Gao F, et al. Prognostic Impact of Multiple Lymphocyte-Based Inflammatory Indices in Acute Coronary Syndrome Patients. Front Cardiovasc Med. 2022;9:811790. doi: https://doi.org/10.3389/fcvm.2022.811790
Ministry of Health of Ukraine. [Unified clinical protocol of emergency, primary, secondary (specialized), tertiary (highly specialized) medical care and medical rehabilitation. Acute coronary syndrome without ST segment elevation]. Order dated 2021 Sep 15, No. 1957. Ukrainian. Available from: https://zakon.rada.gov.ua/rada/show/v1957282-21
Ministry of Health of Ukraine. [Unified clinical protocol of emergency, primary, secondary (specialized), tertiary (highly specialized) medical care and medical rehabilitation. Acute coronary syndrome with ST segment elevation]. Order dated 2021 Sep 14, No. 1936. Ukrainian. Available from: https://zakon.rada.gov.ua/rada/show/v1936282-21
Byrne RA, Rossello X, Coughlan JJ, Barbato E, Berry C, Chieffo A, et al. 2023 ESC Guidelines for the management of acute coronary syndromes. Eur Heart J. 2023;44(38):3720-826. doi: https://doi.org/10.1093/eurheartj/ehad191
Alberta Health Services. Post COVID-19 Functional Status Scale and Post COVID-19 Symptom Checklist [Internet]. Alberta Health Services; 2022 May [cited 2025 May 13]. Available from: https://www.albertahealthservices.ca/frm-21820.pdf
Balsara K, Iftikhar A, Galiatsatos P, DiClemente C, Mattingly B, Kanarek NF. Cigarette smoking, mental health, depression, Maryland Behavioral Risk Factor Surveillance System survey, 2020. Tob Use Insights. 2024;17:1179173X241285351. doi: https://doi.org/10.1177/1179173X241285351
Pivina L, Batenova G, Ygiyeva D, Orekhov A, Pivin M, Dyussupov A. Assessment of the Predictive Ability of the Neutrophil-to-Lymphocyte Ratio in Patients with In-Stent Restenosis after COVID-19. Diagnostics (Basel). 2024;14(20):2262. doi: https://doi.org/10.3390/diagnostics14202262
Tudurachi BS, Anghel L, Tudurachi A, Sascău RA, Stătescu C. Assessment of inflammatory hematological ratios (NLR, PLR, MLR, LMR and monocyte/HDL-cholesterol ratio) in acute myocardial infarction and particularities in young patients. Int J Mol Sci. 2023;24(18):14378. doi: https://doi.org/10.3390/ijms241814378
Tashchuk VK, Bota RA, Al Salama MVO. [Dynamics of leukocyte inflammatory markers in patients with ST-elevation myocardial infarction depending on left ventricle ejection fraction]. Pathologia. 2022;19(3):195-200. Ukrainian. doi: https://doi.org/10.14739/2310-1237.2022.3.267268
Jin Z, Wu Q, Chen S, Gao J, Li X, Zhang X, et al. The Associations of Two Novel Inflammation Indexes, SII and SIRI with the Risks for Cardiovascular Diseases and All-Cause Mortality: A Ten-Year Follow-Up Study in 85,154 Individuals. J Inflamm Res. 2021;14:131-40. doi: https://doi.org/10.2147/JIR.S283835
Jiang Y, Luo B, Lu W, Chen Y, Peng Y, Chen L, et al. Association Between the Aggregate Index of Systemic Inflammation and Clinical Outcomes in Patients with Acute Myocardial Infarction: A Retrospective Study. J Inflamm Res. 2024;17:7057-67. doi: https://doi.org/10.2147/JIR.S481515
Suryana KK, Widiana R, Suharsono H, Pujasakti MP, Putra W, Yaniswari N. Severity of anxiety disorder and other factors associated with disease severity among COVID-19 patients in a hospital, Bali, Indonesia. Med J Malays. 2021;76(4):461-5.
Fedrizal FF, Wijaya IP, Abdullah M, Yamin M. Elevated neutrophil-to-lymphocyte ratio and smoking are associated with chronic total occlusion in patients with ST elevation myocardial infarction. BMC Cardiovasc Disord. 2024;24(1):12. doi: https://doi.org/10.1186/s12872-023-03680-3
Haybar H, Pezeshki SM, Saki N. Evaluation of complete blood count parameters in cardiovascular diseases: An early indicator of prognosis? Exp Mol Pathol. 2019;110:104267. doi: https://doi.org/10.1016/j.yexmp.2019.104267
Lagunas-Rangel FA. Neutrophil-to-lymphocyte ratio and lymphocyte-to-C-reactive protein ratio in patients with severe coronavirus disease 2019 (COVID-19): A meta-analysis. J Med Virol. 2020;92(10):1733. doi: https://doi.org/10.1002/jmv.25819
Ponti G, Maccaferri M, Ruini C, Tomasi A, Ozben T. Biomarkers associated with COVID-19 disease progression. Crit Rev Clin Lab Sci. 2020;57(6):389-99. doi: https://doi.org/10.1080/10408363.2020.1770685
Long L, Zeng X, Zhang X, Xiao W, Guo E, Zhan W, et al. Short-term outcomes of coronavirus disease 2019 and risk factors for progression. Eur Respir J. 2020;55(5):2000990. doi: https://doi.org/10.1183/13993003.00990-2020
Li J, He D, Yu J, Chen S, Wu Q, Cheng Z, et al. Dynamic status of SII and SIRI alters the risk of cardiovascular diseases: Evidence from Kailuan cohort study. J Inflamm Res. 2022;15:5945-57. doi: https://doi.org/10.2147/JIR.S378309
Xia Y, Xia C, Wu L, Li Z, Li H, Zhang J. Systemic immune inflammation index (SII), system inflammation response index (SIRI) and risk of all-cause mortality and cardiovascular mortality: A 20-year follow-up cohort study of 42,875 US adults. J Clin Med. 2023;12(3):1128. doi: https://doi.org/10.3390/jcm12031128
Xing Y, Sun D, Chen G. Analysis of the Dynamic Cushioning Property of Expanded Polyethylene Based on the Stress-Energy Method. Polymers (Basel). 2023;15(17):3603. doi: https://doi.org/10.3390/polym15173603
Chen YD, Wen ZG, Long JJ, Wang Y. Association between systemic inflammation response index and slow coronary flow phenomenon in patients with ischemia and no obstructive coronary arteries. Int J Gen Med. 2024;17:4045-53. doi: https://doi.org/10.2147/IJGM.S481538
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