Klinik Araştırma
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Relationship Between Atherogenic Indices and Cardiovascular Thromboembolic Events in Patients with COVID-19 Pneumonia

Yıl 2025, Cilt: 7 Sayı: 2, 227 - 234, 23.06.2025
https://doi.org/10.52827/hititmedj.1594744

Öz

Objective: COVID-19, caused by coronavirus SARS-CoV-2, is a pandemic viral respiratory infection in which venous and arterial thromboembolic events are often observed. This study aimed to investigate the relationship between atherogenic indices and cardiovascular thromboembolic events in patients with COVID-19 pneumonia.
Material and Method: In this retrospective study, a total of 805 inpatients (median age 63 [IQR: 52-74] years; 45.1% female) who were diagnosed with COVID-19 pneumonia between March 2020 and December 2020 were evaluated. Patients were divided into two groups based on cardiovascular thromboembolic events with cardiovascular thromboembolic events (n=96) and without-cardiovascular thromboembolic events (n=709). All clinical and demographic data and laboratory results were analyzed. Atherogenic Index of Plasma (AIP (log10 (triglyceride/ HDL)), Atherogenic Coefficient (AC (HDL/ non-HDL)), Risk Index of Castelli-I (CRI-I (Total cholesterol/ HDL)), and Risk Index of Castelli-II (CRI-II (LDL/ HDL)) were calculated.
Results: Atherogenic Coefficient, CRI-I, and CRI-II values were significantly higher in the cardiovascular thromboembolic event group (p=0.001, p=0.001, p=0.007, respectively). AIP values were higher in the cardiovascular thromboembolic events group but were not statistically significant (p=0.051). In the cardiovascular thromboembolic events group, HDL values were found to be significantly lower (p=0.001), but CRP and D-dimer values were found to be significantly higher (p<0.001, p=0.006, respectively). In the multivariable analysis, Atherogenic Coefficient (OR: 1.294, 95% CI: 1.089-1.1537, p=0.003), D-dimer, Hypertension, and current smoking were found to be independent predictors of cardiovascular thromboembolic events in patients with COVID-19 pneumonia.
Conclusion: Atherogenic indices could be used to predict cardiovascular thromboembolic events in patients with COVID-19 pneumonia.

Etik Beyan

This study was approved by the local ethics committee of Sisli Hamidiye Etfal Training and Research Hospital with protocol No. 3227.

Destekleyen Kurum

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Kaynakça

  • Al-Ani F, Chehade S, Lazo-Langner A. Thrombosis risk associated with COVID-19 infection. A scoping review. Thrombosis Research 2020;192:152–160.
  • Wichmann D, Sperhake JP, Lütgehetmann M, et al. Autopsy Findings and Venous Thromboembolism in Patients With COVID-19: A Prospective Cohort Study. Annals of Internal Medicine 2020;173(4):268–277.
  • Ribes A, Vardon-Bounes F, Mémier V, et al. Thromboembolic events and Covid-19. Advances in Biological Regulation 2020;77:100735.
  • Li Y, Zhao K, Wei H et al. Dynamic relationship between D-dimer and COVID-19 severity. Br J Haematol 2020;190(1):e25-27.
  • Wagner J, Garcia-Rodriguez V, Yu A, et al. Elevated D-Dimer Is Associated with Multiple Clinical Outcomes in Hospitalized Covid-19 Patients: a Retrospective Cohort Study. SN Compr Clin Med 2020;2(12):2561–2567.
  • Long B, Brady WJ, Koyfman A, Gottlieb M. Cardiovascular complications in COVID-19. The American Journal of Emergency Medicine 2020;38(7):1504–1507.
  • Chen J, Wu Y, Chen Z et al. High incidence of stroke in COVID-19 patients. Aging 2020;12(22):22390-22398.
  • Del Prete A, Conway F, Della Rocca DG, et al. COVID-19, Acute Myocardial Injury, and Infarction. Cardiac Electrophysiology Clinics 2022;14(1):29–39.
  • Magadum A, Kishore R. Cardiovascular Manifestations of COVID-19 Infection. Cells 2020;9(11):2508.
  • Thachil J, Tang N, Gando S, et al. ISTH interim guidance on recognition and management of coagulopathy in COVID-19. Journal of Thrombosis and Haemostasis 2020;18(5):1023–1026.
  • Miesbach W, Makris M. COVID-19: Coagulopathy, Risk of Thrombosis, and the Rationale for Anticoagulation. Clin Appl Thromb Hemost 2020;26:1-7.
  • Medetalibeyoglu A, Emet S, Senkal N, Aydogan M, Kose M, Tukek T. Cardiovascular view of intermediate and high-risk COVID-19 patients: single-centre experience with low mortality and intensive care hospitalisation rates. CVJA 2021;32(2):25–32.
  • Di Angelantonio E, Gao P, Pennells L, et al. Lipid-Related Markers and Cardiovascular Disease Prediction. JAMA 2012;307(23):2499-2506.
  • Kim MK, Han K, Kim HS, et al. Cholesterol variability and the risk of mortality, myocardial infarction, and stroke: a nationwide population-based study. European Heart Journal 2017;38(48):3560–3566.
  • Fernández-Macías JC, Ochoa-Martínez AC, Varela-Silva JA, Pérez-Maldonado IN. Atherogenic Index of Plasma: Novel Predictive Biomarker for Cardiovascular Illnesses. Archives of Medical Research 2019;50(5):285–294.
  • Koca TT, Tugan CB, Seyithanoglu M, Kocyıgıt BF. The Clinical Importance of the Plasma Atherogenic Index, Other Lipid Indexes, and Urinary Sodium and Potassium Excretion in Patients with Stroke. Eurasian J Med 2019;51(2):171–175.
  • Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19. The Lancet 2020;395(10234):1417–1418.
  • Alzoughool F, Alanagreh L, Abumweis S, Atoum M. Cerebrovascular comorbidity, high blood levels of C-reactive protein and D-dimer are associated with disease outcomes in COVID-19 patients. CH 2021;77(3):311–322.
  • Modin D, Claggett B, Sindet-Pedersen C, et al. Acute COVID-19 and the Incidence of Ischemic Stroke and Acute Myocardial Infarction. Circulation 2020;142(21):2080–2082.
  • Kashi M, Jacquin A, Dakhil B, et al. Severe arterial thrombosis associated with Covid-19 infection. Thrombosis Research 2020;192:75–77.
  • Weiss P, Murdoch DR. Clinical course and mortality risk of severe COVID-19. The Lancet 2020;395(10229):1014–5.
  • Harrison SL, Buckley BJR, Rivera-Caravaca JM, Zhang J, Lip GYH. Cardiovascular risk factors, cardiovascular disease, and COVID-19: an umbrella review of systematic reviews. European Heart Journal - Quality of Care and Clinical Outcomes 2021;7:330-339.
  • Cui S, Chen S, Li X, Liu S, Wang F. Prevalence of venous thromboembolism in patients with severe novel coronavirus pneumonia. Journal of Thrombosis and Haemostasis 2020;18(6):1421–1424.
  • Brosnahan SB, Smilowitz NR, Amoroso NE, et al. Thrombosis at hospital presentation in patients with and without coronavirus disease 2019. Journal of Vascular Surgery: Venous and Lymphatic Disorders 2021;9(4):845–852.
  • Demelo-Rodríguez P, Cervilla-Muñoz E, Ordieres-Ortega L et al. Incidence of asymptomatic deep vein thrombosis in patients with COVID-19 pneumonia and elevated D-dimer levels. Thrombosis Research 2020;192:23–26.
  • Bosevski M, Krstevski G, Bosevska G, et al. The role of D-dimer in relation to the clinical course of patients with COVID-19. ABBS 2020;53(1):119–120.
  • Valerio L, Ferrazzi P, Sacco C et al. Course of D-Dimer and C-Reactive Protein Levels in Survivors and Nonsurvivors with COVID-19 Pneumonia: A Retrospective Analysis of 577 Patients. Thromb Haemost 2021;121(01):98–101.
  • Eljilany I, Elzouki AN. D-Dimer, Fibrinogen, and IL-6 in COVID-19 Patients with Suspected Venous Thromboembolism: A Narrative Review. VHRM 2020;16:455–462.
  • Bannaga AS, Tabuso M, Farrugia A, et al. C-reactive protein and albumin association with mortality of hospitalised SARS-CoV-2 patients: A tertiary hospital experience. Clin Med 2020;20(5):463–467.
  • Libby P, Lüscher T. COVID-19 is, in the end, an endothelial disease. European Heart Journal 2020;41(32):3038–3044.
  • Pons S, Fodil S, Azoulay E, Zafrani L. The vascular endothelium: the cornerstone of organ dysfunction in severe SARS-CoV-2 infection. Crit Care 2020;24(1):353.
  • Lin GL, McGinley JP, Drysdale SB, Pollard AJ. Epidemiology and Immune Pathogenesis of Viral Sepsis. Front Immunol 2018;9:2147.
  • Kinosian B. Cholesterol and Coronary Heart Disease: Predicting Risks by Levels and Ratios. Ann Intern Med 1994;121(9):641.
  • Gunay S, Sariaydin M, Acay A. New Predictor of Atherosclerosis in Subjects With COPD: Atherogenic Indices. Respir Care 2016;61(11):1481–1487.
  • Sujatha R, Kavitha S. Atherogenic indices in stroke patients: A retrospective study. Iran J Neurol 2017;16(2):78–82.
  • Turgay Yıldırım Ö, Kaya Ş. The atherogenic index of plasma as a predictor of mortality in patients with COVID-19. Heart & Lung 2021;50(2):329–333.

COVID-19 Pnömonili Hastalarda Aterojenik İndeksler ile Kardiyovasküler Tromboembolik Olaylar Arasındaki İlişki

Yıl 2025, Cilt: 7 Sayı: 2, 227 - 234, 23.06.2025
https://doi.org/10.52827/hititmedj.1594744

Öz

Amaç: Koronavirüs SARS-CoV 2’nin neden olduğu COVID-19, venöz ve arteriyel tromboembolik olayların sıklıkla görüldüğü pandemik bir viral solunum yolu enfeksiyonudur. Bu çalışma COVID-19 pnömonili hastalarda aterojenik indeksler ile kardiyovasküler tromboembolik olaylar arasındaki ilişkiyi araştırmayı amaçlamıştır.
Gereç ve Yöntem: Bu retrospektif çalışmaya Mart 2020 ile Aralık 2020 arasında COVID-19 pnömonisi tanısı alan toplam 805 yatan hasta (ortanca yaş 63 [IQR: 52-74] yıl; %45,1 kadın) dahil edildi. Hastalar kardiyovasküler tromboembolik olaylara göre kardiyovasküler tromboembolik olay olanlar (n=96) ve kardiyovasküler tromboembolik olay olmayanlar (n=709) olarak iki gruba ayrıldı. Tüm klinik ve demografik veriler ve laboratuvar sonuçları analiz edildi. Çalışmaya dahil edilen hastalarda Plazmanın Aterojenik İndeksi (AIP (Log10 (trigliserit / HDL)), Aterojenik Coefficient (AC (HDL / HDL olmayan)) Castelli-I Risk İndeksi (CRI-I (Total kolesterol / HDL)), Castelli-II Risk İndeksi (CRI-II (LDL / HDL)) hesaplanmıştır.
Bulgular: Aterojenik Coefficient, CRI-I ve CRI-II değerleri kardiyovasküler tromboembolik olay grubunda istatistiksel anlamlı derecede yüksek saptandı (sırasıyla p=0,001, p=0,001, p=0,007). Kardiyovasküler tromboembolik olaylar grubunda AIP değerleri daha yüksekti ancak istatistiksel olarak anlamlı değildi (p=0,051). Kardiyovasküler tromboembolik olaylar grubunda HDL değerleri istatiksel olarak anlamlı derecede düşük bulundu (p=0,001), CRP ve D-dimer değerleri ise istatiksel olarak anlamlı olarak yüksek bulundu (sırasıyla p<0,001, p=0,006). Çok değişkenli analizde COVID-19 pnömonili hastalarda Aterojenik Coefficient (OR: 1,294, %95 CI: 1,089-1,1537, p= 0,003), D-dimer, Hipertansiyon ve mevcut sigara içiminin kardiyovasküler tromboembolik olayların bağımsız öngördürücüleri olduğu saptandı.
Sonuç: Bu çalışmanın sonuçları COVID-19 pnömonili hastalarda kardiyovasküler tromboembolik olayları tahmin etmek için aterojenik indeksler kullanılabileceğini göstermektedir.

Kaynakça

  • Al-Ani F, Chehade S, Lazo-Langner A. Thrombosis risk associated with COVID-19 infection. A scoping review. Thrombosis Research 2020;192:152–160.
  • Wichmann D, Sperhake JP, Lütgehetmann M, et al. Autopsy Findings and Venous Thromboembolism in Patients With COVID-19: A Prospective Cohort Study. Annals of Internal Medicine 2020;173(4):268–277.
  • Ribes A, Vardon-Bounes F, Mémier V, et al. Thromboembolic events and Covid-19. Advances in Biological Regulation 2020;77:100735.
  • Li Y, Zhao K, Wei H et al. Dynamic relationship between D-dimer and COVID-19 severity. Br J Haematol 2020;190(1):e25-27.
  • Wagner J, Garcia-Rodriguez V, Yu A, et al. Elevated D-Dimer Is Associated with Multiple Clinical Outcomes in Hospitalized Covid-19 Patients: a Retrospective Cohort Study. SN Compr Clin Med 2020;2(12):2561–2567.
  • Long B, Brady WJ, Koyfman A, Gottlieb M. Cardiovascular complications in COVID-19. The American Journal of Emergency Medicine 2020;38(7):1504–1507.
  • Chen J, Wu Y, Chen Z et al. High incidence of stroke in COVID-19 patients. Aging 2020;12(22):22390-22398.
  • Del Prete A, Conway F, Della Rocca DG, et al. COVID-19, Acute Myocardial Injury, and Infarction. Cardiac Electrophysiology Clinics 2022;14(1):29–39.
  • Magadum A, Kishore R. Cardiovascular Manifestations of COVID-19 Infection. Cells 2020;9(11):2508.
  • Thachil J, Tang N, Gando S, et al. ISTH interim guidance on recognition and management of coagulopathy in COVID-19. Journal of Thrombosis and Haemostasis 2020;18(5):1023–1026.
  • Miesbach W, Makris M. COVID-19: Coagulopathy, Risk of Thrombosis, and the Rationale for Anticoagulation. Clin Appl Thromb Hemost 2020;26:1-7.
  • Medetalibeyoglu A, Emet S, Senkal N, Aydogan M, Kose M, Tukek T. Cardiovascular view of intermediate and high-risk COVID-19 patients: single-centre experience with low mortality and intensive care hospitalisation rates. CVJA 2021;32(2):25–32.
  • Di Angelantonio E, Gao P, Pennells L, et al. Lipid-Related Markers and Cardiovascular Disease Prediction. JAMA 2012;307(23):2499-2506.
  • Kim MK, Han K, Kim HS, et al. Cholesterol variability and the risk of mortality, myocardial infarction, and stroke: a nationwide population-based study. European Heart Journal 2017;38(48):3560–3566.
  • Fernández-Macías JC, Ochoa-Martínez AC, Varela-Silva JA, Pérez-Maldonado IN. Atherogenic Index of Plasma: Novel Predictive Biomarker for Cardiovascular Illnesses. Archives of Medical Research 2019;50(5):285–294.
  • Koca TT, Tugan CB, Seyithanoglu M, Kocyıgıt BF. The Clinical Importance of the Plasma Atherogenic Index, Other Lipid Indexes, and Urinary Sodium and Potassium Excretion in Patients with Stroke. Eurasian J Med 2019;51(2):171–175.
  • Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19. The Lancet 2020;395(10234):1417–1418.
  • Alzoughool F, Alanagreh L, Abumweis S, Atoum M. Cerebrovascular comorbidity, high blood levels of C-reactive protein and D-dimer are associated with disease outcomes in COVID-19 patients. CH 2021;77(3):311–322.
  • Modin D, Claggett B, Sindet-Pedersen C, et al. Acute COVID-19 and the Incidence of Ischemic Stroke and Acute Myocardial Infarction. Circulation 2020;142(21):2080–2082.
  • Kashi M, Jacquin A, Dakhil B, et al. Severe arterial thrombosis associated with Covid-19 infection. Thrombosis Research 2020;192:75–77.
  • Weiss P, Murdoch DR. Clinical course and mortality risk of severe COVID-19. The Lancet 2020;395(10229):1014–5.
  • Harrison SL, Buckley BJR, Rivera-Caravaca JM, Zhang J, Lip GYH. Cardiovascular risk factors, cardiovascular disease, and COVID-19: an umbrella review of systematic reviews. European Heart Journal - Quality of Care and Clinical Outcomes 2021;7:330-339.
  • Cui S, Chen S, Li X, Liu S, Wang F. Prevalence of venous thromboembolism in patients with severe novel coronavirus pneumonia. Journal of Thrombosis and Haemostasis 2020;18(6):1421–1424.
  • Brosnahan SB, Smilowitz NR, Amoroso NE, et al. Thrombosis at hospital presentation in patients with and without coronavirus disease 2019. Journal of Vascular Surgery: Venous and Lymphatic Disorders 2021;9(4):845–852.
  • Demelo-Rodríguez P, Cervilla-Muñoz E, Ordieres-Ortega L et al. Incidence of asymptomatic deep vein thrombosis in patients with COVID-19 pneumonia and elevated D-dimer levels. Thrombosis Research 2020;192:23–26.
  • Bosevski M, Krstevski G, Bosevska G, et al. The role of D-dimer in relation to the clinical course of patients with COVID-19. ABBS 2020;53(1):119–120.
  • Valerio L, Ferrazzi P, Sacco C et al. Course of D-Dimer and C-Reactive Protein Levels in Survivors and Nonsurvivors with COVID-19 Pneumonia: A Retrospective Analysis of 577 Patients. Thromb Haemost 2021;121(01):98–101.
  • Eljilany I, Elzouki AN. D-Dimer, Fibrinogen, and IL-6 in COVID-19 Patients with Suspected Venous Thromboembolism: A Narrative Review. VHRM 2020;16:455–462.
  • Bannaga AS, Tabuso M, Farrugia A, et al. C-reactive protein and albumin association with mortality of hospitalised SARS-CoV-2 patients: A tertiary hospital experience. Clin Med 2020;20(5):463–467.
  • Libby P, Lüscher T. COVID-19 is, in the end, an endothelial disease. European Heart Journal 2020;41(32):3038–3044.
  • Pons S, Fodil S, Azoulay E, Zafrani L. The vascular endothelium: the cornerstone of organ dysfunction in severe SARS-CoV-2 infection. Crit Care 2020;24(1):353.
  • Lin GL, McGinley JP, Drysdale SB, Pollard AJ. Epidemiology and Immune Pathogenesis of Viral Sepsis. Front Immunol 2018;9:2147.
  • Kinosian B. Cholesterol and Coronary Heart Disease: Predicting Risks by Levels and Ratios. Ann Intern Med 1994;121(9):641.
  • Gunay S, Sariaydin M, Acay A. New Predictor of Atherosclerosis in Subjects With COPD: Atherogenic Indices. Respir Care 2016;61(11):1481–1487.
  • Sujatha R, Kavitha S. Atherogenic indices in stroke patients: A retrospective study. Iran J Neurol 2017;16(2):78–82.
  • Turgay Yıldırım Ö, Kaya Ş. The atherogenic index of plasma as a predictor of mortality in patients with COVID-19. Heart & Lung 2021;50(2):329–333.
Toplam 36 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Kardiyoloji
Bölüm Araştırma Makaleleri
Yazarlar

Hakan Kilci 0000-0002-2530-919X

Adem Melekoğlu 0000-0002-5764-3678

Güneş Melike Doğan 0000-0002-6989-1011

Mutlu Cagan Sumerkan 0000-0003-1694-0606

Özgür Selim Ser 0000-0002-5232-1100

Ertuğrul Altınbilek 0000-0003-4201-8850

Yayımlanma Tarihi 23 Haziran 2025
Gönderilme Tarihi 17 Aralık 2024
Kabul Tarihi 21 Mayıs 2025
Yayımlandığı Sayı Yıl 2025 Cilt: 7 Sayı: 2

Kaynak Göster

AMA Kilci H, Melekoğlu A, Doğan GM, Sumerkan MC, Ser ÖS, Altınbilek E. Relationship Between Atherogenic Indices and Cardiovascular Thromboembolic Events in Patients with COVID-19 Pneumonia. Hitit Medical Journal. Haziran 2025;7(2):227-234. doi:10.52827/hititmedj.1594744