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Effect of systemic inflammatory response syndrome on ventricular repolarization parameters in COVID-19 patients

Yıl 2025, Cilt: 16 Sayı: 3, 516 - 522, 30.09.2025

Öz

Aim: Malignant ventricular arrhythmia is a significant cause of mortality in COVID-19 patients. We aimed to investigate ventricular repolarization parameters that predict the risk of malignant ventricular arrhythmia in COVID-19 patients who developed systemic inflammatory response syndrome (SIRS).
Material and Methods: Our study included 533 COVID-19 patients, divided into two groups: those who developed SIRS (n=197) and those without SIRS (n=336). ECG measurements were taken for QRS, QT, QTc, Tp-e intervals, Tp-e/QTc, Tp-e/QT, QT/QRS (Index of Cardiac Electrophysiological Balance, İCEB) and QTc/QRS (ICEBc), and these values were compared between groups.
Results: The mean age of the study population was 62 years, and 49% (261) were female. The ICEBc was 5.1 for the SIRS group and 4.98 for the non-SIRS group (p=0.004). The QTc interval was 450 ms in the SIRS group and 427 ms in the non-SIRS group (p=0.001), indicating a substantially higher QTc interval in the SIRS group. Multivariable linear regression analysis revealed a significant correlation between ICEBc and SIRS, age, gender, and C-reactive protein (CRP). ROC analysis showed that ICEBc was a more significant predictor of in-hospital mortality than QTc (ICEBc: 64.5% sensitivity, 50.4% specificity; QTc: 56.4% sensitivity, 53.9% specificity).
Conclusion: ICEBc and QTc were significantly higher in COVID-19 patients with SIRS compared to those without SIRS. ICEBc, known to be related to malignant arrhythmias on ECG in SIRS patients, may aid in predicting and preventing arrhythmic events. Additionally, ICEBc was found to be a better predictor of in-hospital mortality than QTc.

Etik Beyan

The study was approved by the ethics committee of University of Health Sciences Diyarbakır Gazi Yaşargil Education and Research Hospital. 02/07/2021/84).

Kaynakça

  • Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y,et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395(10223):497-506
  • Long B, Brady WJ, Koyfman A, Gottlieb M. Cardiovascular complications in COVID-19. Am J Emerg Med 2020; 38(7):1504-1507
  • Xiong TY, Redwood S, Prendergast B, Chen M. Coronaviruses and the cardiovascular system: acute and long-term implications. Eur Heart J 2020; 41(19):1798-1800
  • Yenerçağ M, Arslan U, Doğduş M, Günal Ö, Öztürk ÇE, Aksan G et al. Evaluation of electrocardiographic ventricular repolarization variables in patients with newly diagnosed COVID-19. J Electrocardiol 2020; 62:5-9.
  • Nafakhi H, Al-Mosawi AA, Alareedh M, Al-Nafakh HA. Index of cardiac electrophysiological balance and transmural dispersion of the repolarization index relationships with pericardial fat volume and coronary calcification. Biomark Med 2018; 12(4):321-328.
  • Mandala S, Di TC. ECG Parameters for Malignant Ventricular Arrhythmias: A Comprehensive Review. J Med Biol Eng 2017; 37(4):441-453.
  • Al-Mosawi AA, Nafakhi H, Hassan MB, Alareedh M, Al-Nafakh HA. ECG markers of arrythmogenic risk relationships with pericardial fat volume and BMI in patients with coronary atherosclerosis. J Electrocardiol 2018; 51(4):569-572.
  • Lu HR, Yan GX, Gallacher DJ. A new biomarker--index of cardiac electrophysiological balance (iCEB)--plays an important role in drug-induced cardiac arrhythmias: beyond QT-prolongation and Torsades de Pointes (TdPs). J Pharmacol Toxicol Methods 2013; 68(2):250-259.
  • Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, et al. Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. JAMA 2020; 323(11):1061-1069.
  • American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference: definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit Care Med 1992; 20(6):864-74.
  • Thygesen K, Alpert JS, Jaffe AS, Chaitman BR, Bax JJ, Morrow DA, et al. Executive Group on behalf of the Joint European Society of Cardiology (ESC)/American College of Cardiology (ACC)/American Heart Association (AHA)/World Heart Federation (WHF) Task Force for the Universal Definition of Myocardial Infarction. Fourth Universal Definition of Myocardial Infarction (2018). J Am Coll Cardiol 2018; 72(18):2231-2264.
  • Shi S, Qin M, Shen B, Cai Y, Liu T, Yang F, et al. Association of Cardiac Injury with Mortality in Hospitalized Patients With COVID-19 in Wuhan, China. JAMA Cardiol 2020; 5(7):802-810.
  • Yang AP, Liu JP, Tao WQ, Li HM. The diagnostic and predictive role of NLR, d-NLR and PLR in COVID-19 patients. Int Immunopharmacol 2020; 84:106504.
  • Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ HLH. Across Speciality Collaboration, UK. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet 2020; 395(10229):1033-1034.
  • Koh HM, Chong PF, Tan JN, Chidambaram SK, Chua HJ. QT prolongation associated with hydroxychloroquine and protease inhibitors in COVID-19. J Clin Pharm Ther 2021; 46(3):800-806.
  • Çap M, Bilge Ö, Işık F, Burak C, Karagöz A, İnci Ü, et al. The effect of favipiravir on QTc interval in patients hospitalized with coronavirus disease 2019. J Electrocardiol 2021; 63:115-119.
  • Lazzerini PE, Capecchi PL, Laghi-Pasini F. Long QT Syndrome: An Emerging Role for Inflammation and Immunity. Front Cardiovasc Med 2015; 2:26
  • Siripanthong B, Nazarian S, Muser D, Deo R, Santangeli P, Khanji MY, et al. Recognizing COVID-19-related myocarditis: The possible pathophysiology and proposed guideline for diagnosis and management. Heart Rhythm 2020; 17(9):1463-1471.
  • Thakore A, Nguyen J, Pollack S, Muehlbauer S, Chi B, Knight D,et al. Electrocardiographic manifestations of COVID-19: Effect on cardiac activation and repolarization. EClinicalMedicine 2021; 39:101057.
  • Özdemir L, Sökmen E. Effect of habitual cigarette smoking on the index of cardiac electrophysiological balance in apparently healthy individuals. J Electrocardiol 2020; 59:41-44.
  • Bacharova L. Missing Link between Molecular Aspects of Ventricular Arrhythmias and QRS Complex Morphology in Left Ventricular Hypertrophy. Int J Mol Sci 2019; 21(1):48.
  • Robyns T, Lu HR, Gallacher DJ, Garweg C, Ector J, Willems R, Janssens S, et al. Evaluation of Index of Cardio-Electrophysiological Balance (iCEB) as a New Biomarker for the Identification of Patients at Increased Arrhythmic Risk. Ann Noninvasive Electrocardiol 2016; 21(3):294-304.
  • Yayla Ç, Bilgin M, Akboğa MK, Gayretli Yayla K, Canpolat U, Dinç Asarcikli L,et al. Evaluation of Tp-E Interval and Tp-E/QT Ratio in Patients with Aortic Stenosis. Ann Noninvasive Electrocardiol 2016; 21(3):287-93.
  • Panikkath R, Reinier K, Uy-Evanado A, Teodorescu C, Hattenhauer J, Mariani R, et al. Prolonged Tpeak-to-tend interval on the resting ECG is associated with increased risk of sudden cardiac death. Circ Arrhythm Electrophysiol 2011; 4(4):441-7.
  • Öztürk F, Karaduman M, Çoldur R, İncecik Ş, Güneş Y, Tuncer M. Interpretation of arrhythmogenic effects of COVID-19 disease through ECG. Aging Male 2020; 23(5):1362-1365.
  • Alareedh M, Nafakhi H, Shaghee F, Nafakhi. A Electrocardiographic markers of increased risk of sudden cardiac death in patients with COVID-19 pneumonia. Ann Noninvasive Electrocardiol 2021; 26(3):e12824.
  • Ibisoglu E, Boyraz B. Comparison of ventricular repolarization parameters of Covid-19 patients diagnosed with chest CT and RT-PCR. Acta Cardiol 2021; 76(9):1013-1018.
  • Shaghee F, Nafakhi H, Alareedh M, Nafakhi A, Al-Buthabhak K. ECG markers of malignant arrhythmias and in-hospital outcome of COVID-19 pneumonia. J Arrhythm 2021; 37(2):426-431.

COVID-19 hastalarında sistemik inflamatuar yanıt sendromunun ventriküler repolarizasyon parametreleri üzerindeki etkisi

Yıl 2025, Cilt: 16 Sayı: 3, 516 - 522, 30.09.2025

Öz

Amaç: Malign ventriküler aritmi, COVID-19 hastalarında önemli bir mortalite nedenidir. Sistemik inflamatuar yanıt sendromu (SIRS) gelişen COVID-19 hastalarında malign ventriküler aritmi riskini öngören ventriküler repolarizasyon parametrelerini araştırmayı amaçladık.
Gereç ve Yöntemler: Çalışmamıza 533 COVID-19 hastası dahil edildi ve hastalar iki gruba ayrıldı: SIRS gelişenler (n=197) ve gelişmeyenler (n=336). QRS, QT, QTc, Tp-e intervalleri, Tp-e/QTc, Tp-e/QT, QT/QRS (Kardiyak Elektrofizyolojik Denge İndeksi, İCEB) ve QTc/QRS (ICEBc) için EKG ölçümleri alındı ve bu değerler gruplar arasında karşılaştırıldı.
Sonuçlar: Çalışma grubunun ortalama yaşı 62 olup, %49'u (261) kadındı. ICEBc, SIRS grubunda 5,1, SIRS olmayan grupta ise 4,98 olarak bulundu (p=0,004). QTc aralığı, SIRS grubunda 450 ms, SIRS olmayan grupta ise 427 ms olarak bulundu (p=0,001). Bu da SIRS grubunda önemli ölçüde daha yüksek bir QTc aralığı olduğunu göstermektedir. Çok değişkenli doğrusal regresyon analizi, ICEBc ile SIRS, yaş, cinsiyet ve C-reaktif protein (CRP) arasında anlamlı bir korelasyon olduğunu ortaya koymuştur. ROC analizi, ICEBc'nin hastane içi mortaliteyi QTc'den daha anlamlı bir öngörücü olduğunu göstermiştir (ICEBc: %64,5 duyarlılık, %50,4 özgüllük; QTc: %56,4 duyarlılık, %53,9 özgüllük).
Sonuç: ICEBc ve QTc, SIRS gelişen COVID-19 hastalarında, SIRS gelişmeyen hastalara kıyasla anlamlı derecede yüksekti. SIRS hastalarında EKG'de malign aritmilerle ilişkili olduğu bilinen ICEBc, aritmik olayların öngörülmesine ve önlenmesine yardımcı olabilir. Ayrıca, ICEBc'nin QTc'den daha iyi bir hastane içi mortalite öngörücüsü olduğu bulunmuştur.

Kaynakça

  • Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y,et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395(10223):497-506
  • Long B, Brady WJ, Koyfman A, Gottlieb M. Cardiovascular complications in COVID-19. Am J Emerg Med 2020; 38(7):1504-1507
  • Xiong TY, Redwood S, Prendergast B, Chen M. Coronaviruses and the cardiovascular system: acute and long-term implications. Eur Heart J 2020; 41(19):1798-1800
  • Yenerçağ M, Arslan U, Doğduş M, Günal Ö, Öztürk ÇE, Aksan G et al. Evaluation of electrocardiographic ventricular repolarization variables in patients with newly diagnosed COVID-19. J Electrocardiol 2020; 62:5-9.
  • Nafakhi H, Al-Mosawi AA, Alareedh M, Al-Nafakh HA. Index of cardiac electrophysiological balance and transmural dispersion of the repolarization index relationships with pericardial fat volume and coronary calcification. Biomark Med 2018; 12(4):321-328.
  • Mandala S, Di TC. ECG Parameters for Malignant Ventricular Arrhythmias: A Comprehensive Review. J Med Biol Eng 2017; 37(4):441-453.
  • Al-Mosawi AA, Nafakhi H, Hassan MB, Alareedh M, Al-Nafakh HA. ECG markers of arrythmogenic risk relationships with pericardial fat volume and BMI in patients with coronary atherosclerosis. J Electrocardiol 2018; 51(4):569-572.
  • Lu HR, Yan GX, Gallacher DJ. A new biomarker--index of cardiac electrophysiological balance (iCEB)--plays an important role in drug-induced cardiac arrhythmias: beyond QT-prolongation and Torsades de Pointes (TdPs). J Pharmacol Toxicol Methods 2013; 68(2):250-259.
  • Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, et al. Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. JAMA 2020; 323(11):1061-1069.
  • American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference: definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit Care Med 1992; 20(6):864-74.
  • Thygesen K, Alpert JS, Jaffe AS, Chaitman BR, Bax JJ, Morrow DA, et al. Executive Group on behalf of the Joint European Society of Cardiology (ESC)/American College of Cardiology (ACC)/American Heart Association (AHA)/World Heart Federation (WHF) Task Force for the Universal Definition of Myocardial Infarction. Fourth Universal Definition of Myocardial Infarction (2018). J Am Coll Cardiol 2018; 72(18):2231-2264.
  • Shi S, Qin M, Shen B, Cai Y, Liu T, Yang F, et al. Association of Cardiac Injury with Mortality in Hospitalized Patients With COVID-19 in Wuhan, China. JAMA Cardiol 2020; 5(7):802-810.
  • Yang AP, Liu JP, Tao WQ, Li HM. The diagnostic and predictive role of NLR, d-NLR and PLR in COVID-19 patients. Int Immunopharmacol 2020; 84:106504.
  • Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ HLH. Across Speciality Collaboration, UK. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet 2020; 395(10229):1033-1034.
  • Koh HM, Chong PF, Tan JN, Chidambaram SK, Chua HJ. QT prolongation associated with hydroxychloroquine and protease inhibitors in COVID-19. J Clin Pharm Ther 2021; 46(3):800-806.
  • Çap M, Bilge Ö, Işık F, Burak C, Karagöz A, İnci Ü, et al. The effect of favipiravir on QTc interval in patients hospitalized with coronavirus disease 2019. J Electrocardiol 2021; 63:115-119.
  • Lazzerini PE, Capecchi PL, Laghi-Pasini F. Long QT Syndrome: An Emerging Role for Inflammation and Immunity. Front Cardiovasc Med 2015; 2:26
  • Siripanthong B, Nazarian S, Muser D, Deo R, Santangeli P, Khanji MY, et al. Recognizing COVID-19-related myocarditis: The possible pathophysiology and proposed guideline for diagnosis and management. Heart Rhythm 2020; 17(9):1463-1471.
  • Thakore A, Nguyen J, Pollack S, Muehlbauer S, Chi B, Knight D,et al. Electrocardiographic manifestations of COVID-19: Effect on cardiac activation and repolarization. EClinicalMedicine 2021; 39:101057.
  • Özdemir L, Sökmen E. Effect of habitual cigarette smoking on the index of cardiac electrophysiological balance in apparently healthy individuals. J Electrocardiol 2020; 59:41-44.
  • Bacharova L. Missing Link between Molecular Aspects of Ventricular Arrhythmias and QRS Complex Morphology in Left Ventricular Hypertrophy. Int J Mol Sci 2019; 21(1):48.
  • Robyns T, Lu HR, Gallacher DJ, Garweg C, Ector J, Willems R, Janssens S, et al. Evaluation of Index of Cardio-Electrophysiological Balance (iCEB) as a New Biomarker for the Identification of Patients at Increased Arrhythmic Risk. Ann Noninvasive Electrocardiol 2016; 21(3):294-304.
  • Yayla Ç, Bilgin M, Akboğa MK, Gayretli Yayla K, Canpolat U, Dinç Asarcikli L,et al. Evaluation of Tp-E Interval and Tp-E/QT Ratio in Patients with Aortic Stenosis. Ann Noninvasive Electrocardiol 2016; 21(3):287-93.
  • Panikkath R, Reinier K, Uy-Evanado A, Teodorescu C, Hattenhauer J, Mariani R, et al. Prolonged Tpeak-to-tend interval on the resting ECG is associated with increased risk of sudden cardiac death. Circ Arrhythm Electrophysiol 2011; 4(4):441-7.
  • Öztürk F, Karaduman M, Çoldur R, İncecik Ş, Güneş Y, Tuncer M. Interpretation of arrhythmogenic effects of COVID-19 disease through ECG. Aging Male 2020; 23(5):1362-1365.
  • Alareedh M, Nafakhi H, Shaghee F, Nafakhi. A Electrocardiographic markers of increased risk of sudden cardiac death in patients with COVID-19 pneumonia. Ann Noninvasive Electrocardiol 2021; 26(3):e12824.
  • Ibisoglu E, Boyraz B. Comparison of ventricular repolarization parameters of Covid-19 patients diagnosed with chest CT and RT-PCR. Acta Cardiol 2021; 76(9):1013-1018.
  • Shaghee F, Nafakhi H, Alareedh M, Nafakhi A, Al-Buthabhak K. ECG markers of malignant arrhythmias and in-hospital outcome of COVID-19 pneumonia. J Arrhythm 2021; 37(2):426-431.
Toplam 28 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Kardiyoloji
Bölüm Araştırma Makalesi
Yazarlar

Önder Bilge 0000-0002-4896-6000

Halil Akın 0000-0002-6651-7403

Ercan Taştan 0000-0002-4896-6993

Murat Çap 0000-0002-4896-6901

Ferhat Işık 0000-0002-4896-6902

Metin Okşul 0000-0002-4896-6903

Şafak Kaya 0000-0002-4896-6904

Burhan Aslan 0000-0002-4896-6905

Emrah Erdoğan 0000-0002-4896-6906

Mehmet Zülkif Karahan 0000-0002-4896-6910

Yayımlanma Tarihi 30 Eylül 2025
Gönderilme Tarihi 17 Haziran 2025
Kabul Tarihi 9 Eylül 2025
Yayımlandığı Sayı Yıl 2025 Cilt: 16 Sayı: 3

Kaynak Göster

APA Bilge, Ö., Akın, H., Taştan, E., … Çap, M. (2025). Effect of systemic inflammatory response syndrome on ventricular repolarization parameters in COVID-19 patients. Turkish Journal of Clinics and Laboratory, 16(3), 516-522. https://doi.org/10.18663/tjcl.1721505
AMA Bilge Ö, Akın H, Taştan E, vd. Effect of systemic inflammatory response syndrome on ventricular repolarization parameters in COVID-19 patients. TJCL. Eylül 2025;16(3):516-522. doi:10.18663/tjcl.1721505
Chicago Bilge, Önder, Halil Akın, Ercan Taştan, Murat Çap, Ferhat Işık, Metin Okşul, Şafak Kaya, Burhan Aslan, Emrah Erdoğan, ve Mehmet Zülkif Karahan. “Effect of systemic inflammatory response syndrome on ventricular repolarization parameters in COVID-19 patients”. Turkish Journal of Clinics and Laboratory 16, sy. 3 (Eylül 2025): 516-22. https://doi.org/10.18663/tjcl.1721505.
EndNote Bilge Ö, Akın H, Taştan E, Çap M, Işık F, Okşul M, Kaya Ş, Aslan B, Erdoğan E, Karahan MZ (01 Eylül 2025) Effect of systemic inflammatory response syndrome on ventricular repolarization parameters in COVID-19 patients. Turkish Journal of Clinics and Laboratory 16 3 516–522.
IEEE Ö. Bilge vd., “Effect of systemic inflammatory response syndrome on ventricular repolarization parameters in COVID-19 patients”, TJCL, c. 16, sy. 3, ss. 516–522, 2025, doi: 10.18663/tjcl.1721505.
ISNAD Bilge, Önder vd. “Effect of systemic inflammatory response syndrome on ventricular repolarization parameters in COVID-19 patients”. Turkish Journal of Clinics and Laboratory 16/3 (Eylül2025), 516-522. https://doi.org/10.18663/tjcl.1721505.
JAMA Bilge Ö, Akın H, Taştan E, Çap M, Işık F, Okşul M, Kaya Ş, Aslan B, Erdoğan E, Karahan MZ. Effect of systemic inflammatory response syndrome on ventricular repolarization parameters in COVID-19 patients. TJCL. 2025;16:516–522.
MLA Bilge, Önder vd. “Effect of systemic inflammatory response syndrome on ventricular repolarization parameters in COVID-19 patients”. Turkish Journal of Clinics and Laboratory, c. 16, sy. 3, 2025, ss. 516-22, doi:10.18663/tjcl.1721505.
Vancouver Bilge Ö, Akın H, Taştan E, Çap M, Işık F, Okşul M, vd. Effect of systemic inflammatory response syndrome on ventricular repolarization parameters in COVID-19 patients. TJCL. 2025;16(3):516-22.


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