The Impact of Severe COVID-19 on Plasma Antioxidants
Abstract
:1. Introduction
2. Results
3. Discussion
4. Materials and Methods
4.1. Samples Collection
4.2. Methods
4.2.1. Antioxidant Parameters
Determination of Protein Antioxidants
Determination of Low Molecular Antioxidants
4.2.2. Lipid Peroxidation Products Determination
4.2.3. Determination of Protein Oxidative Modifications
4.3. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Sample Availability
References
- Trachootham, D.; Lu, W.; Ogasawara, M.A.; Nilsa, R.-D.V.; Huang, P. Redox Regulation of Cell Survival. Antioxid. Redox Signal. 2008, 10, 1343–1374. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lim, J.K.M.; Leprivier, G. The Impact of Oncogenic RAS on Redox Balance and Implications for Cancer Development. Cell Death Dis. 2019, 10, 955. [Google Scholar] [CrossRef] [PubMed]
- Lee, B.W.L.; Ghode, P.; Ong, D.S.T. Redox Regulation of Cell State and Fate. Redox Biol. 2019, 25, 101056. [Google Scholar] [CrossRef] [PubMed]
- Miyazawa, T.; Burdeos, G.C.; Itaya, M.; Nakagawa, K.; Miyazawa, T. Vitamin E: Regulatory Redox Interactions. IUBMB Life 2019, 71, 430–441. [Google Scholar] [CrossRef] [PubMed]
- Lingappan, K. NF-ΚB in Oxidative Stress. Curr. Opin. Toxicol. 2018, 7, 81–86. [Google Scholar] [CrossRef] [PubMed]
- Griffiths, H.R.; Gao, D.; Pararasa, C. Redox Regulation in Metabolic Programming and Inflammation. Redox Biol. 2017, 12, 50–57. [Google Scholar] [CrossRef] [PubMed]
- Ivanov, A.V.; Bartosch, B.; Isaguliants, M.G. Oxidative Stress in Infection and Consequent Disease. Oxidative Med. Cell. Longev. 2017, 2017, e3496043. [Google Scholar] [CrossRef]
- Pohanka, M. Role of Oxidative Stress in Infectious Diseases. A Review. Folia Microbiol. 2013, 58, 503–513. [Google Scholar] [CrossRef]
- Novaes, R.D.; Teixeira, A.L.; de Miranda, A.S. Oxidative Stress in Microbial Diseases: Pathogen, Host, and Therapeutics. Oxidative Med. Cell. Longev. 2019, 2019, e8159562. [Google Scholar] [CrossRef]
- Belikov, A.V.; Schraven, B.; Simeoni, L. T Cells and Reactive Oxygen Species. J. Biomed Sci. 2015, 22, 85. [Google Scholar] [CrossRef] [Green Version]
- Komaravelli, N.; Casola, A. Respiratory Viral Infections and Subversion of Cellular Antioxidant Defenses. J. Pharm. Pharm. 2014, 5, 1000141. [Google Scholar] [CrossRef]
- Shastri, M.D.; Shukla, S.D.; Chong, W.C.; Dua, K.; Peterson, G.M.; Patel, R.P.; Hansbro, P.M.; Eri, R.; O’Toole, R.F. Role of Oxidative Stress in the Pathology and Management of Human Tuberculosis. Oxidative Med. Cell. Longev. 2018, 2018, e7695364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ebrahimi, M.; Norouzi, P.; Aazami, H.; Moosavi-Movahedi, A.A. Review on Oxidative Stress Relation on COVID-19: Biomolecular and Bioanalytical Approach. Int. J. Biol. Macromol. 2021, 189, 802–818. [Google Scholar] [CrossRef] [PubMed]
- Karkhanei, B.; Talebi Ghane, E.; Mehri, F. Evaluation of Oxidative Stress Level: Total Antioxidant Capacity, Total Oxidant Status and Glutathione Activity in Patients with COVID-19. New Microbes New Infect. 2021, 42, 100897. [Google Scholar] [CrossRef] [PubMed]
- Laforge, M.; Elbim, C.; Frère, C.; Hémadi, M.; Massaad, C.; Nuss, P.; Benoliel, J.-J.; Becker, C. Tissue Damage from Neutrophil-Induced Oxidative Stress in COVID-19. Nat. Rev. Immunol. 2020, 20, 515–516. [Google Scholar] [CrossRef] [PubMed]
- Darenskaya, M.A.; Kolesnikova, L.I.; Kolesnikov, S. Free Radical Reactions in Socially Significant Infectious Diseases: HIV Infection, Hepatitis, Tuberculosis. Ann. Russ. Acad. Med. Sci. 2020, 75, 196–203. [Google Scholar] [CrossRef]
- Zarkovic, N.; Jakovcevic, A.; Mataic, A.; Jaganjac, M.; Vukovic, T.; Waeg, G.; Zarkovic, K. Post-Mortem Findings of Inflammatory Cells and the Association of 4-Hydroxynonenal with Systemic Vascular and Oxidative Stress in Lethal COVID-19. Cells 2022, 11, 444. [Google Scholar] [CrossRef]
- Solis-Paredes, J.M.; Montoya-Estrada, A.; Cruz-Rico, A.; Reyes-Muñoz, E.; Perez-Duran, J.; Espino Y Sosa, S.; Garcia-Salgado, V.R.; Sevilla-Montoya, R.; Martinez-Portilla, R.J.; Estrada-Gutierrez, G.; et al. Plasma Total Antioxidant Capacity and Carbonylated Proteins Are Increased in Pregnant Women with Severe COVID-19. Viruses 2022, 14, 723. [Google Scholar] [CrossRef]
- Chen, Z.; Tian, R.; She, Z.; Cai, J.; Li, H. Role of Oxidative Stress in the Pathogenesis of Nonalcoholic Fatty Liver Disease. Free Radic. Biol. Med. 2020, 152, 116–141. [Google Scholar] [CrossRef]
- Ayala, A.; Muñoz, M.F.; Argüelles, S. Lipid Peroxidation: Production, Metabolism, and Signaling Mechanisms of Malondialdehyde and 4-Hydroxy-2-Nonenal. Oxidative Med. Cell. Longev. 2014, 2014, 360438. [Google Scholar] [CrossRef]
- Łuczaj, W.; Gęgotek, A.; Skrzydlewska, E. Antioxidants and HNE in Redox Homeostasis. Free Radic. Biol. Med. 2017, 111, 87–101. [Google Scholar] [CrossRef] [PubMed]
- Žarković, N.; Orehovec, B.; Milković, L.; Baršić, B.; Tatzber, F.; Wonisch, W.; Tarle, M.; Kmet, M.; Mataić, A.; Jakovčević, A.; et al. Preliminary Findings on the Association of the Lipid Peroxidation Product 4-Hydroxynonenal with the Lethal Outcome of Aggressive COVID-19. Antioxidants 2021, 10, 1341. [Google Scholar] [CrossRef] [PubMed]
- Völlmy, F.; van den Toorn, H.; Zenezini Chiozzi, R.; Zucchetti, O.; Papi, A.; Volta, C.A.; Marracino, L.; Vieceli Dalla Sega, F.; Fortini, F.; Demichev, V.; et al. A Serum Proteome Signature to Predict Mortality in Severe COVID-19 Patients. Life Sci. Alliance 2021, 4, e202101099. [Google Scholar] [CrossRef] [PubMed]
- Fernandes, I.G.; de Brito, C.A.; Dos Reis, V.M.S.; Sato, M.N.; Pereira, N.Z. SARS-CoV-2 and Other Respiratory Viruses: What Does Oxidative Stress Have to Do with It? Oxidative Med. Cell. Longev. 2020, 2020, 8844280. [Google Scholar] [CrossRef]
- Mullen, L.; Mengozzi, M.; Hanschmann, E.-M.; Alberts, B.; Ghezzi, P. How the Redox State Regulates Immunity. Free Radic. Biol. Med. 2020, 157, 3–14. [Google Scholar] [CrossRef]
- Koo, S.-J.; Garg, N.J. Metabolic Programming of Macrophage Functions and Pathogens Control. Redox Biol. 2019, 24, 101198. [Google Scholar] [CrossRef]
- Violi, F.; Pastori, D.; Pignatelli, P.; Cangemi, R. SARS-CoV-2 and Myocardial Injury: A Role for Nox2? Intern. Emerg. Med. 2020, 15, 755–758. [Google Scholar] [CrossRef]
- Wu, H.; Wang, Y.; Zhang, Y.; Xu, F.; Chen, J.; Duan, L.; Zhang, T.; Wang, J.; Zhang, F. Breaking the Vicious Loop between Inflammation, Oxidative Stress and Coagulation, a Novel Anti-Thrombus Insight of Nattokinase by Inhibiting LPS-Induced Inflammation and Oxidative Stress. Redox Biol. 2020, 32, 101500. [Google Scholar] [CrossRef]
- Anca, P.S.; Toth, P.P.; Kempler, P.; Rizzo, M. Gender Differences in the Battle against COVID-19: Impact of Genetics, Comorbidities, Inflammation and Lifestyle on Differences in Outcomes. Int. J. Clin. Pract. 2021, 75, e13666. [Google Scholar] [CrossRef]
- Jevtic, S.D.; Nazy, I. The COVID Complex: A Review of Platelet Activation and Immune Complexes in COVID-19. Front. Immunol. 2022, 13, 807934. [Google Scholar] [CrossRef]
- Pennathur, S.; Heinecke, J.W. Oxidative Stress and Endothelial Dysfunction in Vascular Disease. Curr. Diabetes Rep. 2007, 7, 257–264. [Google Scholar] [CrossRef] [PubMed]
- Libby, P.; Lüscher, T. COVID-19 Is, in the End, an Endothelial Disease. Eur. Heart J. 2020, 41, 3038–3044. [Google Scholar] [CrossRef] [PubMed]
- Spadaro, S.; Fogagnolo, A.; Campo, G.; Zucchetti, O.; Verri, M.; Ottaviani, I.; Tunstall, T.; Grasso, S.; Scaramuzzo, V.; Murgolo, F.; et al. Markers of Endothelial and Epithelial Pulmonary Injury in Mechanically Ventilated COVID-19 ICU Patients. Crit. Care 2021, 25, 74. [Google Scholar] [CrossRef] [PubMed]
- Vieceli Dalla Sega, F.; Fortini, F.; Spadaro, S.; Ronzoni, L.; Zucchetti, O.; Manfrini, M.; Mikus, E.; Fogagnolo, A.; Torsani, F.; Pavasini, R.; et al. Time Course of Endothelial Dysfunction Markers and Mortality in COVID-19 Patients: A Pilot Study. Clin. Transl. Med. 2021, 11, e283. [Google Scholar] [CrossRef]
- Zhou, F.; Yu, T.; Du, R.; Fan, G.; Liu, Y.; Liu, Z.; Xiang, J.; Wang, Y.; Song, B.; Gu, X.; et al. Clinical Course and Risk Factors for Mortality of Adult Inpatients with COVID-19 in Wuhan, China: A Retrospective Cohort Study. Lancet 2020, 395, 1054–1062. [Google Scholar] [CrossRef]
- Jastrząb, A.; Skrzydlewska, E. Thioredoxin-Dependent System. Application of Inhibitors. J. Enzym. Inhib. Med. Chem. 2021, 36, 362–371. [Google Scholar] [CrossRef]
- Polonikov, A. Endogenous Deficiency of Glutathione as the Most Likely Cause of Serious Manifestations and Death in COVID-19 Patients. ACS Infect. Dis. 2020, 6, 1558–1562. [Google Scholar] [CrossRef]
- Derouiche, S. Oxidative Stress Associated with SARS-Cov-2 (COVID-19) Increases the Severity of the Lung Disease—A Systematic Review. J. Infect. Dis. Epidemiol. 2020, 6, 121. [Google Scholar] [CrossRef]
- Çakırca, G.; Çakırca, T.D.; Üstünel, M.; Torun, A.; Koyuncu, İ. Thiol Level and Total Oxidant/Antioxidant Status in Patients with COVID-19 Infection. Ir. J. Med. Sci. 2021, 191, 1925–1930. [Google Scholar] [CrossRef]
- Murata, Y.; Ohteki, T.; Koyasu, S.; Hamuro, J. IFN-Gamma and pro-Inflammatory Cytokine Production by Antigen-Presenting Cells Is Dictated by Intracellular Thiol Redox Status Regulated by Oxygen Tension. Eur. J. Immunol. 2002, 32, 2866–2873. [Google Scholar] [CrossRef]
- Contoli, M.; Papi, A.; Tomassetti, L.; Rizzo, P.; Vieceli Dalla Sega, F.; Fortini, F.; Torsani, F.; Morandi, L.; Ronzoni, L.; Zucchetti, O.; et al. Blood Interferon-α Levels and Severity, Outcomes, and Inflammatory Profiles in Hospitalized COVID-19 Patients. Front. Immunol. 2021, 12, 648004. [Google Scholar] [CrossRef] [PubMed]
- Amatore, D.; Sgarbanti, R.; Aquilano, K.; Baldelli, S.; Limongi, D.; Civitelli, L.; Nencioni, L.; Garaci, E.; Ciriolo, M.R.; Palamara, A.T. Influenza Virus Replication in Lung Epithelial Cells Depends on Redox-Sensitive Pathways Activated by NOX4-Derived ROS. Cell. Microbiol. 2015, 17, 131–145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schwartz, S.L.; Conn, G.L. RNA Regulation of the Antiviral Protein 2′-5′-Oligoadenylate Synthetase. WIREs RNA 2019, 10, e1534. [Google Scholar] [CrossRef]
- Busnadiego, I.; Kane, M.; Rihn, S.J.; Preugschas, H.F.; Hughes, J.; Blanco-Melo, D.; Strouvelle, V.P.; Zang, T.M.; Willett, B.J.; Boutell, C.; et al. Host and Viral Determinants of Mx2 Antiretroviral Activity. J. Virol. 2014, 88, 7738–7752. [Google Scholar] [CrossRef] [Green Version]
- Murata, Y.; Shimamura, T.; Tagami, T.; Takatsuki, F.; Hamuro, J. The Skewing to Th1 Induced by Lentinan Is Directed through the Distinctive Cytokine Production by Macrophages with Elevated Intracellular Glutathione Content. Int. Immunopharmacol. 2002, 2, 673–689. [Google Scholar] [CrossRef]
- Fraternale, A.; Zara, C.; De Angelis, M.; Nencioni, L.; Palamara, A.T.; Retini, M.; Di Mambro, T.; Magnani, M.; Crinelli, R. Intracellular Redox-Modulated Pathways as Targets for Effective Approaches in the Treatment of Viral Infection. Int. J. Mol. Sci. 2021, 22, 3603. [Google Scholar] [CrossRef]
- Khomich, O.A.; Kochetkov, S.N.; Bartosch, B.; Ivanov, A.V. Redox Biology of Respiratory Viral Infections. Viruses 2018, 10, 392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Muhammad, Y.; Aminu, Y.K.; Ahmad, A.E.; Iliya, S.; Muhd, N.; Yahaya, M.; Mustapha, A.S.; Tahiru, A.; Abdulkadir, S.S.; Ibrahim, J.S.; et al. An Elevated 8-Isoprostaglandin F2 Alpha (8-Iso-PGF2α) in COVID-19 Subjects Co-Infected with Malaria. Pan. Afr. Med. J. 2020, 37, 78. [Google Scholar] [CrossRef] [PubMed]
- Ye, Z.-W.; Zhang, J.; Townsend, D.M.; Tew, K.D. Oxidative Stress, Redox Regulation and Diseases of Cellular Differentiation. Biochim. Biophys. Acta Gen. Subj. 2015, 1850, 1607–1621. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pincemail, J.; Cavalier, E.; Charlier, C.; Cheramy–Bien, J.-P.; Brevers, E.; Courtois, A.; Fadeur, M.; Meziane, S.; Goff, C.L.; Misset, B.; et al. Oxidative Stress Status in COVID-19 Patients Hospitalized in Intensive Care Unit for Severe Pneumonia. A Pilot Study. Antioxidants 2021, 10, 257. [Google Scholar] [CrossRef]
- Martín-Fernández, M.; Aller, R.; Heredia-Rodríguez, M.; Gómez-Sánchez, E.; Martínez-Paz, P.; Gonzalo-Benito, H.; Sánchez-de Prada, L.; Gorgojo, Ó.; Carnicero-Frutos, I.; Tamayo, E.; et al. Lipid Peroxidation as a Hallmark of Severity in COVID-19 Patients. Redox Biol. 2021, 48, 102181. [Google Scholar] [CrossRef] [PubMed]
- Bekyarova, G.; Tzaneva, M.; Bratoeva, K.; Ivanova, I.; Kotzev, A.; Hristova, M.; Krastev, D.; Kindekov, I.; Mileva, M. 4-Hydroxynonenal (HNE) and Hepatic Injury Related to Chronic Oxidative Stress. Biotechnol. Biotechnol. Equip. 2019, 33, 1544–1552. [Google Scholar] [CrossRef] [Green Version]
- van den Brand, J.M.A.; Haagmans, B.L.; van Riel, D.; Osterhaus, A.D.M.E.; Kuiken, T. The Pathology and Pathogenesis of Experimental Severe Acute Respiratory Syndrome and Influenza in Animal Models. J. Comp. Pathol. 2014, 151, 83–112. [Google Scholar] [CrossRef] [Green Version]
- Kelleher, Z.T.; Sha, Y.; Foster, M.W.; Foster, W.M.; Forrester, M.T.; Marshall, H.E. Thioredoxin-Mediated Denitrosylation Regulates Cytokine-Induced Nuclear Factor ΚB (NF-ΚB) Activation. J. Biol. Chem. 2014, 289, 3066–3072. [Google Scholar] [CrossRef] [Green Version]
- Cuadrado, A.; Rojo, A.I.; Wells, G.; Hayes, J.D.; Cousin, S.P.; Rumsey, W.L.; Attucks, O.C.; Franklin, S.; Levonen, A.-L.; Kensler, T.W.; et al. Therapeutic Targeting of the NRF2 and KEAP1 Partnership in Chronic Diseases. Nat. Rev. Drug Discov. 2019, 18, 295–317. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yaghoubi, N.; Youssefi, M.; Hashemy, S.I.; Rafat Panah, H.; Mashkani, B.A.; Zahedi Avval, F. Thioredoxin Reductase Gene Expression and Activity among Human T-Cell Lymphotropic Virus Type 1-Infected Patients. J. Med. Virol. 2019, 91, 865–871. [Google Scholar] [CrossRef] [PubMed]
- Chung, Y.; Zhang, N.; Wooten, R.M. Borrelia Burgdorferi Elicited-IL-10 Suppresses the Production of Inflammatory Mediators, Phagocytosis, and Expression of Co-Stimulatory Receptors by Murine Macrophages and/or Dendritic Cells. PLoS ONE 2013, 8, e84980. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stoian, A.P.; Banerjee, Y.; Rizvi, A.A.; Rizzo, M. Diabetes and the COVID-19 Pandemic: How Insights from Recent Experience Might Guide Future Management. Metab. Syndr. Relat. Disord. 2020, 18, 173–175. [Google Scholar] [CrossRef]
- Zhang, P.; Li, T.; Wu, X.; Nice, E.C.; Huang, C.; Zhang, Y. Oxidative Stress and Diabetes: Antioxidative Strategies. Front. Med. 2020, 14, 583–600. [Google Scholar] [CrossRef]
- Paglia, D.E.; Valentine, W.N. Studies on the Quantitative and Qualitative Characterization of Erythrocyte Glutathione Peroxidase. J. Lab Clin. Med. 1967, 70, 158–169. [Google Scholar]
- Mize, C.E.; Langdon, R.G. Hepatic Glutathione Reductase. I. Purification and General Kinetic Properties. J. Biol. Chem. 1962, 237, 1589–1595. [Google Scholar] [CrossRef]
- Lovell, M.A.; Xie, C.; Gabbita, S.P.; Markesbery, W.R. Decreased Thioredoxin and Increased Thioredoxin Reductase Levels in Alzheimer’s Disease Brain. Free Radic. Biol. Med. 2000, 28, 418–427. [Google Scholar] [CrossRef]
- Holmgren, A.; Björnstedt, M. Thioredoxin and Thioredoxin Reductase. In Methods in Enzymology; Academic Press: Cambridge, MA, USA, 1995; Volume 252, pp. 199–208. [Google Scholar] [CrossRef]
- Sykes, J.A.; McCormack, F.X.; O’Brien, T.J. A Preliminary Study of the Superoxide Dismutase Content of Some Human Tumors. Cancer Res. 1978, 38, 2759–2762. [Google Scholar] [PubMed]
- Geller, B.L.; Winge, D.R. A Method for Distinguishing Cu,Zn- and Mn-Containing Superoxide Dismutases. Anal. Biochem. 1983, 128, 86–92. [Google Scholar] [CrossRef]
- Maeso, N.; García-Martínez, D.; Rupérez, F.J.; Cifuentes, A.; Barbas, C. Capillary Electrophoresis of Glutathione to Monitor Oxidative Stress and Response to Antioxidant Treatments in an Animal Model. J. Chromatogr. B 2005, 822, 61–69. [Google Scholar] [CrossRef]
- Vatassery, G.T.; Brin, M.F.; Fahn, S.; Kayden, H.J.; Traber, M.G. Effect of High Doses of Dietary Vitamin E on the Concentrations of Vitamin E in Several Brain Regions, Plasma, Liver, and Adipose Tissue of Rats. J. Neurochem. 1988, 51, 621–623. [Google Scholar] [CrossRef]
- Ivanović, D.; Popović, A.; Radulović, D.; Medenica, M. Reversed-Phase Ion-Pair HPLC Determination of Some Water-Soluble Vitamins in Pharmaceuticals. J. Pharm. Biomed. Anal. 1999, 18, 999–1004. [Google Scholar] [CrossRef]
- Tsikas, D.; Rothmann, S.; Schneider, J.Y.; Gutzki, F.-M.; Beckmann, B.; Frölich, J.C. Simultaneous GC-MS/MS Measurement of Malondialdehyde and 4-Hydroxy-2-Nonenal in Human Plasma: Effects of Long-Term L-Arginine Administration. Anal. Biochem. 2017, 524, 31–44. [Google Scholar] [CrossRef]
- Coolen, S.A.J.; van Buuren, B.; Duchateau, G.; Upritchard, J.; Verhagen, H. Kinetics of Biomarkers: Biological and Technical Validity of Isoprostanes in Plasma. Amino Acids 2005, 29, 429–436. [Google Scholar] [CrossRef]
- Dupuy, A.; Le Faouder, P.; Vigor, C.; Oger, C.; Galano, J.-M.; Dray, C.; Lee, J.C.-Y.; Valet, P.; Gladine, C.; Durand, T.; et al. Simultaneous Quantitative Profiling of 20 Isoprostanoids from Omega-3 and Omega-6 Polyunsaturated Fatty Acids by LC-MS/MS in Various Biological Samples. Anal. Chim. Acta 2016, 921, 46–58. [Google Scholar] [CrossRef] [Green Version]
- Weber, D.; Milkovic, L.; Bennett, S.J.; Griffiths, H.R.; Zarkovic, N.; Grune, T. Measurement of HNE-Protein Adducts in Human Plasma and Serum by ELISA-Comparison of Two Primary Antibodies. Redox Biol. 2013, 1, 226–233. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Levine, R.L.; Garland, D.; Oliver, C.N.; Amici, A.; Climent, I.; Lenz, A.G.; Ahn, B.W.; Shaltiel, S.; Stadtman, E.R. Determination of Carbonyl Content in Oxidatively Modified Proteins. Methods Enzymol. 1990, 186, 464–478. [Google Scholar] [CrossRef] [PubMed]
- Pang, Z.; Zhou, G.; Ewald, J.; Chang, L.; Hacariz, O.; Basu, N.; Xia, J. Using MetaboAnalyst 5.0 for LC–HRMS Spectra Processing, Multi-Omics Integration and Covariate Adjustment of Global Metabolomics Data. Nat. Protoc. 2022, 17, 1735–1761. [Google Scholar] [CrossRef] [PubMed]
Healthy Control | COVID-19 Recovered | COVID-19 Deceased | |
---|---|---|---|
Age (years) | 38.5 ± 9.3 | 65.4 ± 8.1 a | 75.7 ± 7.6 a,b |
Sex | 22F 11M | 21F 45M | 11F 11M |
Body Mass Index | 26.8 ± 4.4 | 28.5 ± 3.4 | 27.1 ± 6.8 |
Normal Range | COVID-19 Recovered | COVID-19 Deceased | |
---|---|---|---|
WBC [103/μL] Neutrophils [%] Platelets [103/μL] | 4.00–10.00 40.0–72.0 150–400 | 10.15 ± 3.27 80.67 ± 7.71 255.97 ± 93.21 | 10.86 ± 3.64 84.82 ± 5.87 * 199.35 ± 52.78 * |
Blood oxygen saturation [%] | >95% | 92.49 ± 3.47 | 87.13 ± 8.43 * |
Ferritin [μg/L] | 11–336 | 959 ± 573 | 1007 ± 486 |
PCT [ng/mL] | <0.1 | 0.58 ± 0.7 | 1.71 ± 1.87 |
LDH [U/L] | 140–280 | 355 ± 147 | 456 ± 224 |
CRP [mg/L] | 0.00–5.00 | 114.51 ± 61.88 | 172.06 ± 71.23 * |
IL-6 [pg/mL] | 0–43.5 | 125 ± 107 | 266 ± 179 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Žarković, N.; Jastrząb, A.; Jarocka-Karpowicz, I.; Orehovec, B.; Baršić, B.; Tarle, M.; Kmet, M.; Lukšić, I.; Łuczaj, W.; Skrzydlewska, E. The Impact of Severe COVID-19 on Plasma Antioxidants. Molecules 2022, 27, 5323. https://doi.org/10.3390/molecules27165323
Žarković N, Jastrząb A, Jarocka-Karpowicz I, Orehovec B, Baršić B, Tarle M, Kmet M, Lukšić I, Łuczaj W, Skrzydlewska E. The Impact of Severe COVID-19 on Plasma Antioxidants. Molecules. 2022; 27(16):5323. https://doi.org/10.3390/molecules27165323
Chicago/Turabian StyleŽarković, Neven, Anna Jastrząb, Iwona Jarocka-Karpowicz, Biserka Orehovec, Bruno Baršić, Marko Tarle, Marta Kmet, Ivica Lukšić, Wojciech Łuczaj, and Elżbieta Skrzydlewska. 2022. "The Impact of Severe COVID-19 on Plasma Antioxidants" Molecules 27, no. 16: 5323. https://doi.org/10.3390/molecules27165323
APA StyleŽarković, N., Jastrząb, A., Jarocka-Karpowicz, I., Orehovec, B., Baršić, B., Tarle, M., Kmet, M., Lukšić, I., Łuczaj, W., & Skrzydlewska, E. (2022). The Impact of Severe COVID-19 on Plasma Antioxidants. Molecules, 27(16), 5323. https://doi.org/10.3390/molecules27165323