Free Radicals, Mitochondrial Dysfunction and Sepsis-induced Organ Dysfunction: A Mechanistic Insight


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Abstract

Sepsis is a complex clinical condition and a leading cause of death worldwide. During Sepsis, there is a derailment in the host response to infection, which can progress to severe sepsis and multiple organ dysfunction or failure, which leads to death. Free radicals, including reactive oxygen species (ROS) generated predominantly in mitochondria, are one of the key players in impairing normal organ function in sepsis. ROS contributing to oxidative stress has been reported to be the main culprit in the injury of the lung, heart, liver, kidney, gastrointestinal, and other organs. Here in the present review, we describe the generation, and essential properties of various types of ROS, their effect on macromolecules, and their role in mitochondrial dysfunction. Furthermore, the mechanism involved in the ROS-mediated pathogenesis of sepsis-induced organ dysfunction has also been discussed.

About the authors

Sanni Kumar

Department of Biotechnology Engineering and Food Technology, University Institute of Engineering, Chandigarh University

Email: info@benthamscience.net

Vijay Kumar Srivastava

Amity Institute of Biotechnology, Amity University

Email: info@benthamscience.net

Sanket Kaushik

Amity Institute of Biotechnology, Amity University

Email: info@benthamscience.net

Juhi Saxena

Department of Biotechnology, Parul Institute of Technology, Parul University

Email: info@benthamscience.net

Anupam Jyoti

Department of Life Sciences, Parul Institute of Applied Sciences, Parul University

Author for correspondence.
Email: info@benthamscience.net

References

  1. Gomberg M. An instance of trivalent carbon: Triphenylmethyl. J Am Chem Soc 1900; 22(11): 757-71. doi: 10.1021/ja02049a006
  2. Gerschman R, Gilbert D, Nye SW, Dwyer P, Fenn WO. Oxygen poisoning and X-irradiation: A mechanism in common. 1954. Nutrition 2001; 17(2): 162. PMID: 11683139
  3. Commoner B, Townsend J, Pake G. Free radicals in biological materials. Nature 1954; 174(4432): 689-91. doi: 10.1038/174689a0 PMID: 13213980
  4. Harman D. The aging process. Proc Natl Acad Sci 1981; 78(11): 7124-8. doi: 10.1073/pnas.78.11.7124 PMID: 6947277
  5. McCord JM, Roy RS, Schaffer SW. Free radicals and myocardial ischemia. The role of xanthine oxidase. Adv Myocardiol 1985; 5: 183-9. doi: 10.1007/978-1-4757-1287-2_14 PMID: 2982206
  6. Loschen G, Flohé L, Chance B. Respiratory chain linked H2O2 production in pigeon heart mitochondria. FEBS Lett 1971; 18(2): 261-4. doi: 10.1016/0014-5793(71)80459-3 PMID: 11946135
  7. Mittal CK, Murad F. Activation of guanylate cyclase by superoxide dismutase and hydroxyl radical: A physiological regulator of guanosine 3′,5′-monophosphate formation. Proc Natl Acad Sci 1977; 74(10): 4360-4. doi: 10.1073/pnas.74.10.4360 PMID: 22077
  8. Nohl H, Hegner D. Do mitochondria produce oxygen radicals in vivo? Eur J Biochem 1978; 82(2): 563-7. doi: 10.1111/j.1432-1033.1978.tb12051.x PMID: 203456
  9. Bergendi L, Beneš L, Ďuračková Z, Ferenčik M. Chemistry, physiology and pathology of free radicals. Life Sci 1999; 65(18-19): 1865-74. doi: 10.1016/S0024-3205(99)00439-7 PMID: 10576429
  10. Phaniendra A, Jestadi DB, Periyasamy L. Free radicals: Properties, sources, targets, and their implication in various diseases. Indian J Clin Biochem 2015; 30(1): 11-26. doi: 10.1007/s12291-014-0446-0 PMID: 25646037
  11. Lobo V, Patil A, Phatak A, Chandra N. Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn Rev 2010; 4(8): 118-26. doi: 10.4103/0973-7847.70902 PMID: 22228951
  12. Dröge W. Free radicals in the physiological control of cell function. Physiol Rev 2002; 82(1): 47-95. doi: 10.1152/physrev.00018.2001 PMID: 11773609
  13. Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev 2014; 94(3): 909-50. doi: 10.1152/physrev.00026.2013 PMID: 24987008
  14. Adams L, Franco MC, Estevez AG. Reactive nitrogen species in cellular signaling. Exp Biol Med 2015; 240(6): 711-7. doi: 10.1177/1535370215581314 PMID: 25888647
  15. Le Gal K, Schmidt EE, Sayin VI. Cellular redox homeostasis. Antioxidants 2021; 10(9): 1377. doi: 10.3390/antiox10091377 PMID: 34573009
  16. Jyoti A, Mishra N, Dhas Y. Ageing: Consequences of excessive free radicals and inflammation. Curr Sci 2016; 111(11): 1787-93. doi: 10.18520/cs/v111/i11/1787-1793
  17. Jomova K, Raptova R, Alomar SY, et al. Reactive oxygen species, toxicity, oxidative stress, and antioxidants: Chronic diseases and aging. Arch Toxicol 2023; 97(10): 2499-574. doi: 10.1007/s00204-023-03562-9 PMID: 37597078
  18. Kumar S, Saxena J, Srivastava VK, et al. The interplay of oxidative stress and ROS scavenging: Antioxidants as a therapeutic potential in sepsis. Vaccines 2022; 10(10): 1575. doi: 10.3390/vaccines10101575 PMID: 36298439
  19. Irato P, Santovito G. Enzymatic and non-enzymatic molecules with antioxidant function. Antioxidants 2021; 10(4): 579. doi: 10.3390/antiox10040579 PMID: 33918542
  20. Snezhkina AV, Kudryavtseva AV, Kardymon OL, et al. ROS generation and antioxidant defense systems in normal and malignant cells. Oxid Med Cell Longev 2019; 2019: 1-17. doi: 10.1155/2019/6175804 PMID: 31467634
  21. Aranda-Rivera AK, Cruz-Gregorio A, Arancibia-Hernández YL, Hernández-Cruz EY, Pedraza-Chaverri J. RONS and oxidative stress: An overview of basic concepts. Oxygen 2022; 2(4): 437-78. doi: 10.3390/oxygen2040030
  22. Liu J, Wu M, Zhang R, Xu ZP. Oxygen-derived free radicals: Production, biological importance, bioimaging, and analytical detection with responsive luminescent nanoprobes. VIEW 2021; 2(5): 20200139. doi: 10.1002/VIW.20200139
  23. Henle ES, Linn S. Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide. J Biol Chem 1997; 272(31): 19095-8. doi: 10.1074/jbc.272.31.19095 PMID: 9235895
  24. Lundberg JO, Weitzberg E. Nitric oxide signaling in health and disease. Cell 2022; 185(16): 2853-78. doi: 10.1016/j.cell.2022.06.010 PMID: 35931019
  25. Graves DB, Bauer G. Key roles of reactive oxygen and nitrogen species. Comprehensive Clinical Plasma Medicine: Cold Physical Plasma for Medical Application 2018; 71-82. doi: 10.1007/978-3-319-67627-2_4
  26. Davies MJ. Protein oxidation and peroxidation. Biochem J 2016; 473(7): 805-25. doi: 10.1042/BJ20151227 PMID: 27026395
  27. Al-Shehri SS. Reactive oxygen and nitrogen species and innate immune response. Biochimie 2021; 181: 52-64. doi: 10.1016/j.biochi.2020.11.022 PMID: 33278558
  28. van der Poll T, Shankar-Hari M, Wiersinga WJ. The immunology of sepsis. Immunity 2021; 54(11): 2450-64. doi: 10.1016/j.immuni.2021.10.012 PMID: 34758337
  29. Stearns-Kurosawa DJ, Osuchowski MF, Valentine C, Kurosawa S, Remick DG. The pathogenesis of sepsis. Annu Rev Pathol: Pathol Mech Dis 2011; 6: 19-48. doi: 10.1146/annurev-pathol-011110-130327
  30. Bhattacharyya A, Chattopadhyay R, Mitra S, Crowe SE. Oxidative stress: An essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol Rev 2014; 94(2): 329-54. doi: 10.1152/physrev.00040.2012 PMID: 24692350
  31. Victor VM, Esplugues JV, Hernandez-Mijares A, Rocha M. Oxidative stress and mitochondrial dysfunction in sepsis: A potential therapy with mitochondria-targeted antioxidants. Infect Disord Drug Targets 2009; 9(4): 376-89. doi: 10.2174/187152609788922519
  32. Alsharabasy AM, Glynn S, Farràs P, Pandit A. Protein nitration induced by Hemin/NO: A complementary mechanism through the catalytic functions of hemin and NO-scavenging. Nitric Oxide 2022; 124: 49-67. doi: 10.1016/j.niox.2022.04.005 PMID: 35513288
  33. Galluzzi L, Kepp O, Kroemer G. Mitochondria: Master regulators of danger signalling. Nat Rev Mol Cell Biol 2012; 13(12): 780-8. doi: 10.1038/nrm3479 PMID: 23175281
  34. Singer M. The role of mitochondrial dysfunction in sepsis-induced multi-organ failure. Virulence 2014; 5(1): 66-72. doi: 10.4161/viru.26907 PMID: 24185508
  35. Kessas K, Chouari Z, Ghzaiel I, et al. Role of bioactive compounds in the regulation of mitochondrial dysfunctions in brain and age-related neurodegenerative diseases. Cells 2022; 11(2): 257. doi: 10.3390/cells11020257 PMID: 35053373
  36. Kovacic P, Pozos RS, Somanathan R, Shangari N, O’Brien PJ. Mechanism of mitochondrial uncouplers, inhibitors, and toxins: Focus on electron transfer, free radicals, and structure-activity relationships. Curr Med Chem 2005; 12(22): 2601-23. doi: 10.2174/092986705774370646 PMID: 16248817
  37. Tirichen H, Yaigoub H, Xu W, Wu C, Li R, Li Y. Mitochondrial reactive oxygen species and their contribution in chronic kidney disease progression through oxidative stress. Front Physiol 2021; 12: 627837. doi: 10.3389/fphys.2021.627837 PMID: 33967820
  38. N Kolodkin A, Sharma RP, Colangelo AM, et al. ROS networks: Designs, aging, Parkinson’s disease and precision therapies. NPJ Syst Biol Appl 2020; 6(1): 34. doi: 10.1038/s41540-020-00150-w PMID: 33106503
  39. Voets AM, Huigsloot M, Lindsey PJ, et al. Transcriptional changes in OXPHOS complex I deficiency are related to anti-oxidant pathways and could explain the disturbed calcium homeostasis. Biochim Biophys Acta Mol Basis Dis 2012; 1822(7): 1161-8. doi: 10.1016/j.bbadis.2011.10.009 PMID: 22033105
  40. Nadalutti CA, Ayala-Peña S, Santos JH. Mitochondrial DNA damage as driver of cellular outcomes. Am J Physiol Cell Physiol 2022; 322(2): C136-50. doi: 10.1152/ajpcell.00389.2021 PMID: 34936503
  41. Andreazza AC, Shao L, Wang JF, Young LT. Mitochondrial complex I activity and oxidative damage to mitochondrial proteins in the prefrontal cortex of patients with bipolar disorder. Arch Gen Psychiatry 2010; 67(4): 360-8. doi: 10.1001/archgenpsychiatry.2010.22 PMID: 20368511
  42. Brealey D, Brand M, Hargreaves I, et al. Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 2002; 360(9328): 219-23. doi: 10.1016/S0140-6736(02)09459-X PMID: 12133657
  43. Yin F, Sancheti H, Cadenas E. Mitochondrial thiols in the regulation of cell death pathways. Antioxid Redox Signal 2012; 17(12): 1714-27. doi: 10.1089/ars.2012.4639 PMID: 22530585
  44. Leyane TS, Jere SW, Houreld NN. Oxidative stress in ageing and chronic degenerative pathologies: Molecular mechanisms involved in counteracting oxidative stress and chronic inflammation. Int J Mol Sci 2022; 23(13): 7273. doi: 10.3390/ijms23137273 PMID: 35806275
  45. Kong C, Song W, Fu T. Systemic inflammatory response syndrome is triggered by mitochondrial damage (Review). Mol Med Rep 2022; 25(4): 147. doi: 10.3892/mmr.2022.12663 PMID: 35234261
  46. Hee JS, Cresswell P. Viperin interaction with mitochondrial antiviral signaling protein (MAVS) limits viperin-mediated inhibition of the interferon response in macrophages. PLoS One 2017; 12(2): e0172236. doi: 10.1371/journal.pone.0172236 PMID: 28207838
  47. Segal AW. How neutrophils kill microbes. Annu Rev Immunol 2005; 23(1): 197-223. doi: 10.1146/annurev.immunol.23.021704.115653 PMID: 15771570
  48. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303(5663): 1532-5.
  49. Fuchs TA, Abed U, Goosmann C, et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007; 176(2): 231-41. doi: 10.1083/jcb.200606027 PMID: 17210947
  50. Papayannopoulos V, Metzler KD, Hakkim A, Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol 2010; 191(3): 677-91. doi: 10.1083/jcb.201006052 PMID: 20974816
  51. Saffarzadeh M, Juenemann C, Queisser MA, et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: A predominant role of histones. PLoS One 2012; 7(2): e32366. doi: 10.1371/journal.pone.0032366 PMID: 22389696
  52. Kumar S, Gupta E, Gupta N, et al. Functional role of iNOS-Rac2 interaction in neutrophil extracellular traps (NETs) induced cytotoxicity in sepsis. Clin Chim Acta 2021; 513: 43-9. doi: 10.1016/j.cca.2020.12.004 PMID: 33309799
  53. Klebanoff SJ, Kettle AJ, Rosen H, Winterbourn CC, Nauseef WM. Myeloperoxidase: A front-line defender against phagocytosed microorganisms. J Leukoc Biol 2013; 93(2): 185-98. doi: 10.1189/jlb.0712349 PMID: 23066164
  54. Martemucci G, Costagliola C, Mariano M, D’andrea L, Napolitano P, D’Alessandro AG. Free radical properties, source and targets, antioxidant consumption and health. Oxygen 2022; 2(2): 48-78. doi: 10.3390/oxygen2020006
  55. Holmström KM, Finkel T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol 2014; 15(6): 411-21. doi: 10.1038/nrm3801 PMID: 24854789
  56. Rohrbach AS, Slade DJ, Thompson PR, Mowen KA. Activation of PAD4 in NET formation. Front Immunol 2012; 3: 360. doi: 10.3389/fimmu.2012.00360 PMID: 23264775
  57. Parker H, Dragunow M, Hampton MB, Kettle AJ, Winterbourn CC. Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. J Leukoc Biol 2012; 92(4): 841-9. doi: 10.1189/jlb.1211601 PMID: 22802447
  58. Keshari RS, Verma A, Barthwal MK, Dikshit M. Reactive oxygen species-induced activation of ERK and p38 MAPK mediates PMA-induced NETs release from human neutrophils. J Cell Biochem 2013; 114(3): 532-40. doi: 10.1002/jcb.24391 PMID: 22961925
  59. Kumar S, Gupta E, Kaushik S, Jyoti A. Neutrophil extracellular traps: Formation and involvement in disease progression. Iran J Allergy Asthma Immunol 2018; 17(3): 208-20. PMID: 29908538
  60. Metzler KD, Fuchs TA, Nauseef WM, et al. Myeloperoxidase is required for neutrophil extracellular trap formation: Implications for innate immunity. Blood 2011; 117(3): 953-9. doi: 10.1182/blood-2010-06-290171 PMID: 20974672
  61. Shen XF, Cao K, Jiang J, Guan WX, Du JF. Neutrophil dysregulation during sepsis: An overview and update. J Cell Mol Med 2017; 21(9): 1687-97. doi: 10.1111/jcmm.13112 PMID: 28244690
  62. Sônego F, Castanheira FVS, Ferreira RG, et al. Paradoxical roles of the neutrophil in sepsis: Protective and deleterious. Front Immunol 2016; 7: 155. doi: 10.3389/fimmu.2016.00155 PMID: 27199981
  63. Santana-Garrido Á, Reyes-Goya C, Arroyo-Barrios A, André H, Vázquez CM, Mate A. Hypertension secondary to nitric oxide depletion produces oxidative imbalance and inflammatory/fibrotic outcomes in the cornea of C57BL/6 mice. J Physiol Biochem 2022; 78(4): 915-32. doi: 10.1007/s13105-022-00916-2 PMID: 35943663
  64. Kumar S, Gupta E, Kaushik S, Kumar Srivastava V, Mehta S, Jyoti A. Evaluation of oxidative stress and antioxidant status: Correlation with the severity of sepsis. Scand J Immunol 2018; 87(4): e12653. doi: 10.1111/sji.12653 PMID: 29484685
  65. Gofton TE, Young GB. Sepsis-associated encephalopathy. Nat Rev Neurol 2012; 8(10): 557-66. doi: 10.1038/nrneurol.2012.183 PMID: 22986430
  66. Gamal M, Moawad J, Rashed L, Morcos MA, Sharawy N. Possible involvement of tetrahydrobiopterin in the disturbance of redox homeostasis in sepsis – Induced brain dysfunction. Brain Res 2018; 1685: 19-28. doi: 10.1016/j.brainres.2018.02.008 PMID: 29428597
  67. Catalão CHR, Santos-Júnior NN, da Costa LHA, Souza AO, Alberici LC, Rocha MJA. Brain oxidative stress during experimental sepsis is attenuated by simvastatin administration. Mol Neurobiol 2017; 54(9): 7008-18. doi: 10.1007/s12035-016-0218-3 PMID: 27796742
  68. Liu H, Wu J, Yao J, Wang H, Li S. The role of oxidative stress in decreased acetylcholinesterase activity at the neuromuscular junction of the diaphragm during sepsis. Oxid Med Cell Longev 2017; 2017: 1-6. doi: 10.1155/2017/9718615 PMID: 29230271
  69. Ottesen LH, Harry D, Frost M, et al. Increased formation of S-nitrothiols and nitrotyrosine in cirrhotic rats during endotoxemia. Free Radic Biol Med 2001; 31(6): 790-8. doi: 10.1016/S0891-5849(01)00647-5 PMID: 11557317
  70. Hong H, Park TJ, Jang S, et al. Anti-inflammatory activity of 6-O- phospho-7-hydroxycoumarin in LPS-induced RAW 264.7 cells. J Appl Biol Chem 2022; 65(1): 33-41. doi: 10.3839/jabc.2022.005
  71. Mehta C, Mehta Y. Management of refractory hypoxemia. Ann Card Anaesth 2016; 19(1): 89-96. doi: 10.4103/0971-9784.173030 PMID: 26750680
  72. Zeng M, He W, Li L, et al. Ghrelin attenuates sepsis-associated acute lung injury oxidative stress in rats. Inflammation 2015; 38(2): 683-90. doi: 10.1007/s10753-014-9977-z PMID: 25037094
  73. Di Meo S, Reed TT, Venditti P, Victor VM. Role of ROS and RNS sources in physiological and pathological conditions. Oxid Med Cell Longevity 2016; 2016 doi: 10.1155/2016/1245049
  74. Caudrillier A, Kessenbrock K, Gilliss BM, et al. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest 2012; 122(7): 2661-71. doi: 10.1172/JCI61303 PMID: 22684106
  75. Gan T, Yang Y, Hu F, et al. TLR3 regulated poly I: C-induced neutrophil extracellular traps and acute lung injury partly through p38 MAP kinase. Front Microbiol 2018; 9: 3174. doi: 10.3389/fmicb.2018.03174 PMID: 30622526
  76. Tsolaki V, Makris D, Mantzarlis K, Zakynthinos E. Sepsis-induced cardiomyopathy: Oxidative implications in the initiation and resolution of the damage. Oxid Med Cell Longev 2017; 2017: 1-11. doi: 10.1155/2017/7393525 PMID: 29057035
  77. Beesley SJ, Weber G, Sarge T, et al. Septic cardiomyopathy. Crit Care Med 2018; 46(4): 625-34. doi: 10.1097/CCM.0000000000002851 PMID: 29227368
  78. Martin L, Derwall M, Al Zoubi S, et al. The septic heart: Current understanding of molecular mechanisms and clinical implications. Chest 2019; 155(2): 427-37. doi: 10.1016/j.chest.2018.08.1037 PMID: 30171861
  79. Bateman RM, Sharpe MD, Ellis CG. Bench-to-bedside review: Microvascular dysfunction in sepsis-hemodynamics, oxygen transport, and nitric oxide. Crit Care 2003; 7(5): 359-73. doi: 10.1186/cc2353 PMID: 12974969
  80. Yan J, Li S, Li S. The role of the liver in sepsis. Int Rev Immunol 2014; 33(6): 498-510. doi: 10.3109/08830185.2014.889129 PMID: 24611785
  81. Guo S, Zhang Y, Wang Z, Yu Y, Wang G. Intraperitoneal gardiquimod protects against hepatotoxicity through inhibition of oxidative stress and inflammation in mice with sepsis. J Biochem Mol Toxicol 2017; 31(8): e21923. doi: 10.1002/jbt.21923 PMID: 28422377
  82. Cogger VC, Mross PE, Hosie MJ, Ansselin AD, McLean AJ. Le Couteur1, 2, 4, 5, 6 DG. The effect of acute oxidative stress on the ultrastructure of the perfused rat liver. Pharmacol Toxicol 2001; 89(6): 306-11. doi: 10.1034/j.1600-0773.2001.d01-165.x PMID: 11903956
  83. Li Z, Liu T, Feng Y, et al. PPARγ alleviates sepsis-induced liver injury by inhibiting hepatocyte pyroptosis via inhibition of the ROS/TXNIP/NLRP3 signaling pathway. Oxid Med Cell Longev 2022; 2022: 1-15. doi: 10.1155/2022/1269747
  84. Oliva-Vilarnau N, Hankeova S, Vorrink SU, Mkrtchian S, Andersson ER, Lauschke VM. Calcium signaling in liver injury and regeneration. Front Med 2018; 5: 192. doi: 10.3389/fmed.2018.00192 PMID: 30023358
  85. Peerapornratana S, Manrique-Caballero CL, Gómez H, Kellum JA. Acute kidney injury from sepsis: Current concepts, epidemiology, pathophysiology, prevention and treatment. Kidney Int 2019; 96(5): 1083-99. doi: 10.1016/j.kint.2019.05.026 PMID: 31443997
  86. Fani F, Regolisti G, Delsante M, et al. Recent advances in the pathogenetic mechanisms of sepsis-associated acute kidney injury. J Nephrol 2018; 31(3): 351-9. doi: 10.1007/s40620-017-0452-4 PMID: 29273917
  87. Kumar S, Gupta E, Srivastava VK, et al. Nitrosative stress and cytokines are linked with the severity of sepsis and organ dysfunction. Br J Biomed Sci 2019; 76(1): 29-34. doi: 10.1080/09674845.2018.1543160 PMID: 30379116
  88. Kumar S, Payal N, Srivastava VK, Kaushik S, Saxena J, Jyoti A. Neutrophil extracellular traps and organ dysfunction in sepsis. Clin Chim Acta 2021; 523: 152-62. doi: 10.1016/j.cca.2021.09.012 PMID: 34537216
  89. Caloren L. Exploration of rare mitochondrial DNA mutations in lymphocyte subsets of people living with human immunodeficiency virus. University of British Columbia 2023.
  90. Vallianou NG, Skourtis A, Kounatidis D, et al. The role of the respiratory microbiome in the pathogenesis of aspiration pneumonia: Implications for diagnosis and potential therapeutic choices. Antibiotics 2023; 12(1): 140. doi: 10.3390/antibiotics12010140 PMID: 36671341
  91. Mokhtari B, Yavari R, Badalzadeh R, Mahmoodpoor A. An overview on mitochondrial-based therapies in sepsis-related myocardial dysfunction: Mitochondrial transplantation as a promising approach. Can J Infect Dis Med Microbiol 2022; 2022: 1-17. doi: 10.1155/2022/3277274 PMID: 35706715
  92. Kothari N, Keshari RS, Bogra J, et al. Increased myeloperoxidase enzyme activity in plasma is an indicator of inflammation and onset of sepsis. J Crit Care 2011; 26(4): 435.e1-7. doi: 10.1016/j.jcrc.2010.09.001 PMID: 21036525

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