Biomarkers and prognostic models for severe COVID-19 in comparison with other etiologies of sepsis

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Severe COVID-19 shares pathophysiological, immunological, metabolic, and clinical features with classic bacterial sepsis. Patients with severe COVID-19 have sepsis-like manifestations, such as acute respiratory distress syndrome and multiple organ failure. However, research indicates that COVID-19 leads to acute respiratory distress syndrome and that septic syndrome is more fatal than septic syndrome of other etiologies. SARS-CoV-2 initially infects the lungs; however, in COVID-19-associated sepsis, the majority of deaths are caused by the subsequent involvement of multiple organs. Many patients who died because of COVID-19 died from sepsis, a life-threatening dysfunctional response to infection that is accompanied by respiratory and multiple organ failure.

Overlapping molecular characteristics are found in patients with severe COVID-19 and sepsis from all causes. Endotypes that reflect different etiologies of sepsis have been identified in patients with severe COVID-19. Whole-blood proteomics and transcriptomics are useful in identifying the pathogenetic mechanisms and multimolecular signatures of COVID-associated sepsis and other sepsis, which allow for the development of more specific criteria for early diagnosis, patient classification, and therapeutic choices.

The detection of sepsis endotypes in patients with COVID-19 implies that sepsis endotypes may be useful for clinical risk stratification in COVID-associated sepsis and the potential opportunity to treat these patients with targeted immunomodulatory therapies that can correct endotype-specific dysfunctional immune processes.

Full Text

Restricted Access

About the authors

Sergey G. Sсherbak

City Hospital No. 40 Kurortny District; St Petersburg University

Email: b40@zdrav.spb.ru
ORCID iD: 0000-0001-5036-1259
SPIN-code: 1537-9822

MD, dr. sci. (med.), professor

Russian Federation, 9B Borisova street, 197706 Sestroretsk

Andrey M. Sarana

St Petersburg University; Health Committee of the Administration of Saint Petersburg

Email: asarana@mail.ru
ORCID iD: 0000-0003-3198-8990
SPIN-code: 7922-2751

MD, cand. sci. (med.), associate professor

Russian Federation, Saint-Petersburg

Dmitry A. Vologzhanin

City Hospital No. 40 Kurortny District; St Petersburg University

Email: volog@bk.ru
ORCID iD: 0000-0002-1176-794X
SPIN-code: 7922-7302

MD, dr. sci. med.)

Russian Federation, 9B Borisova street, Sestroretsk, 197706

Aleksandr S. Golota

City Hospital No. 40 Kurortny District

Email: golotaa@yahoo.com
ORCID iD: 0000-0002-5632-3963

MD, cand. sci. (med.), associate professor

Russian Federation, 9B Borisova street, 197706 Sestroretsk

Tatiana A. Kamilova

City Hospital No. 40 Kurortny District

Email: kamilovaspb@mail.ru
ORCID iD: 0000-0001-6360-132X
SPIN-code: 2922-4404

cand. sci. (biol.)

Russian Federation, 9B Borisova street, 197706 Sestroretsk

Stanislav V. Makarenko

City Hospital No. 40 Kurortny District; St Petersburg University

Author for correspondence.
Email: st.makarenko@gmail.com
ORCID iD: 0000-0002-1595-6668
SPIN-code: 8114-3984
Russian Federation, 9B Borisova street, 197706 Sestroretsk

References

  1. Buturovic L, Zheng H, Tang B, et al. A 6-mRNA host response classifier in whole blood predicts outcomes in COVID-19 and other acute viral infections. Sci Rep. 2022;12(1):889. doi: 10.1038/s41598-021-04509-9
  2. Schmidt K, Gensichen J, Fleischmann-Struzek C, et al. Long-term survival following sepsis. Dtsch Arztebl Int. 2020;117(46): 775–782. doi: 10.3238/arztebl.2020.0775
  3. Antonakos N, Gilbert C, Théroude C, et al. Modes of action and diagnostic value of miRNAs in sepsis. Front Immunol. 2022;13:951798. doi: 10.3389/fimmu.2022.951798
  4. Singer M, Deutschman CS, Seymour CW, et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA. 2016;315(8):801–810. doi: 10.1001/jama.2016.0287
  5. Formosa A, Turgeon P, Dos Santos CC. Role of miRNA dysregulation in sepsis. Mol Med. 2022;28(1):99. doi: 10.1186/s10020-022-00527-z
  6. Alhazzani W, Evans L, Alshamsi F, et al. Surviving sepsis campaign guidelines on the management of adults with coronavirus disease 2019 (COVID-19) in the ICU: first update. Critical Care Medicine. 2021;49(3):e219–e234. doi: 10.1097/CCM.0000000000004899
  7. Miró Ò, Jiménez S, Llorens P, et al. Pulmonary embolism severity and in-hospital mortality: an international comparative study between COVID-19 and non-COVID patients. Eur J Intern Med. 2022;98:69–76. doi: 10.1016/j.ejim.2022.01.035
  8. Huang S, Perry A, Parra CS, et al. Frequency of thrombosis in covid-19 patients compared to non-Covid-19 sepsis patients admitted to the intensive care unit. Blood. 2022;140(Suppl. 1):2782. doi: 10.1182/blood-2022-168088
  9. Shappell CN, Klompas M, Kanjilal S, et al. Prevalence, clinical characteristics, and outcomes of sepsis caused by severe acute respiratory syndrome coronavirus 2 versus other pathogens in hospitalized patients with COVID-19. Crit Care Explor. 2022;4(5):e0703. doi: 10.1097/CCE.0000000000000703
  10. Scherbak SG, Kamilova TA, Golota AS, Vologzhanin DA. Risk factors of the severe course and fatal outcome in COVID-19. Physical and Rehabilitation Medicine, Medical Rehabilitation. 2022;4(1):14–36. (In Russ). doi: 10.36425/rehab104997
  11. Shcherbak SG, Sarana AM, Vologzhanin DA, et al. Biomarkers for surgical sepsis. A review of foreign scientific and medical publications. Journal of Clinical Practice. 2023;14(2):66–78. (In Russ). doi: 10.17816/clinpract346695
  12. Shcherbak S, Kamilova T, Golota A, et al. Pathogenesis of pulmonary complications COVID-19. Medical Alliance. 2021;9(4): 6–25. (In Russ). doi: 10.36422/23076348-2021-9-4-6-25
  13. Wu M, Zou ZY, Chen YH, et al. Severe COVID-19-associated sepsis is different from classical sepsis induced by pulmonary infection with carbapenem-resistant klebsiella pneumonia (CrKP). Chin J Traumatol. 2022;25(1):17–24. doi: 10.1016/j.cjtee.2021.11.001
  14. Moser D, Feuerecker M, Biere K, et al. SARS-CoV-2 pneumonia and bacterial pneumonia patients differ in a second hit immune response model. Sci Rep. 2022;12(1):15485. doi: 10.1038/s41598-022-17368-9
  15. Heubner L, Hattenhauer S, Güldner A, et al. Characteristics and outcomes of sepsis patients with and without COVID-19. J Infect Public Health. 2022;15(6):670–676. doi: 10.1016/j.jiph.2022.05.008
  16. Li P, Wang C, Pang S. The diagnostic accuracy of mid-regional pro-adrenomedullin for sepsis: a systematic review and meta-analysis. Minerva Anestesiol. 2021;87(10):1117–1127. doi: 10.23736/S0375-9393.21.15585-3
  17. Saeed K, Legramante JM, Angeletti S, et al. Mid-regional pro-adrenomedullin as a supplementary tool to clinical parameters in cases of suspicion of infection in the emergency department. Expert Rev Mol Diagn. 2021;21(4):397–404. doi: 10.1080/14737159.2021.1902312
  18. De Montmollin E, Peoc’h K, Marzouk M, et al. Mid-regional pro-adrenomedullin as a prognostic factor for severe COVID-19 ARDS. Antibiotics. 2022;11(9):1166. doi: 10.3390/antibiotics11091166
  19. Montrucchio G, Sales G, Balzani E, et al. Effectiveness of mid-regional pro-adrenomedullin, compared to other biomarkers (including lymphocyte subpopulations and immunoglobulins), as a prognostic biomarker in COVID-19 critically ill patients: new evidence from a 15-month observational prospective study. Front Med (Lausanne). 2023;10:1122367. doi: 10.3389/fmed.2023.1122367
  20. Iwamura APD, Tavares da Silva MR, Hümmelgen AL, et al. Immunity and inflammatory biomarkers in COVID-19: a systematic review. Rev Med Virol. 2021;31(4):e2199. doi: 10.1002/rmv.2199
  21. Khodeir MM, Shabana HA, Alkhamiss AS, et al. Early prediction keys for COVID-19 cases progression: a meta-analysis. J Infect Public Health. 2021;14(5):561–569. doi: 10.1016/j.jiph.2021.03.001
  22. Melo AKG, Milby KM, Caparroz ALMA, et al. Biomarkers of cytokine storm as red flags for severe and fatal COVID-19 cases: a living systematic review and meta-analysis. PLoS One. 2021;16(6):e0253894. doi: 10.1371/journal.pone.0253894
  23. Bima P, Montrucchio G, Caramello V, et al. Prognostic value of mid-regional Proadrenomedullin sampled at presentation and after 72 hours in septic patients presenting to the emergency department: an observational two-center study. Biomedicines. 2022;10(3):719. doi: 10.3390/biomedicines10030719
  24. Zhang H, Wang Y, Qu M, et al. Neutrophil, neutrophil extracellular traps and endothelial cell dysfunction in sepsis. Clin Transl Med. 2023;13(1):e1170. doi: 10.1002/ctm2.1170
  25. Baby S, Reljic T, Villalba N, et al. Endothelial glycocalyx-associated molecules as potential serological markers for sepsis-associated encephalopathy: a systematic review and meta-analysis. PLoS One. 2023;18(2):e0281941. doi: 10.1371/journal.pone.0281941
  26. Goonewardena SN, Grushko OG, Wells J, et al. Immune-mediated glycocalyx remodeling in hospitalized COVID-19 patients. Cardiovasc Drugs Ther. 2023;37(2):307–313. doi: 10.1007/s10557-021-07288-7
  27. Ioannou M, Hoving D, Aramburu IV, et al. Microbe capture by splenic macrophages triggers sepsis via T cell-death-dependent neutrophil lifespan shortening. Nat Commun. 2022;13(1):4658. doi: 10.1038/s41467-022-32320-1
  28. Aramburu IV, Hoving D, Vernardis SI, et al. Functional proteomic profiling links deficient DNA clearance with increased mortality in individuals with severe COVID-19 pneumonia. Immunity. 2022; 55(12):2436–2453.e5. doi: 10.1016/j.immuni.2022.11.007
  29. Yang MY, Zheng MH, Meng XT, et al. Role of toll-like receptors in the pathogenesis of COVID-19: current and future perspectives. Scand J Immunol. 2023;98(2):e13275. doi: 10.1111/sji.13275
  30. Yang JX, Tseng JC, Yu GY, et al. Recent advances in the development of toll-like receptor agonist-based vaccine adjuvants for infectious diseases. Pharmaceutics. 2022;14(2):423. doi: 10.3390/pharmaceutics14020423
  31. Bortolotti D, Gentili V, Rizzo S, et al. TLR3 and TLR7 RNA sensor activation during SARS-CoV-2 infection. Microorganisms. 2021;9(9):1820. doi: 10.3390/microorganisms9091820
  32. Menezes MCS, Veiga ADM, Martins de Lima T, et al. Lower peripheral blood toll-like receptor 3 expression is associated with an unfavorable outcome in severe COVID-19 patients. Sci Rep. 2021;11(1):15223. doi: 10.1038/s41598-021-94624-4
  33. Mukherjee R, Bhattacharya A, Bojkova D, et al. Famotidine inhibits toll-like receptor 3-mediated inflammatory signaling in SARS-CoV-2 infection. J Biol Chem. 2021;297(2):100925. doi: 10.1016/j.jbc.2021.100925
  34. Croci S, Venneri MA, Mantovani S, et al. The polymorphism L412F in TLR3 inhibits autophagy and is a marker of severe COVID-19 in males. Autophagy. 2022;18(7):1662–1672. doi: 10.1080/15548627.2021.1995152
  35. Xu B, Sui Q, Hu H, et al. SAMHD1 Attenuates acute inflammation by maintaining mitochondrial function in macrophages via interaction with VDAC1. Int J Mol Sci. 2023;24(9):7888. doi: 10.3390/ijms24097888
  36. Müller MM, Baldauf C, Hornischer S, et al. Staphylococcus aureus induces tolerance in human monocytes accompanied with expression changes of cell surface markers. Front Immunol. 2023;14:1046374. doi: 10.3389/fimmu.2023.1046374
  37. Giamarellos-Bourboulis EJ, Netea MG, Rovina N, et al. Complex immune dysregulation in COVID-19 patients with severe respiratory failure. Cell Host Microbe. 2020;27(6):992–1000.e3. doi: 10.1016/j.chom.2020.04.009
  38. De Oliveira Formiga R, Amaral FC, Souza CF, et al. Neuraminidase is a host-directed approach to regulate neutrophil responses in sepsis and COVID-19. Br J Pharmacol. 2023;180(11):1460–1481. doi: 10.1111/bph.16013
  39. Chiba S. Effect of early oseltamivir on outpatients without hypoxia with suspected COVID-19. Wien Klin Wochenschr. 2021;133(7-8): 292–297. doi: 10.1007/s00508-020-01780-0
  40. Rohmann N, Stürmer P, Geisler C, et al. Brief research report: serum clara cell 16 kDa protein levels are increased in patients hospitalized for severe SARS-CoV-2 or sepsis infection. Front Immunol. 2022;13:1037115. doi: 10.3389/fimmu.2022.1037115
  41. Fagyas M, Fejes Z, Sütő R, et al. Circulating ACE2 activity predicts mortality and disease severity in hospitalized COVID-19 patients. Int J Infect Dis. 2022;115:8–16. doi: 10.1016/j.ijid.2021.11.028
  42. Hortová-Kohoutková M, Skotáková M, Onyango IG, et al. Hepcidin and ferritin levels as markers of immune cell activation during septic shock, severe COVID-19 and sterile inflammation. Front Immunol. 2023;14:1110540. doi: 10.3389/fimmu.2023.1110540
  43. Protti A, Meessen J, Bottazz B, et al. Circulating pentraxin 3 in severe COVID-19 or other pulmonary sepsis. Eur J Clin Invest. 2021;51(5):e13530. doi: 10.1111/eci.13530
  44. Seymour CW, Liu VX, Iwashyna TJ, et al. Assessment of clinical criteria for sepsis: for the third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA. 2016;315(8):762–774. doi: 10.1001/jama.2016.0288
  45. Leisman DE, Ronner L, Pinotti R, et al. Cytokine elevation in severe and critical COVID-19: a rapid systematic review, meta-analysis, and comparison with other inflammatory syndromes. Lancet Respir Med. 2020;8(12):1233–1244. doi: 10.1016/S2213-2600(20)30404-5
  46. Stolarski AE, Kim J, Zhang Q, Remick DG. Cytokine drizzle-the rationale for abandoning “Cytokine Storm”. Shock. 2021;56(5): 667–672. doi: 10.1097/SHK.0000000000001769
  47. Herminghausa A, Osuchowski MF. How sepsis parallels and differs from COVID-19. EBioMedicine. 2022;86:104355. doi: 10.1016/j.ebiom.2022.104355
  48. Ebihara T, Matsumoto H, Matsubara T, et al. Cytokine elevation in severe COVID-19 from longitudinal proteomics analysis: comparison with sepsis. Front Immunol. 2022;12:798338. doi: 10.3389/fimmu.2021.798338
  49. Patton MJ, Orihuela CJ, Harrod KS, et al. COVID-19 bacteremic co-infection is a major risk factor for mortality, ICU admission, and mechanical ventilation. Crit Care. 2023;27(1):34. doi: 10.1186/s13054-023-04312-0
  50. Seymour CW, Kennedy JN, Shu Wang, et al. Derivation, validation, and potential treatment implications of novel clinical phenotypes for sepsis. JAMA. 2019;321(20):2003–2017. doi: 10.1001/jama.2019.5791
  51. Bruse N, Kooistra EJ, Jansen A, et al. Clinical sepsis phenotypes in critically ill COVID-19 patients. Crit Care. 2022;26(1):244. doi: 10.1186/s13054-022-04118-6
  52. Kaur S, Hussain S, Kolhe K, Kumar G. Elevated plasma ICAM1 levels predict 28-day mortality in cirrhotic patients with COVID-19 or bacterial sepsis. JHEP Rep. 2021;3(4):100303. doi: 10.1016/j.jhepr.2021.100303
  53. Iepsen UW, Plovsing RR, Tjelle K, et al. The role of lactate in sepsis and COVID-19: perspective from contracting skeletal muscle metabolism. Exp Physiol. 2022;107(7):665–673. doi: 10.1113/EP089474
  54. Campbell RA, Hisada Y, Denorme F, et al. Comparison of the coagulopathies associated with COVID-19 and sepsis. Res Pract Thromb Haemost. 2021;5(4):e12525. doi: 10.1002/rth2.12525
  55. Karakike E, Giamarellos-Bourboulis EJ, Kyprianou M, et al. Coronavirus disease 2019 as cause of viral sepsis: a systematic review and meta-analysis. Crit Care Med. 2021;49(12):2042–2057. doi: 10.1097/CCM.0000000000005195
  56. Batra R, Whalen W, Alvarez-Mulett S, et al. Multi-omic comparative analysis of COVID-19 and bacterial sepsis-induced ARDS. PLoS Pathog. 2022;18(9):e1010819. doi: 10.1371/journal.ppat.1010819
  57. Trovato FM, Mujib S, Jerome E, et al. Immunometabolic analysis shows a distinct cyto-metabotype in Covid-19 compared to sepsis from other causes. Heliyon. 2022;8(6):e09733. doi: 10.1016/j.heliyon.2022.e09733
  58. Huang L, Li X, Gu X, et al. Health outcomes in people 2 years after surviving hospitalisation with COVID-19: a longitudinal cohort study. Lancet Respir Med. 2022;10(9):863–876. doi: 10.1016/S2213-2600(22)00126-6
  59. Puntmann VO, Martin S, Shchendrygina A, et al. Long-term cardiac pathology in individuals with mild initial COVID-19 illness. Nat Med. 2022;28(10):2117–2123. doi: 10.1038/s41591-022-02000-0
  60. Vassiliou AG, Zacharis A, Vrettou CS, et al. Comparison of the mortality prediction value of soluble urokinase plasminogen activator receptor (suPAR) in COVID-19 and sepsis. Diagnostics (Basel). 2022;12(5):1261. doi: 10.3390/diagnostics12051261
  61. Ming S, Qu S, Wu Y, et al. COVID-19 metabolomic-guided amino acid therapy protects from inflammation and disease sequelae. Adv Biol (Weinh). 2023;e2200265. doi: 10.1002/adbi.202200265
  62. Karki R, Sharma BR, Tuladhar S, et al. Synergism of TNF-α and IFN-γ triggers inflammatory cell death, tissue damage, and mortality in SARS-CoV-2 infection and cytokine shock syndromes. Cell. 2021;184(1):149–168.e17. doi: 10.1016/j.cell.2020.11.025
  63. Komorowski M, Green A, Tatham KC, et al. Sepsis biomarkers and diagnostic tools with a focus on machine learning. EBioMedicine. 2022;86:104394. doi: 10.1016/j.ebiom.2022.104394
  64. Kalil AC, Patterson TF, Mehta AK, et al. Baricitinib plus remdesivir for hospitalized adults with COVID-19. N Engl J Med. 2021;384(9): 795–807. doi: 10.1056/NEJMoa2031994
  65. Guimarães PO, Quirk D, Furtado RH, et al. Tofacitinib in patients hospitalized with Covid-19 pneumonia. N Engl J Med. 2021;385(5):406–415. doi: 10.1056/NEJMoa2101643
  66. Helms J, Tacquard C, Severac F, et al. High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study. Intensive Care Med. 2020;46(6):1089–1098. doi: 10.1007/s00134-020-06062-x
  67. Batra R, Uni R, Akchurin OM, et al. Urine-based multi-omic comparative analysis of COVID-19 and bacterial sepsis-induced ARDS. Mol Med. 2023;29(1):13. doi: 10.1186/s10020-023-00609-6
  68. Schrijver IT, Karakike E, Theroude C, et al. High levels of monocytic myeloid-derived suppressor cells are associated with favorable outcome in patients with pneumonia and sepsis with multi-organ failure. Intensive Care Med Exp. 2022;10(1):5. doi: 10.1186/s40635-022-00431-0
  69. Schrijver IT, Theroude C, Antonakos N, et al. COVID-19 rapidly increases MDSCs and prolongs innate immune dysfunctions. Eur J Immunol. 2022;52(10):1676–1679. doi: 10.1002/eji.202249827
  70. Akula SM, Bolin P, Cook PP. Cellular miR-150-5p may have a crucial role to play in the biology of SARS-CoV-2 infection by regulating nsp10 gene. RNA Biol. 2022;19(1):1–11. doi: 10.1080/15476286.2021.2010959
  71. Nicoletti AS, Visacri MB, da Ronda CRDSC, et al. Differentially expressed plasmatic microRNAs in Brazilian patients with Coronavirus disease 2019 (COVID-19): preliminary results. Mol Biol Rep. 2022;49(7):6931–6943. doi: 10.1007/s11033-022-07338-9
  72. An AY, Baghela A, Zhang P, et al. Severe COVID-19 and non-COVID-19 severe sepsis converge transcriptionally after a week in the intensive care unit, indicating common disease mechanisms. Front Immunol. 2023;14:1167917. doi: 10.3389/fimmu.2023.1167917
  73. Gottlieb RL, Vaca CE, Paredes R, et al. Early remdesivir to prevent progression to severe COVID-19 in outpatients. N Engl J Med. 2022;386(4):305–315. doi: 10.1056/NEJMoa2116846
  74. Weinreich DM, Sivapalasingam S, Norton T, et al. REGEN-COV antibody combination and outcomes in outpatients with COVID-19. N Engl J Med. 2021;385(23):e81. doi: 10.1056/NEJMoa2108163
  75. ACTIV-3/TICO LY-CoV555 Study Group; Lundgren JD, Grund B, et al. A neutralizing monoclonal antibody for hospitalized patients with COVID-19. N Engl J Med. 2021;384(10):905–914. doi: 10.1056/NEJMoa2033130
  76. Beltrán-García J, Osca-Verdegal R, Pallardó FV, et al. Sepsis and coronavirus disease 2019: common features and anti-inflammatory therapeutic approaches. Crit Care Med. 2020;48(12):1841–1844. doi: 10.1097/CCM.0000000000004625
  77. Yan Q, Li P, Ye X, et al. Longitudinal peripheral blood transcriptional analysis reveals molecular signatures of disease progression in COVID-19 patients. J Immunol. 2021;206(9): 2146–2159. doi: 10.4049/jimmunol.2001325
  78. Olwal CO, Nganyewo NN, Tapela K, et al. Parallels in sepsis and COVID-19 conditions: implications for managing severe COVID-19. Front Immunol. 2021;12:602848. doi: 10.3389/fimmu.2021.602848
  79. Cummings MJ, Jacob ST. Equitable endotyping is essential to achieve a global standard of precise, effective, and locally-relevant sepsis care. EBioMedicine. 2022;86:104348. doi: 10.1016/j.ebiom.2022.104348
  80. Vincent JL. Emerging paradigms in sepsis. EBioMedicine. 2022; 86:104398. doi: 10.1016/j.ebiom.2022.104398
  81. Gupta S, Leaf DE. Tocilizumab in COVID-19: some clarity amid controversy. Lancet. 2021;397(10285):1599–1601. doi: 10.1016/S0140-6736(21)00712-1
  82. Supady A, Zeiser R. Baricitinib for patients with severe COVID-19–time to change the standard of care? Lancet Respir Med. 2022;10(4):314–315. doi: 10.1016/S2213-2600(22)00021-2
  83. Baghela A, Pena OM, Lee AH, et al. Predicting sepsis severity at first clinical presentation: the role of endotypes and mechanistic signatures. EBioMedicine. 2022;75:103776. doi: 10.1016/j.ebiom.2021.103776
  84. Sweeney TE, Liesenfeld O, Wacker J, et al. Validation of inflammopathic, adaptive, and coagulopathic sepsis endotypes in coronavirus disease 2019. Crit Care Med. 2021;49(2):e170–e178. doi: 10.1097/CCM.0000000000004786
  85. Torres LK, Pickkers P, van der Poll T. Sepsis-induced immunosuppression. Annu Rev Physiol. 2022;84:157–181. doi: 10.1146/annurev-physiol-061121-040214
  86. Li H, Liu L, Zhang D, et al. SARS-CoV-2 and viral sepsis: observations and hypotheses. Lancet. 2020;395(10235):1517–1520. doi: 10.1016/S0140-6736(20)30920-X
  87. Shafran N, Shafran I, Ben-Zvi H, et al. Secondary bacterial infection in COVID-19 patients is a stronger predictor for death compared to influenza patients. Sci Rep. 2021;11(1):1–8. doi: 10.1038/s41598-021-92220-0
  88. Baghela A, An A, Zhang P, et al. Predicting severity in COVID-19 disease using sepsis blood gene expression signatures. Sci Rep. 2023;13(1):1247. doi: 10.1038/s41598-023-28259-y
  89. Vegivinti CTR, Evanson KW, Lyons H, et al. Efficacy of antiviral therapies for COVID-19: a systematic review of randomized controlled trials. BMC Infect Dis. 2022;22(1):1–45. doi: 10.1186/s12879-022-07068-0
  90. Park J, Dean LS, Jiyarom B, et al. Elevated circulating monocytes and monocyte activation in COVID-19 convalescent individuals. Front Immunol. 2023;14:1151780. doi: 10.3389/fimmu.2023.1151780
  91. Cusinato M, Hadcocks L, Yona S, et al. Increased monocyte distribution width in COVID-19 and sepsis arises from a complex interplay of altered monocyte cellular size and subset frequency. Int J Lab Hematol. 2022;44(6):1029–1039. doi: 10.1111/ijlh.13941
  92. Malinovska A, Hernried B, Lin A, et al. Monocyte distribution width as a diagnostic marker for infection: a systematic review and meta-analysis. Chest. 2023;164(1):101–113. doi: 10.1016/j.chest.2022.12.049
  93. Koc S, Hanikoglu F, Dokur M, et al. Comparison of cytokine hemadsorption as an immunomodulator therapy in COVID-19 patients with and without bacterial sepsis. Clin Lab. 2022;68(10). doi: 10.7754/Clin.Lab.2022.211249
  94. Golicnik A, Zivanovic I, Gorjup V, Berden J. Same but different-ECMO in COVID-19 and ARDS of other etiologies. comparison of survival outcomes and management in different ARDS groups. J Intensive Care Med. 2023;38(7):635–642. doi: 10.1177/08850666231157286
  95. Zaaqoq A, Sallam T, Merley C, et al. The interplay of inflammation and coagulation in COVID-19 patients receiving extracorporeal membrane oxygenation support. Perfusion. 2023;38(2):384–392. doi: 10.1177/02676591211057506

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2023 Eco-Vector


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия  ПИ № ФС 77 - 86296 от 11.12.2023 г. 
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ЭЛ № ФС 77 - 80632 от 15.03.2021 г.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies