Тромбоз, гемостаз и реология

Tromboz, Gemostaz I Reologiya
scientific and practical journal

ISSN 2078–1008 (Print); ISSN 2687-1483 (online)
2023, Review
2023

COVID‐19‐related thrombosis: new experiences and challenges of thrombotic complications arising from the pandemic: 616-005.6

Review
Published 2023-09-22
Pavel G. Madonov
Novosibirsk State Medical University, Ministry of Health of the Russian Federation; 52 Krasny Prospekt, Novosibirsk 630091, Russia;
ФГБОУ ВО «Новосибирский государственный медицинский университет» Министерства здравоохранения Российской Федерации; Россия, 630091 Новосибирск, Красный проспект, 52;
https://orcid.org/0000-0002-1093-8938 (unauthenticated)
Andrey P. Momot
Altai Branch of National Medical Research Centre for Hematology, Ministry of Health of the Russian Federation; 1 Lyapidevskogo Str., Barnaul 656045, Russia; Altai State Medical University, Ministry of Health of the Russian Federation; 40 Prospekt Lenina, Barnaul 656038, Russia;
Алтайский филиал ФГБУ «Национальный медицинский исследовательский центр гематологии» Министерства здравоохранения Российской Федерации; Россия, 656024 Барнаул, ул. Ляпидевского, 1; ФГБОУ ВО «Алтайский государственный медицинский университет» Министерства здравоохранения Российской Федерации; Россия, 656038 Барнаул, проспект Ленина, 40;
https://orcid.org/0000-0002-8413-5484 (unauthenticated)
Eugene V. Roitman
Pirogov Russian National Research Medical University, Ministry of Health of the Russian Federation; 1 Ostrovityanova Str., Moscow 117997, Russia; Research Center of Neurology; 80 Volokolamskoe Shosse, Moscow 125367, Russia;
ФГАОУ ВО «Российский национальный исследовательский медицинский университет имени Н.И. Пирогова» Министерства здравоохранения Российской Федерации; Россия, 117997 Москва, ул. Островитянова, 1; ФГБНУ «Научный центр неврологии»; Россия, 125367 Москва, Волоколамское шоссе, 80;
https://orcid.org/0000-0002-3015-9317 (unauthenticated)
Vladimir V. Udut
Goldberg Research Institute of Pharmacology and Regenerative Medicine, Tomsk National Research Medical Center, Russian Academy of Sciences; 3 Prospekt Lenina, Tomsk 634028, Russia
«Научно-исследовательский институт фармакологии и регенеративной медицины имени Е.Д. Гольдберга» ФГБНУ «Томский национальный исследовательский медицинский центр Российской академии наук»; Россия, 634028 Томск, проспект Ленина, 3
https://orcid.org/0000-0002-3829-7132 (unauthenticated)

Keywords

COVID‐19‐related thrombosis
pathogenesis and treatment
anticoagulants
thrombolytic therapy
  Full Text

Abstract

Summary. COVID-19 is distinguished by the rapid development of coagulopathy associated with thromboses that affect both the main vessels and microcirculation. The pathogenesis of COVID-19-related thrombosis is diverse and individual, while the gold standard for its diagnosing has not yet been established. The main method for COVID-19-related thrombosis prevention and treat- ment is anticoagulant therapy. There is no reliable evidence for the use of antiplatelet agents in thromboprophylaxis for COVID-19. Targeted treatment in COVID-19-related thrombosis is thrombolytic therapy that is now used off-label. Clinical studies are being conducted; however, clinical recommendations for its use in patients with COVID-19 are not yet available.

For citation: Madonov P.G., Momot A.P., Roitman E.V., Udut V.V. COVID-19-related thrombosis: new experiences and challenges of thrombotic complications arising from the pandemic. Tromboz, gemostaz i reologiya. 2023;(2):59–66. (In Russ.).

References

  1. Poissy J., Goutay J., Caplan M. et al.; Lille ICU Haemostasis COVID‐19 Group. Pulmonary embolism in patients with COVID‐19: awareness of an increased prevalence. Circulation. 2020;142(2):184– 6. DOI: 10.1161/CIRCULATIONAHA.120.047430.
  2. Smilowitz N.R., Subashchandran V., Yuriditsky E. et al. Thrombosis in hospitalized patients with viral respiratory infections versus COVID‐19. Am Heart J. 2021;231:93–5. DOI: 10.1016/j. ahj.2020.10.075.
  3. Burn E., Duarte‐Salles T., Fernandez‐Bertolin S. et al. Venous or arterial thrombosis and deaths among COVID‐19 cases: a European network cohort study. Lancet Infect Dis. 2022;22(8):1142–52. DOI: 10.1016/S1473‐3099(22)00223‐7.
  4. Cui S., Chen S., Li X. et al. Prevalence of venous thromboembolism in patients with severe novel coronavirus pneumonia. J Thromb Haemost. 2020;18(6):1421–4. DOI: 10.1111/jth.14830.
  5. Klok F.A., Kruip M.J.H.A., van der Meer N.J.M. et al. Confirmation of the high cumulative incidence of thrombotic complications in critically ill ICU patients with COVID‐19: An updated analysis. Thromb Res. 2020;191:148–50. DOI: 10.1016/j.thromres.2020.04.041.
  6. Mansory E.M., Srigunapalan S., Lazo‐Langner A. Venous thromboembolism in hospitalized critical and noncritical COVID‐19 patients: A systematic review and meta‐analysis. TH Open. 2021;5(3):e286‐e294. DOI: 10.1055/s‐0041‐1730967.
  7. Nopp S., Moik F., Jilma B. et al. Risk of venous thromboembolism in patients with COVID‐19: a systematic review and meta‐analysis. Res Pract Thromb Haemost. 2020;4(7):1178–91. DOI: 10.1002/rth2.12439.
  8. Morici N., Podda G., Birocchi S. et al. Enoxaparin for thromboprophylaxis in hospitalized COVID‐19 patients: The X– COVID‐19 Randomized Trial. Eur J Clin Invest. 2022;52(5):e13735. DOI: 10.1111/eci.13735.
  9. Fitzek A., Schädler J., Dietz E. et al. Prospective postmortem evaluation of 735 consecutive SARS‐CoV‐2‐associated death cases. Sci Rep. 2021;11(1):19342. DOI: 10.1038/s41598‐021‐98499‐3.
  10. Zhang S., Zhang J., Wang C. et al. COVID‐19 and ischemic stroke: Mechanisms of hypercoagulability (Review). Int J Mol Med. 2021;47(3):21. DOI: 10.3892/ijmm.2021.4854.
  11. Cheruiyot I., Kipkorir V., Ngure B. et al. Arterial thrombosis in coronavirus disease 2019 patients: A rapid systematic review. Ann Vasc Surg. 2021;70:273–81. DOI: 10.1016/j.avsg.2020.08.087.
  12. Ulanowska M., Olas B. Modulation of hemostasis in COVID‐19; blood platelets may be important pieces in the COVID‐19 puzzle. Pathogens. 2021;10(3):370. DOI: 10.3390/pathogens10030370.
  13. Kim B., Arany Z. Editorial commentary: Could shear stress mimetics delay complications in COVID‐19? Trends Cardiovasc Med. 2022;32(2):71–2. DOI: 10.1016/j.tcm.2021.01.004.
  14. Stein R.A., Young L.M. From ACE2 to COVID‐19: A multiorgan endothelial disease. Int J Infect Dis. 2020;100:425–30. DOI: 10.1016/j. ijid.2020.08.083.
  15. Libby P., Lüscher T. COVID‐19 is, in the end, an endothelial disease. Eur Heart J. 2020;41(32):3038–44. DOI: 10.1093/eurheartj/ehaa623.
  16. Varga Z., Flammer A.J., Steiger P. et al. Endothelial cell infection and endotheliitis in COVID‐19. Lancet. 2020;395(10234):1417–8. DOI: 10.1016/S0140‐6736(20)30937‐5.
  17. Escher R., Breakey N., Lämmle B. Severe COVID‐19 infection associated with endothelial activation. Thromb Res. 2020;190:62. DOI: 10.1016/j.thromres.2020.04.014.
  18. Ward S.E., Curley G.F., Lavin M. et al.; Irish COVID‐19 Vasculopathy Study (ICVS) Investigators. Von Willebrand factor propeptide in severe coronavirus disease 2019 (COVID‐19): evidence of acute and sustained endothelial cell activation. Br J Haematol. 2021;192(4):714–9. DOI: 10.1111/bjh.17273.
  19. Sastry S., Cuomo F., Muthusamy J. COVID‐19 and thrombosis: The role of hemodynamics. Thromb Res. 2022;212:51–7. DOI: 10.1016/j. thromres.2022.02.016.
  20. Nelson M., Shi D., Gordon M. et al. Where there’s smoke, there’s fire: a case report of turbulent blood flow in lower extremity point‐of‐care ultrasound in COVID‐19. Clin Pract Cases Emerg Med. 2021;5(1):30–4. DOI: 10.5811/cpcem.2020.10.48809.
  21. Leisman D. E., 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):1233–44. DOI: 10.1016/S2213‐2600(20)30404‐5.
  22. Ranucci M., Ballotta A., Di Dedda U. et al. The procoagulant pattern of patients with COVID‐19 acute respiratory distress syndrome. J Thromb Haemost. 2020;18(7):1747–51. DOI: 10.1111/jth.14854.
  23. Bulanov A.Yu., Simarova I.B., Bulanova E.L. et al. New coronavirus infection COVID‐19: clinical and prognostic significance of plasma fibrinogen level. Vestnik intensivnoj terapii imeni A.I. Saltanova. 2020;(4):42–7. (In Russ). DOI: 10.21320/1818‐474X‐2020‐4‐42‐47.
  24. Iba T., Levy J.H., Levi M. et al. Coagulopathy of coronavirus disease 2019. Crit Care Med. 2020;48(9):1358–64. DOI: 10.1097/CCM.0000000000004458.
  25. Heinz C., Miesbach W., Herrmann E et al. Greater fibrinolysis resistance but no greater platelet aggregation in critically ill COVID‐19 patients. Anesthesiology. 2021;134(3):457–67. DOI: 10.1097/ALN.0000000000003685.
  26. Wright F.L., Vogler T.O., Moore E.E. et al. Fibrinolysis shutdown correlation with thromboembolic events in severe COVID‐19 infection. J Am Coll Surg. 2020;231(2):193–203.e1. DOI: 10.1016/j.jamcoll surg.2020.05.007.
  27. Mussbacher M., Salzmann M., Brostjan C. et al. Cell type‐specific roles of NF‐κB linking inflammation and thrombosis. Front Immunol. 2019;10:85. DOI: 10.3389/fimmu.2019.00085.
  28. Mackman N., Antoniak S., Wolberg A.S. et al. Coagulation abnormalities and thrombosis in patients infected with SARS‐CoV‐2 and other pandemic viruses. Arterioscler Thromb Vasc Biol. 2020;40(9):2033–44. DOI: 10.1161/ATVBAHA.120.314514.
  29. McGonagle D., Sharif K., O’Regan A., Bridgewood C. The role of cytokines including Interleukin‐6 in COVID‐19 induced pneumonia and macrophage activation syndrome‐like disease. Autoimmun Rev. 2020;19(6):102537. DOI: 10.1016/j.autrev.2020.102537. 30. Zaid Y., Puhm F., Allaeys I. et al. Platelets can associate with SARS‐CoV‐2 RNA and are hyperactivated in COVID‐19. Circ Res. 2020;127(11):1404–18. DOI: 10.1161/CIRCRESAHA.120.317703.
  30. Lim M.S., Mcrae S. COVID‐19 and immunothrombosis: Pathophysiology and therapeutic implications. Crit Rev Oncol Hematol. 2021;168:103529. DOI: 10.1016/j.critrevonc.2021.103529.
  31. Jiang L., Tang K., Levin M. et al. COVID‐19 and multisystem inflammatory syndrome in children and adolescents. Lancet Infect Dis. 2020;20(11): e276‐e288. DOI: 10.1016/S1473‐3099(20)30651‐4.
  32. Leppkes M., Knopf J., Naschberger E. et al. Vascular occlusion by neutrophil extracellular traps in COVID‐19. EBioMedicine. 2020;58:102925. DOI: 10.1016/j.ebiom.2020.102925.
  33. Middleton E.A., He X.Y., Denorme F. et al. Neutrophil extracellular traps contribute to immunothrombosis in COVID‐19 acute respiratory distress syndrome. Blood. 2020;136(10):1169–79. DOI: 10.1182/blood.2020007008.
  34. Roitman E.V. The recovery of endothelial function in novel coronavirus infection COVID‐19 (review). Meditsinskiy sovet. 2021;(14):78– 86. (In Russ.). DOI: 10.21518/2079‐701X‐2021‐14‐78‐86.
  35. Freeman T.L., Swartz T.H. Targeting the NLRP3 inflammasome in severe COVID‐19. Front Immunol. 2020;11:1518. DOI: 10.3389/ fimmu.2020.01518.
  36. Ahamed J., Laurence J. Long COVID endotheliopathy: hypothesized mechanisms and potential therapeutic approaches. J Clin Invest. 2022;132(15): e161167. DOI: 10.1172/JCI161167.
  37. Ho C.‐Y., Salimian M., Hegert J. et al. Postmortem assessment of olfactory tissue degeneration and microvasculopathy in patients with COVID‐19. JAMA Neurol. 2022;79(6):544–53. DOI: 10.1001/jamaneurol.2022.0154.
  38. Choi D., Waksman O., Shaik A. et al. Association of blood viscosity with mortality among patients hospitalized with COVID‐19. J Am Coll Cardiol. 2022;80(4):316–28. DOI: 10.1016/j.jacc.2022.04.060.
  39. Bonaventura A., Potere N. Blood hyperviscosity: A novel link between hyperinflammation and hypercoagulability in COVID‐19. J Am Coll Cardiol. 2022;80(4):329–31. DOI: 10.1016/j.jacc.2022.04.061.
  40. Interim guidelines “Prevention, diagnosis and treatment of a new coronavirus infection (COVID‐19)”. Version 17 (14.12.2022). Moscow: Ministerstvo zdravoohraneniya Rossijskoj Federacii, 2022. 260 рp. (In Russ.). Available at: https://static‐0.minzdrav.gov. ru/system/attachments/attaches/000/061/254/original/ВМР_ COVID‐19_V17.pdf?1671088207. [Accessed: 20.01.2023].
  41. Zabolotskikh I.B., Kirov M.Yu., Lebedinskii K.M. et al. Anesthesia and intensive care for patients with COVID‐19. Russian Federation of anesthesiologists and reanimatologists guidelines. Vestnik intensivnoj terapii imeni A.I. Saltanova. 2022;(1):5–140. (In Russ.). DOI: 10.21320/1818‐474X‐2022‐1‐5‐140.
  42. REMAP‐CAP Investigators; ACTIV‐4a Investigators; ATTACC Investigators et al. Therapeutic anticoagulation with heparin in critically ill patients with Covid‐19. N Engl J Med. 2021;385(9):777– 89. DOI: 10.1056/NEJMoa2103417.
  43. Spyropoulos A. C., Bonaca M. P. Studying the coagulopathy of COVID‐19. Lancet. 2022;399(10320):118–9. DOI: 10.1016/ S0140‐6736(21)01906‐1.
  44. RECOVERY Collaborative Group. Aspirin in patients admitted to hospital with COVID‐19 (RECOVERY): A randomised, controlled, open‐label, platform trial. Lancet. 2022;399(10320):143– 51. DOI: 10.1016/s0140‐6736(21)01825‐0.
  45. Desilles J.P., Di Meglio L., Delvoye F. et al. Composition and organization of acute ischemic stroke thrombus: A wealth of information for future thrombolytic strategies. Front Neurol. 2022;13:870331. DOI: 10.3389/fneur.2022.870331.
  46. Barrett C.D., Moore H.B., Moore E.E. et al. Study of alteplase for respiratory failure in SARS‐CoV‐2 COVID‐19: A vanguard multicenter, rapidly adaptive, pragmatic, randomized controlled trial. Chest. 2022;161(3):710–27. DOI: 10.1016/j.chest.2021.09.024.
  47. Raval M., Rajendran S., Stephen E. The outcome of catheterdirected thrombolysis in COVID‐19‐associated deep vein thrombosis. Vasc Endovascular Surg. 2022;56(3):258–62. DOI: 10.1177/15385744211068640.
  48. Kocas B.B., Kilickesmez K. Catheter‐directed thrombolysis in a COVID‐19 patient complicated with pulmonary embolism. Turk J Emerg Med. 2022;22(1):54–7. DOI: 10.4103/2452‐2473.336102.
  49. Pérez‐Calatayud A.A., Enriquez‐García R., Fareli‐González C. et al. In situ pulmonary thrombolysis and perfusion lung angiography in severe COVID‐19 respiratory failure. Crit Care Explor. 2022;4(4): e0670. DOI: 10.1097/CCE.0000000000000670.
  50. Sakai N., Takeuchi M., Imamura H. et al. Safety, pharmacokinetics and pharmacodynamics of DS‐1040, in combination with thrombectomy, in Japanese patients with acute ischemic stroke. Clin Drug Invest. 2022;42(2):137–49. DOI: 10.1007/s40261‐021‐01112‐8.
  51. Abdul Rahim P., Rengaswamy D. Fibrinolytic enzyme — an overview. Curr Pharm Biotechnol. 2022;23(11):1336–45. DOI: 10.2174/13 89201023666220104143113.
  52. Madonov P.G., Mishenina S.V., Kinsht D.N., Kikhtenko N.V. Targeted pharmacodynamics of subtilisins. Sibirskij nauchnyj medicinskij zhurnal. 2016;36(4):15–24. (In Russ.).
  53. Yuan L., Liangqi C., Xiyu T., Jinyao L. Biotechnology, bioengineering and applications of Bacillus nattokinase. Biomolecules. 2022;12(7):980. DOI: 10.3390/biom12070980.
  54. Wang Y., Wang H., Zhang Y. et al. Stepwise strategy to identify thrombin as a hydrolytic substrate for nattokinase. J Chem Inf Model. 2022;62(22):5780–93. DOI: 10.1021/acs.jcim.2c00978.
  55. MisheninaS.V.,MadonovP.G.,BaikalovG.I.etal.Theoralthrombolysis for venous thrombosis (clinical trial). Tromboz, gemostaz i reologiya. 2019;(4):54–67. (In Russ.). DOI: 10.25555/THR.2019.4.0900.
  56. Artamonov A.V., Bekarev A.A., Kinsht D.N. Method for treating patients with acute thrombosis of venous bed of lower extremities. Patent of the Russian Federation No. 2613155 dated March 15, 2017. Bull. No. 8. 9 pр. (In Russ.). Available at: https://patents. s3.yandex.net/RU2613155C1_20170315.pdf. [Accessed: 20.01.2023].
  57. MadonovP.G., ErshovK.I., MisheninaS.V. et al. Antithrombotic effects of combination of anticoagulant and thrombolytic in conditions of lesion to the pulmonary vascular bed in modeling systemic thrombosis. Byulleten’ medicinskoj nauki. 2021;21(1):88–93. (In Russ.).
  58. Rubio‐Rivas M., Mora‐Luján J.M., Formiga F. et al.; SEMI–COVID‐19 Network. WHO ordinal scale and inflammation risk categories in COVID‐19. Comparative study of the severity scales. J Gen Intern Med. 2022;37(8):1980–7. DOI: 10.1007/s11606‐022‐07511‐7.